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1
Kaltenpoth, Martin, and Laura V. Flórez. "Versatile and Dynamic Symbioses Between Insects and Burkholderia Bacteria." Annual Review of Entomology 65, no. 1 (January 7, 2020): 145–70. http://dx.doi.org/10.1146/annurev-ento-011019-025025.
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Symbiotic associations with microorganisms represent major sources of ecological and evolutionary innovations in insects. Multiple insect taxa engage in symbioses with bacteria of the genus Burkholderia, a diverse group that is widespread across different environments and whose members can be mutualistic or pathogenic to plants, fungi, and animals. Burkholderia symbionts provide nutritional benefits and resistance against insecticides to stinkbugs, defend Lagria beetle eggs against pathogenic fungi, and may be involved in nitrogen metabolism in ants. In contrast to many other insect symbioses, the known associations with Burkholderia are characterized by environmental symbiont acquisition or mixed-mode transmission, resulting in interesting ecological and evolutionary dynamics of symbiont strain composition. Insect– Burkholderia symbioses present valuable model systems from which to derive insights into general principles governing symbiotic interactions because they are often experimentally and genetically tractable and span a large fraction of the diversity of functions, localizations, and transmission routes represented in insect symbioses.
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Stoy, Kayla S., Joselyne Chavez, Valeria De Las Casas, Venkat Talla, Aileen Berasategui, Levi T. Morran, and Nicole M. Gerardo. "Evaluating coevolution in a horizontally transmitted mutualism." Evolution 77, no. 1 (December 8, 2022): 166–85. http://dx.doi.org/10.1093/evolut/qpac009.
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Abstract Many interspecific interactions are shaped by coevolution. Transmission mode is thought to influence opportunities for coevolution within symbiotic interactions. Vertical transmission maintains partner fidelity, increasing opportunities for coevolution, but horizontal transmission may disrupt partner fidelity, potentially reducing opportunities for coevolution. Despite these predictions, the role of coevolution in the maintenance of horizontally transmitted symbioses is unclear. Leveraging a tractable insect–bacteria symbiosis, we tested for signatures of pairwise coevolution by assessing patterns of host–symbiont specialization. If pairwise coevolution defines the interaction, we expected to observe evidence of reciprocal specialization between hosts and their local symbionts. We found no evidence for local adaptation between sympatric lineages of Anasa tristis squash bugs and Caballeronia spp. symbionts across their native geographic range. We also found no evidence for specialization between three co-localized Anasa host species and their native Caballeronia symbionts. Our results demonstrate generalist dynamics underlie the interaction between Anasa insect hosts and their Caballeronia symbionts. We predict that selection from multiple host species may favor generalist symbiont traits through diffuse coevolution. Alternatively, selection for generalist traits may be a consequence of selection by hosts for fixed cooperative symbiont traits without coevolution.
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Gundel, Pedro E., Prudence Sun, Nikki D. Charlton, Carolyn A. Young, Tom E. X. Miller, and Jennifer A. Rudgers. "Simulated folivory increases vertical transmission of fungal endophytes that deter herbivores and alter tolerance to herbivory in Poa autumnalis." Annals of Botany 125, no. 6 (February 3, 2020): 981–91. http://dx.doi.org/10.1093/aob/mcaa021.
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Abstract Background and Aims The processes that maintain variation in the prevalence of symbioses within host populations are not well understood. While the fitness benefits of symbiosis have clearly been shown to drive changes in symbiont prevalence, the rate of transmission has been less well studied. Many grasses host symbiotic fungi (Epichloë spp.), which can be transmitted vertically to seeds or horizontally via spores. These symbionts may protect plants against herbivores by producing alkaloids or by increasing tolerance to damage. Therefore, herbivory may be a key ecological factor that alters symbiont prevalence within host populations by affecting either symbiont benefits to host fitness or the symbiont transmission rate. Here, we addressed the following questions: Does symbiont presence modulate plant tolerance to herbivory? Does folivory increase symbiont vertical transmission to seeds or hyphal density in seedlings? Do plants with symbiont horizontal transmission have lower rates of vertical transmission than plants lacking horizontal transmission? Methods We studied the grass Poa autumnalis and its symbiotic fungi in the genus Epichloë. We measured plant fitness (survival, growth, reproduction) and symbiont transmission to seeds following simulated folivory in a 3-year common garden experiment and surveyed natural populations that varied in mode of symbiont transmission. Key Results Poa autumnalis hosted two Epichloë taxa, an undescribed vertically transmitted Epichloë sp. PauTG-1 and E. typhina subsp. poae with both vertical and horizontal transmission. Simulated folivory reduced plant survival, but endophyte presence increased tolerance to damage and boosted fitness. Folivory increased vertical transmission and hyphal density within seedlings, suggesting induced protection for progeny of damaged plants. Across natural populations, the prevalence of vertical transmission did not correlate with symbiont prevalence or differ with mode of transmission. Conclusions Herbivory not only mediated the reproductive fitness benefits of symbiosis, but also promoted symbiosis prevalence by increasing vertical transmission of the fungus to the next generation. Our results reveal a new mechanism by which herbivores could influence the prevalence of microbial symbionts in host populations.
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Ferrari, Julia, and Fabrice Vavre. "Bacterial symbionts in insects or the story of communities affecting communities." Philosophical Transactions of the Royal Society B: Biological Sciences 366, no. 1569 (May 12, 2011): 1389–400. http://dx.doi.org/10.1098/rstb.2010.0226.
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Bacterial symbionts are widespread in insects and other animals. Most of them are predominantly vertically transmitted, along with their hosts' genes, and thus extend the heritable genetic variation present in one species. These passengers have a variety of repercussions on the host's phenotypes: besides the cost imposed on the host for maintaining the symbiont population, they can provide fitness advantages to the host or manipulate the host's reproduction. We argue that insect symbioses are ideal model systems for community genetics. First, bacterial symbionts directly or indirectly affect the interactions with other species within a community. Examples include their involvement in modifying the use of host plants by phytophagous insects, in providing resistance to natural enemies, but also in reducing the global genetic diversity or gene flow between populations within some species. Second, one emerging picture in insect symbioses is that many species are simultaneously infected with more than one symbiont, which permits studying the factors that shape bacterial communities; for example, horizontal transmission, interactions between host genotype, symbiont genotype and the environment and interactions among symbionts. One conclusion is that insects' symbiotic complements are dynamic communities that affect and are affected by the communities in which they are embedded.
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Cheng, D. J., and R. F. Hou. "Histological observations on transovarial transmission of a yeast-like symbiote in Nilaparvata lugens Stal (Homoptera, Delphacidae)." Tissue and Cell 33, no. 3 (June 2001): 273–79. http://dx.doi.org/10.1054/tice.2001.0173.
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Acar, Tessa, Sandra Moreau, Marie-Françoise Jardinaud, Gabriella Houdinet, Felicia Maviane-Macia, Frédéric De Meyer, Bart Hoste, et al. "The association between Dioscorea sansibarensis and Orrella dioscoreae as a model for hereditary leaf symbiosis." PLOS ONE 19, no. 4 (April 22, 2024): e0302377. http://dx.doi.org/10.1371/journal.pone.0302377.
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Hereditary, or vertically-transmitted, symbioses affect a large number of animal species and some plants. The precise mechanisms underlying transmission of functions of these associations are often difficult to describe, due to the difficulty in separating the symbiotic partners. This is especially the case for plant-bacteria hereditary symbioses, which lack experimentally tractable model systems. Here, we demonstrate the potential of the leaf symbiosis between the wild yam Dioscorea sansibarensis and the bacterium Orrella dioscoreae (O. dioscoreae) as a model system for hereditary symbiosis. O. dioscoreae is easy to grow and genetically manipulate, which is unusual for hereditary symbionts. These properties allowed us to design an effective antimicrobial treatment to rid plants of bacteria and generate whole aposymbiotic plants, which can later be re-inoculated with bacterial cultures. Aposymbiotic plants did not differ morphologically from symbiotic plants and the leaf forerunner tip containing the symbiotic glands formed normally even in the absence of bacteria, but microscopic differences between symbiotic and aposymbiotic glands highlight the influence of bacteria on the development of trichomes and secretion of mucilage. This is to our knowledge the first leaf symbiosis where both host and symbiont can be grown separately and where the symbiont can be genetically altered and reintroduced to the host.
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Salem, Hassan, Laura Florez, Nicole Gerardo, and Martin Kaltenpoth. "An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects." Proceedings of the Royal Society B: Biological Sciences 282, no. 1804 (April 7, 2015): 20142957. http://dx.doi.org/10.1098/rspb.2014.2957.
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Across animals and plants, numerous metabolic and defensive adaptations are a direct consequence of symbiotic associations with beneficial microbes. Explaining how these partnerships are maintained through evolutionary time remains one of the central challenges within the field of symbiosis research. While genome erosion and co-cladogenesis with the host are well-established features of symbionts exhibiting intracellular localization and transmission, the ecological and evolutionary consequences of an extracellular lifestyle have received little attention, despite a demonstrated prevalence and functional importance across many host taxa. Using insect–bacteria symbioses as a model, we highlight the diverse routes of extracellular symbiont transfer. Extracellular transmission routes are unified by the common ability of the bacterial partners to survive outside their hosts, thereby imposing different genomic, metabolic and morphological constraints than would be expected from a strictly intracellular lifestyle. We emphasize that the evolutionary implications of symbiont transmission routes (intracellular versus extracellular) do not necessarily correspond to those of the transmission mode (vertical versus horizontal), a distinction of vital significance when addressing the genomic and physiological consequences for both host and symbiont.
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Boyd, Bret M., Julie M. Allen, Ryuichi Koga, Takema Fukatsu, Andrew D. Sweet, Kevin P. Johnson, and David L. Reed. "Two Bacterial Genera, Sodalis and Rickettsia, Associated with the Seal Louse Proechinophthirus fluctus (Phthiraptera: Anoplura)." Applied and Environmental Microbiology 82, no. 11 (March 18, 2016): 3185–97. http://dx.doi.org/10.1128/aem.00282-16.
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ABSTRACTRoughly 10% to 15% of insect species host heritable symbiotic bacteria known as endosymbionts. The lice parasitizing mammals rely on endosymbionts to provide essential vitamins absent in their blood meals. Here, we describe two bacterial associates from a louse,Proechinophthirus fluctus, which is an obligate ectoparasite of a marine mammal. One of these is a heritable endosymbiont that is not closely related to endosymbionts of other mammalian lice. Rather, it is more closely related to endosymbionts of the genusSodalisassociated with spittlebugs and feather-chewing bird lice. Localization and vertical transmission of this endosymbiont are also more similar to those of bird lice than to those of other mammalian lice. The endosymbiont genome appears to be degrading in symbiosis; however, it is considerably larger than the genomes of other mammalian louse endosymbionts. These patterns suggest the possibility that thisSodalisendosymbiont might be recently acquired, replacing a now-extinct, ancient endosymbiont. From the same lice, we also identified an abundant bacterium belonging to the genusRickettsiathat is closely related toRickettsia ricketsii, a human pathogen vectored by ticks. No obvious masses of theRickettsiabacterium were observed in louse tissues, nor did we find any evidence of vertical transmission, so the nature of its association remains unclear.IMPORTANCEMany insects are host to heritable symbiotic bacteria. These heritable bacteria have been identified from numerous species of parasitic lice. It appears that novel symbioses have formed between lice and bacteria many times, with new bacterial symbionts potentially replacing existing ones. However, little was known about the symbionts of lice parasitizing marine mammals. Here, we identified a heritable bacterial symbiont in lice parasitizing northern fur seals. This bacterial symbiont appears to have been recently acquired by the lice. The findings reported here provide insights into how new symbioses form and how this lifestyle is shaping the symbiont genome.
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Russell, S. L., E. McCartney, and C. M. Cavanaugh. "Transmission strategies in a chemosynthetic symbiosis: detection and quantification of symbionts in host tissues and their environment." Proceedings of the Royal Society B: Biological Sciences 285, no. 1890 (October 31, 2018): 20182157. http://dx.doi.org/10.1098/rspb.2018.2157.
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Transmission of bacteria vertically through host tissues ensures offspring acquire symbionts; however, horizontal transmission is an effective strategy for many associations and plays a role in some vertically transmitted symbioses. The bivalve Solemya velum and its gammaproteobacterial chemosynthetic symbionts exhibit evolutionary evidence of both transmission modes, but the dominant strategy on an ecological time scale is unknown. To address this, a specific primer set was developed and validated for the S. velum symbiont using a novel workflow called specific marker design (SMD). Symbionts were quantified in spawned eggs and sediment and seawater samples from S. velum habitats with qPCR. Each egg was estimated to contain 50–100 symbiont genomes. By contrast, symbiont DNA was found at low abundance/occurrence in sediment and seawater, often co-occurring with host mitochondrial DNA, obscuring its origin. To ascertain when eggs become infected, histological sections of S. velum tissues were labelled for symbiont 16S rRNA via in situ hybridization. This revealed symbionts in the ovary walls and mature oocytes, suggesting association in late oogenesis. These data support the hypothesis that S. velum symbionts are vertically transmitted every host generation, thus genetic signatures of horizontal transmission are driven by ecologically infrequent events. This knowledge furthers our understanding of vertical and horizontal mode integration and provides insights across animal–bacterial chemosynthetic symbioses.
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Ciche, Todd A., Kwi-suk Kim, Bettina Kaufmann-Daszczuk, Ken C. Q. Nguyen, and David H. Hall. "Cell Invasion and Matricide during Photorhabdus luminescens Transmission by Heterorhabditis bacteriophora Nematodes." Applied and Environmental Microbiology 74, no. 8 (February 15, 2008): 2275–87. http://dx.doi.org/10.1128/aem.02646-07.
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ABSTRACT Many animals and plants have symbiotic relationships with beneficial bacteria. Experimentally tractable models are necessary to understand the processes involved in the selective transmission of symbiotic bacteria. One such model is the transmission of the insect-pathogenic bacterial symbionts Photorhabdus spp. by Heterorhabditis bacteriophora infective juvenile (IJ)-stage nematodes. By observing egg-laying behavior and IJ development, it was determined that IJs develop exclusively via intrauterine hatching and matricide (i.e., endotokia matricida). By transiently exposing nematodes to fluorescently labeled symbionts, it was determined that symbionts infect the maternal intestine as a biofilm and then invade and breach the rectal gland epithelium, becoming available to the IJ offspring developing in the pseudocoelom. Cell- and stage-specific infection occurs again in the pre-IJ pharyngeal intestinal valve cells, which helps symbionts to persist as IJs develop and move to a new host. Synchronous with nematode development are changes in symbiont and host behavior (e.g., adherence versus invasion). Thus, Photorhabdus symbionts are maternally transmitted by an elaborate infectious process involving multiple selective steps in order to achieve symbiont-specific transmission.
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Hayashi, Toshinari, Takahiro Hosokawa, Xian-Ying Meng, Ryuichi Koga, and Takema Fukatsu. "Female-Specific Specialization of a Posterior End Region of the Midgut Symbiotic Organ in Plautia splendens and Allied Stinkbugs." Applied and Environmental Microbiology 81, no. 7 (January 30, 2015): 2603–11. http://dx.doi.org/10.1128/aem.04057-14.
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ABSTRACTMany stinkbugs (Insecta: Hemiptera: Heteroptera) are associated with bacterial symbionts in a posterior region of the midgut. In these stinkbugs, adult females excrete symbiont-containing materials from the anus for transmission of the beneficial symbionts to their offspring. For ensuring the vertical symbiont transmission, a variety of female-specific elaborate traits at the cellular, morphological, developmental, and behavioral levels have been reported from diverse stinkbugs of the families Plataspidae, Urostylididae, Parastrachiidae, etc. Meanwhile, such elaborate female-specific traits for vertical symbiont transmission have been poorly characterized for the largest and economically important stinkbug family Pentatomidae. Here, we investigated the midgut symbiotic system of a pentatomid stinkbug,Plautia splendens. A specific gammaproteobacterial symbiont was consistently present extracellularly in the cavity of numerous crypts arranged in four rows on the midgut fourth section. The symbiont was smeared on the egg surface upon oviposition by adult females, orally acquired by newborn nymphs, and thereby transmitted vertically to the next generation and important for growth and survival of the host insects. We found that, specifically in adult females, several rows of crypts at the posterior end region of the symbiotic midgut were morphologically differentiated and conspicuously enlarged, often discharging the symbiotic bacteria from the crypt cavity to the main tract of the symbiotic midgut. The female-specific enlarged end crypts were also found in other pentatomid stinkbugsPlautia staliandCarbula crassiventris. These results suggest that the enlarged end crypts represent a female-specific specialized morphological trait for vertical symbiont transmission commonly found among stinkbugs of the family Pentatomidae.
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Chen, Jason Z., Zeeyong Kwong, Nicole M. Gerardo, and Nic M. Vega. "Ecological drift during colonization drives within-host and between-host heterogeneity in an animal-associated symbiont." PLOS Biology 22, no. 4 (April 25, 2024): e3002304. http://dx.doi.org/10.1371/journal.pbio.3002304.
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Specialized host–microbe symbioses canonically show greater diversity than expected from simple models, both at the population level and within individual hosts. To understand how this heterogeneity arises, we utilize the squash bug, Anasa tristis, and its bacterial symbionts in the genus Caballeronia. We modulate symbiont bottleneck size and inoculum composition during colonization to demonstrate the significance of ecological drift, the noisy fluctuations in community composition due to demographic stochasticity. Consistent with predictions from the neutral theory of biodiversity, we found that ecological drift alone can account for heterogeneity in symbiont community composition between hosts, even when 2 strains are nearly genetically identical. When acting on competing strains, ecological drift can maintain symbiont genetic diversity among different hosts by stochastically determining the dominant strain within each host. Finally, ecological drift mediates heterogeneity in isogenic symbiont populations even within a single host, along a consistent gradient running the anterior-posterior axis of the symbiotic organ. Our results demonstrate that symbiont population structure across scales does not necessarily require host-mediated selection, as it can emerge as a result of ecological drift acting on both isogenic and unrelated competitors. Our findings illuminate the processes that might affect symbiont transmission, coinfection, and population structure in nature, which can drive the evolution of host–microbe symbioses and microbe–microbe interactions within host-associated microbiomes.
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Werth, Silke, and Christoph Scheidegger. "Congruent Genetic Structure in the Lichen-Forming Fungus Lobaria pulmonaria and Its Green-Algal Photobiont." Molecular Plant-Microbe Interactions® 25, no. 2 (February 2012): 220–30. http://dx.doi.org/10.1094/mpmi-03-11-0081.
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The extent of codispersal of symbionts is one of the key factors shaping genetic structures of symbiotic organisms. Concordant patterns of genetic structure are expected in vertically transmitted symbioses, whereas horizontal transmission generally uncouples genetic structures unless the partners are coadapted. Here, we compared the genetic structures of mutualists, the lichen-forming fungus Lobaria pulmonaria and its primary green-algal photobiont, Dictyochloropsis reticulata. We performed analysis of molecular variance and variogram analysis to compare genetic structures between symbiosis partners. We simulated the expected number of multilocus-genotype recurrences to reveal whether the distribution of multilocus genotypes of either species was concordant with panmixia. Simulations and tests of linkage disequilibrium provided compelling evidence for the codispersal of mutualists. To test whether genotype associations between symbionts were consistent with randomness, as expected under horizontal transmission, we simulated the recurrence of fungal-algal multilocus genotype associations expected by chance. Our data showed nonrandom associations of fungal and algal genotypes. Either vertical transmission or horizontal transmission coupled with coadaptation between symbiont genotypes may have created these nonrandom associations. This study is among the first to show codispersal and highly congruent genetic structures in the partners of a lichen mutualism.
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Ikuta, Tetsuro, Kanae Igawa, Akihiro Tame, Tsuneyoshi Kuroiwa, Haruko Kuroiwa, Yui Aoki, Yoshihiro Takaki, et al. "Surfing the vegetal pole in a small population: extracellular vertical transmission of an 'intracellular' deep-sea clam symbiont." Royal Society Open Science 3, no. 5 (May 2016): 160130. http://dx.doi.org/10.1098/rsos.160130.
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Symbiont transmission is a key event for understanding the processes underlying symbiotic associations and their evolution. However, our understanding of the mechanisms of symbiont transmission remains still fragmentary. The deep-sea clam Calyptogena okutanii harbours obligate sulfur-oxidizing intracellular symbiotic bacteria in the gill epithelial cells. In this study, we determined the localization of their symbiont associating with the spawned eggs, and the population size of the symbiont transmitted via the eggs. We show that the symbionts are located on the outer surface of the egg plasma membrane at the vegetal pole, and that each egg carries approximately 400 symbiont cells, each of which contains close to 10 genomic copies. The very small population size of the symbiont transmitted via the eggs might narrow the bottleneck and increase genetic drift, while polyploidy and its transient extracellular lifestyle might slow the rate of genome reduction. Additionally, the extracellular localization of the symbiont on the egg surface may increase the chance of symbiont exchange. This new type of extracellular transovarial transmission provides insights into complex interactions between the host and symbiont, development of both host and symbiont, as well as the population dynamics underlying genetic drift and genome evolution in microorganisms.
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Drew, Georgia C., Giles E. Budge, Crystal L. Frost, Peter Neumann, Stefanos Siozios, Orlando Yañez, and Gregory D. D. Hurst. "Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts." ISME Journal 15, no. 10 (May 3, 2021): 2956–68. http://dx.doi.org/10.1038/s41396-021-00977-z.
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AbstractA dynamic continuum exists from free-living environmental microbes to strict host-associated symbionts that are vertically inherited. However, knowledge of the forces that drive transitions in symbiotic lifestyle and transmission mode is lacking. Arsenophonus is a diverse clade of bacterial symbionts, comprising reproductive parasites to coevolving obligate mutualists, in which the predominant mode of transmission is vertical. We describe a symbiosis between a member of the genus Arsenophonus and the Western honey bee. The symbiont shares common genomic and predicted metabolic properties with the male-killing symbiont Arsenophonus nasoniae, however we present multiple lines of evidence that the bee Arsenophonus deviates from a heritable model of transmission. Field sampling uncovered spatial and seasonal dynamics in symbiont prevalence, and rapid infection loss events were observed in field colonies and laboratory individuals. Fluorescent in situ hybridisation showed Arsenophonus localised in the gut, and detection was rare in screens of early honey bee life stages. We directly show horizontal transmission of Arsenophonus between bees under varying social conditions. We conclude that honey bees acquire Arsenophonus through a combination of environmental exposure and social contacts. These findings uncover a key link in the Arsenophonus clades trajectory from free-living ancestral life to obligate mutualism, and provide a foundation for studying transitions in symbiotic lifestyle.
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Nováková, Eva, Filip Husník, Eva Šochová, and Václav Hypša. "Arsenophonus and Sodalis Symbionts in Louse Flies: an Analogy to the Wigglesworthia and Sodalis System in Tsetse Flies." Applied and Environmental Microbiology 81, no. 18 (July 6, 2015): 6189–99. http://dx.doi.org/10.1128/aem.01487-15.
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ABSTRACTSymbiosis between insects and bacteria result in a variety of arrangements, genomic modifications, and metabolic interconnections. Here, we present genomic, phylogenetic, and morphological characteristics of a symbiotic system associated withMelophagus ovinus, a member of the blood-feeding family Hippoboscidae. The system comprises four unrelated bacteria representing different stages in symbiosis evolution, from typical obligate mutualists inhabiting bacteriomes to freely associated commensals and parasites. Interestingly, the whole system provides a remarkable analogy to the association betweenGlossinaand its symbiotic bacteria. In both, the symbiotic systems are composed of an obligate symbiont and two facultative intracellular associates,SodalisandWolbachia. In addition, extracellularBartonellaresides in the gut ofMelophagus. However, the phylogenetic origins of the two obligate mutualist symbionts differ. InGlossina, the mutualisticWigglesworthiaappears to be a relatively isolated symbiotic lineage, whereas inMelophagus, the obligate symbiont originated within the widely distributedArsenophonuscluster. Although phylogenetically distant, the two obligate symbionts display several remarkably similar traits (e.g., transmission via the host's “milk glands” or similar pattern of genome reduction). To obtain better insight into the biology and possible role of theM. ovinusobligate symbiont, “CandidatusArsenophonus melophagi,” we performed several comparisons of its gene content based on assignments of the Cluster of Orthologous Genes (COG). Using this criterion, we show that within a set of 44 primary and secondary symbionts, “Ca. Arsenophonus melophagi” is most similar toWigglesworthia. On the other hand, these two bacteria also display interesting differences, such as absence of flagellar genes inArsenophonusand their presence inWigglesworthia. This finding implies that a flagellum is not essential for bacterial transmission via milk glands.
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Sipe, Alison R., Ami E. Wilbur, and S. Craig Cary. "Bacterial Symbiont Transmission in the Wood-Boring Shipworm Bankia setacea (Bivalvia: Teredinidae)." Applied and Environmental Microbiology 66, no. 4 (April 1, 2000): 1685–91. http://dx.doi.org/10.1128/aem.66.4.1685-1691.2000.
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ABSTRACT The Teredinidae (shipworms) are a morphologically diverse group of marine wood-boring bivalves that are responsible each year for millions of dollars of damage to wooden structures in estuarine and marine habitats worldwide. They exist in a symbiosis with cellulolytic nitrogen-fixing bacteria that provide the host with the necessary enzymes for survival on a diet of wood cellulose. These symbiotic bacteria reside in distinct structures lining the interlamellar junctions of the gill. This study investigated the mode by which these nutritionally essential bacterial symbionts are acquired in the teredinid Bankia setacea. Through 16S ribosomal DNA (rDNA) sequencing, the symbiont residing within the B. setaceagill was phylogenetically characterized and shown to be distinct from previously described shipworm symbionts. In situ hybridization using symbiont-specific 16S rRNA-directed probes bound to bacterial ribosome targets located within the host gill coincident with the known location of the gill symbionts. These specific probes were then used as primers in a PCR-based assay which consistently detected bacterial rDNA in host gill (symbiont containing), gonad tissue, and recently spawned eggs, demonstrating the presence of symbiont cells in host ovary and offspring. These results suggest that B. setacea ensures successful inoculation of offspring through a vertical mode of symbiont transmission and thereby enables a broad distribution of larval settlement.
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Luan, Jun-Bo. "Insect Bacteriocytes: Adaptation, Development, and Evolution." Annual Review of Entomology 69, no. 1 (January 25, 2024): 81–98. http://dx.doi.org/10.1146/annurev-ento-010323-124159.
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Bacteriocytes are host cells specialized to harbor symbionts in certain insect taxa. The adaptation, development, and evolution of bacteriocytes underlie insect symbiosis maintenance. Bacteriocytes carry enriched host genes of insect and bacterial origin whose transcription can be regulated by microRNAs, which are involved in host–symbiont metabolic interactions. Recognition proteins of peptidoglycan, the bacterial cell wall component, and autophagy regulate symbiont abundance in bacteriocytes. Horizontally transferred genes expressed in bacteriocytes influence the metabolism of symbiont peptidoglycan, which may affect the bacteriocyte immune response against symbionts. Bacteriocytes release or transport symbionts into ovaries for symbiont vertical transmission. Bacteriocyte development and death, regulated by transcriptional factors, are variable in different insect species. The evolutionary origin of insect bacteriocytes remains unclear. Future research should elucidate bacteriocyte cell biology, the molecular interplay between bacteriocyte metabolic and immune functions, the genetic basis of bacteriocyte origin, and the coordination between bacteriocyte function and host biology in diverse symbioses.
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Szklarzewicz, Teresa, Katarzyna Michalik, Beata Grzywacz, Małgorzata Kalandyk-Kołodziejczyk, and Anna Michalik. "Fungal Associates of Soft Scale Insects (Coccomorpha: Coccidae)." Cells 10, no. 8 (July 29, 2021): 1922. http://dx.doi.org/10.3390/cells10081922.
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Ophiocordyceps fungi are commonly known as virulent, specialized entomopathogens; however, recent studies indicate that fungi belonging to the Ophiocordycypitaceae family may also reside in symbiotic interaction with their host insect. In this paper, we demonstrate that Ophiocordyceps fungi may be obligatory symbionts of sap-sucking hemipterans. We investigated the symbiotic systems of eight Polish species of scale insects of Coccidae family: Parthenolecanium corni, Parthenolecanium fletcheri, Parthenolecanium pomeranicum, Psilococcus ruber, Sphaerolecanium prunasti, Eriopeltis festucae, Lecanopsis formicarum and Eulecanium tiliae. Our histological, ultrastructural and molecular analyses showed that all these species host fungal symbionts in the fat body cells. Analyses of ITS2 and Beta-tubulin gene sequences, as well as fluorescence in situ hybridization, confirmed that they should all be classified to the genus Ophiocordyceps. The essential role of the fungal symbionts observed in the biology of the soft scale insects examined was confirmed by their transovarial transmission between generations. In this paper, the consecutive stages of fungal symbiont transmission were analyzed under TEM for the first time.
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Jäckle, Oliver, Brandon K. B. Seah, Målin Tietjen, Nikolaus Leisch, Manuel Liebeke, Manuel Kleiner, Jasmine S. Berg, and Harald R. Gruber-Vodicka. "Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatwormParacatenula." Proceedings of the National Academy of Sciences 116, no. 17 (April 8, 2019): 8505–14. http://dx.doi.org/10.1073/pnas.1818995116.
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Hosts of chemoautotrophic bacteria typically have much higher biomass than their symbionts and consume symbiont cells for nutrition. In contrast to this, chemoautotrophicCandidatusRiegeria symbionts in mouthlessParacatenulaflatworms comprise up to half of the biomass of the consortium. Each species ofParacatenulaharbors a specificCa. Riegeria, and the endosymbionts have been vertically transmitted for at least 500 million years. Such prolonged strict vertical transmission leads to streamlining of symbiont genomes, and the retained physiological capacities reveal the functions the symbionts provide to their hosts. Here, we studied a species ofParacatenulafrom Sant’Andrea, Elba, Italy, using genomics, gene expression, imaging analyses, as well as targeted and untargeted MS. We show that its symbiont,Ca. R. santandreae has a drastically smaller genome (1.34 Mb) than the symbiont´s free-living relatives (4.29–4.97 Mb) but retains a versatile and energy-efficient metabolism. It encodes and expresses a complete intermediary carbon metabolism and enhanced carbon fixation through anaplerosis and accumulates massive intracellular inclusions such as sulfur, polyhydroxyalkanoates, and carbohydrates. Compared with symbiotic and free-living chemoautotrophs,Ca. R. santandreae’s versatility in energy storage is unparalleled in chemoautotrophs with such compact genomes. Transmission EM as well as host and symbiont expression data suggest thatCa. R. santandreae largely provisions its host via outer-membrane vesicle secretion. With its high share of biomass in the symbiosis and large standing stocks of carbon and energy reserves, it has a unique role for bacterial symbionts—serving as the primary energy storage for its animal host.
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Gehrer, Lukas, and Christoph Vorburger. "Parasitoids as vectors of facultative bacterial endosymbionts in aphids." Biology Letters 8, no. 4 (March 14, 2012): 613–15. http://dx.doi.org/10.1098/rsbl.2012.0144.
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Heritable bacterial endosymbionts play an important role in aphid ecology. Sequence-based evidence suggests that facultative symbionts such as Hamiltonella defensa or Regiella insecticola also undergo horizontal transmission. Other than through male-to-female transfer during the sexual generation in autumn, the routes by which this occurs remain largely unknown. Here, we tested if parasitoids or ectoparasitic mites can act as vectors for horizontal transfer of facultative symbionts. Using symbiont-specific primers for diagnostic PCR, we demonstrate for the first time, to our knowledge, that parasitoids can indeed transfer H. defensa and R. insecticola by sequentially stabbing infected and uninfected individuals of their host, Aphis fabae , establishing new, heritable infections. Thus, a natural route of horizontal symbiont transmission is also available during the many clonal generations of the aphid life cycle. No transmissions by ectoparasitic mites were observed, nor did parasitoids that emerged from symbiont-infected aphids transfer any symbionts in our experiments.
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Shan, Hongwei, Wei Wu, Zongtao Sun, Jianping Chen, and Hongjie Li. "The Gut Microbiota of the Insect Infraorder Pentatomomorpha (Hemiptera: Heteroptera) for the Light of Ecology and Evolution." Microorganisms 9, no. 2 (February 23, 2021): 464. http://dx.doi.org/10.3390/microorganisms9020464.
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The stinkbugs of the infraorder Pentatomomorpha are a group of important plant sap-feeding insects, which host diverse microorganisms. Some are located in their complex morphological midgut compartments, while some within the specialized bacteriomes of insect hosts. This perpetuation of symbioses through host generations is reinforced via the diverse routes of vertical transmission or environmental acquisition of the symbionts. These symbiotic partners, reside either through the extracellular associations in midgut or intracellular associations in specialized cells, not only have contributed nutritional benefits to the insect hosts but also shaped their ecological and evolutionary basis. The stinkbugs and gut microbe symbioses present a valuable model that provides insights into symbiotic interactions between agricultural insects and microorganisms and may become potential agents for insect pest management.
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McCuaig, Bonita, France Liboiron, and Suzanne C. Dufour. "The bivalveThyasiracf.gouldihosts chemoautotrophic symbiont populations with strain level diversity." PeerJ 5 (July 26, 2017): e3597. http://dx.doi.org/10.7717/peerj.3597.
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Invertebrates from various marine habitats form nutritional symbioses with chemosynthetic bacteria. In chemosynthetic symbioses, both the mode of symbiont transmission and the site of bacterial housing can affect the composition of the symbiont population. Vertically transmitted symbionts, as well as those hosted intracellularly, are more likely to form clonal populations within their host. Conversely, symbiont populations that are environmentally acquired and extracellular may be more likely to be heterogeneous/mixed within host individuals, as observed in some mytilid bivalves. The symbionts of thyasirid bivalves are also extracellular, but limited 16S rRNA sequencing data suggest that thyasirid individuals contain uniform symbiont populations. In a recent study,Thyasiracf.gouldiindividuals from Bonne Bay, Newfoundland, Canada were found to host one of three 16S rRNA phylotypes of sulfur-oxidizing gammaproteobacteria, suggesting environmental acquisition of symbionts and some degree of site-specificity. Here, we use Sanger sequencing of both 16S RNA and the more variable ribulose-1,5-bisphosphate carboxylase (RuBisCO) PCR products to further examineThyasiracf.gouldisymbiont diversity at the scale of host individuals, as well as to elucidate any temporal or spatial patterns in symbiont diversity within Bonne Bay, and relationships with host OTU or size. We obtained symbiont 16S rRNA and RuBisCO Form II sequences from 54 and 50 host individuals, respectively, during nine sampling trips to three locations over four years. Analyses uncovered the same three closely related 16S rRNA phylotypes obtained previously, as well as three divergent RuBisCO phylotypes; these were found in various pair combinations within host individuals, suggesting incidents of horizontal gene transfer during symbiont evolution. While we found no temporal patterns in phylotype distribution or relationships with host OTU or size, some spatial effects were noted, with some phylotypes only found within particular sampling sites. The sequencing also revealed symbiont populations within individual hosts that appeared to be a mixture of different phylotypes, based on multiple base callings at divergent sites. This work provides further evidence thatThyasiracf.gouldiacquires its symbionts from the environment, and supports the theory that hosts can harbour symbiont populations consisting of multiple, closely related bacterial phylotypes.
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Itoh, Hideomi, Manabu Aita, Atsushi Nagayama, Xian-Ying Meng, Yoichi Kamagata, Ronald Navarro, Tomoyuki Hori, Satoru Ohgiya, and Yoshitomo Kikuchi. "Evidence of Environmental and Vertical Transmission of Burkholderia Symbionts in the Oriental Chinch Bug, Cavelerius saccharivorus (Heteroptera: Blissidae)." Applied and Environmental Microbiology 80, no. 19 (July 18, 2014): 5974–83. http://dx.doi.org/10.1128/aem.01087-14.
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ABSTRACTThe vertical transmission of symbiotic microorganisms is omnipresent in insects, while the evolutionary process remains totally unclear. The oriental chinch bug,Cavelerius saccharivorus(Heteroptera: Blissidae), is a serious sugarcane pest, in which symbiotic bacteria densely populate the lumen of the numerous tubule-like midgut crypts that the chinch bug develops. Cloning and sequence analyses of the 16S rRNA genes revealed that the crypts were dominated by a specific group of bacteria belonging to the genusBurkholderiaof theBetaproteobacteria. TheBurkholderiasequences were distributed into three distinct clades: theBurkholderia cepaciacomplex (BCC), the plant-associated beneficial and environmental (PBE) group, and the stinkbug-associated beneficial and environmental group (SBE). Diagnostic PCR revealed that only one of the three groups ofBurkholderiawas present in ∼89% of the chinch bug field populations tested, while infections with multipleBurkholderiagroups within one insect were observed in only ∼10%. Deep sequencing of the 16S rRNA gene confirmed that theBurkholderiabacteria specifically colonized the crypts and were dominated by one of threeBurkholderiagroups. The lack of phylogenetic congruence between the symbiont and the host population strongly suggested host-symbiont promiscuity, which is probably caused by environmental acquisition of the symbionts by some hosts. Meanwhile, inspections of eggs and hatchlings by diagnostic PCR and egg surface sterilization demonstrated that almost 30% of the hatchlings vertically acquire symbioticBurkholderiavia symbiont-contaminated egg surfaces. The mixed strategy of symbiont transmission found in the oriental chinch bug might be an intermediate stage in evolution from environmental acquisition to strict vertical transmission in insects.
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Caro, Audrey, Patrice Got, Marc Bouvy, Marc Troussellier, and Olivier Gros. "Effects of Long-Term Starvation on a Host Bivalve (Codakia orbicularis, Lucinidae) and Its Symbiont Population." Applied and Environmental Microbiology 75, no. 10 (April 3, 2009): 3304–13. http://dx.doi.org/10.1128/aem.02659-08.
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ABSTRACT The bivalve Codakia orbicularis, hosting sulfur-oxidizing gill endosymbionts, was starved (in artificial seawater filtered through a 0.22-μm-pore-size membrane) for a long-term experiment (4 months). The effects of starvation were observed using transmission electron microscopy, fluorescence in situ hybridization and catalyzed reporter deposition (CARD-FISH), and flow cytometry to monitor the anatomical and physiological modifications in the gill organization of the host and in the symbiotic population housed in bacteriocytes. The abundance of the symbiotic population decreased through starvation, with a loss of one-third of the bacterial population each month, as shown by CARD-FISH. At the same time, flow cytometry revealed significant changes in the physiology of symbiotic cells, with a decrease in cell size and modifications to the nucleic acid content, while most of the symbionts maintained a high respiratory activity (measured using the 5-cyano-2,3-ditolyl tetrazolium chloride method). Progressively, the number of symbiont subpopulations was reduced, and the subsequent multigenomic state, characteristic of this symbiont in freshly collected clams, turned into one and five equivalent genome copies for the two remaining subpopulations after 3 months. Concomitant structural modifications appeared in the gill organization. Lysosymes became visible in the bacteriocytes, while large symbionts disappeared, and bacteriocytes were gradually replaced by granule cells throughout the entire lateral zone. Those data suggested that host survival under these starvation conditions was linked to symbiont digestion as the main nutritional source.
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Duperron, Sébastien, Thierry Nadalig, Jean-Claude Caprais, Myriam Sibuet, Aline Fiala-Médioni, Rudolf Amann, and Nicole Dubilier. "Dual Symbiosis in a Bathymodiolus sp. Mussel from a Methane Seep on the Gabon Continental Margin (Southeast Atlantic): 16S rRNA Phylogeny and Distribution of the Symbionts in Gills." Applied and Environmental Microbiology 71, no. 4 (April 2005): 1694–700. http://dx.doi.org/10.1128/aem.71.4.1694-1700.2005.
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ABSTRACT Deep-sea mussels of the genus Bathymodiolus (Bivalvia: Mytilidae) harbor symbiotic bacteria in their gills and are among the dominant invertebrate species at cold seeps and hydrothermal vents. An undescribed Bathymodiolus species was collected at a depth of 3,150 m in a newly discovered cold seep area on the southeast Atlantic margin, close to the Zaire channel. Transmission electron microscopy, comparative 16S rRNA analysis, and fluorescence in situ hybridization indicated that this Bathymodiolus sp. lives in a dual symbiosis with sulfide- and methane-oxidizing bacteria. A distinct distribution pattern of the symbiotic bacteria in the gill epithelium was observed, with the thiotrophic symbiont dominating the apical region and the methanotrophic symbiont more abundant in the basal region of the bacteriocytes. No variations in this distribution pattern or in the relative abundances of the two symbionts were observed in mussels collected from three different mussel beds with methane concentrations ranging from 0.7 to 33.7 μM. The 16S rRNA sequence of the methanotrophic symbiont is most closely related to those of known methanotrophic symbionts from other bathymodiolid mussels. Surprisingly, the thiotrophic Bathymodiolus sp. 16S rRNA sequence does not fall into the monophyletic group of sequences from thiotrophic symbionts of all other Bathymodiolus hosts. While these mussel species all come from vents, this study describes the first thiotrophic sequence from a seep mussel and shows that it is most closely related (99% sequence identity) to an environmental clone sequence obtained from a hydrothermal plume near Japan.
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Gerardo, Nicole M., Kim L. Hoang, and Kayla S. Stoy. "Evolution of animal immunity in the light of beneficial symbioses." Philosophical Transactions of the Royal Society B: Biological Sciences 375, no. 1808 (August 10, 2020): 20190601. http://dx.doi.org/10.1098/rstb.2019.0601.
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Immune system processes serve as the backbone of animal defences against pathogens and thus have evolved under strong selection and coevolutionary dynamics. Most microorganisms that animals encounter, however, are not harmful, and many are actually beneficial. Selection should act on hosts to maintain these associations while preventing exploitation of within-host resources. Here, we consider how several key aspects of beneficial symbiotic associations may shape host immune system evolution. When host immunity is used to regulate symbiont populations, there should be selection to evolve and maintain targeted immune responses that recognize symbionts and suppress but not eliminate symbiont populations. Associating with protective symbionts could relax selection on the maintenance of redundant host-derived immune responses. Alternatively, symbionts could facilitate the evolution of host immune responses if symbiont-conferred protection allows for persistence of host populations that can then adapt. The trajectory of immune system evolution will likely differ based on the type of immunity involved, the symbiont transmission mode and the costs and benefits of immune system function. Overall, the expected influence of beneficial symbiosis on immunity evolution depends on how the host immune system interacts with symbionts, with some interactions leading to constraints while others possibly relax selection on immune system maintenance. This article is part of the theme issue ‘The role of the microbiome in host evolution’.
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Kashkouli, M., Y. Fathipour, and M. Mehrabadi. "Habitat visualization, acquisition features and necessity of the gammaproteobacterial symbiont of pistachio stink Bug, Acrosternum heegeri (Hem.: Pentatomidae)." Bulletin of Entomological Research 110, no. 1 (June 13, 2019): 22–33. http://dx.doi.org/10.1017/s0007485319000245.
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AbstractPlant-sucking stinkbugs are especially associated with mutualistic gut bacterial symbionts. Here, we explored the symbiotic relationship of a pistachio stinkbug, Acrosternum heegeri Fieber by histological, fluorescence in situ hybridization (FISH), real-time PCR and molecular phylogenetic techniques. Furthermore, the effects of the symbiont on the resting/wandering behaviors of the newborn nymphs, pre-adult survival rates, and stage compositions were investigated. Transmission electron microscopy and real-time PCR analyses showed that a rod-shaped gammaproteobacterium was persistently located within the posterior midgut crypts. Molecular phylogenetic and FISH techniques strongly suggested that this symbiont should be placed in the genus Pantoea of the Enterobacteriales. Scanning electron microscopy confirmed the presence of the bacterial cells on the egg surface which the surface sterilization of the eggs resulted in the successful removal of the symbiont from the eggs. Symbiotic and aposymbiotic A. heegeri showed no significant differences in the wandering behaviors of the first nymphal stages, while the symbiont-free insects suffered retarded growth and lower survivability. Together, the results highlight the habitat and acquisition features of Pantoea symbiont and its contribution in A. heegeri biology that might help us for better pest management in the future.
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Latorre, Amparo, Rebeca Domínguez-Santos, Carlos García-Ferris, and Rosario Gil. "Of Cockroaches and Symbionts: Recent Advances in the Characterization of the Relationship between Blattella germanica and Its Dual Symbiotic System." Life 12, no. 2 (February 15, 2022): 290. http://dx.doi.org/10.3390/life12020290.
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Mutualistic stable symbioses are widespread in all groups of eukaryotes, especially in insects, where symbionts have played an essential role in their evolution. Many insects live in obligate relationship with different ecto- and endosymbiotic bacteria, which are needed to maintain their hosts’ fitness in their natural environment, to the point of even relying on them for survival. The case of cockroaches (Blattodea) is paradigmatic, as both symbiotic systems coexist in the same organism in two separated compartments: an intracellular endosymbiont (Blattabacterium) inside bacteriocytes located in the fat body, and a rich and complex microbiota in the hindgut. The German cockroach Blattella germanica is a good model for the study of symbiotic interactions, as it can be maintained in the laboratory in controlled populations, allowing the perturbations of the two symbiotic systems in order to study the communication and integration of the tripartite organization of the host–endosymbiont–microbiota, and to evaluate the role of symbiotic antimicrobial peptides (AMPs) in host control over their symbionts. The importance of cockroaches as reservoirs and transmission vectors of antibiotic resistance sequences, and their putative interest to search for AMPs to deal with the problem, is also discussed.
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Kashkouli, Marzieh, Yaghoub Fathipour, and Mohammad Mehrabadi. "Heritable Gammaproteobacterial Symbiont Improves the Fitness of Brachynema germari Kolenati (Hemiptera: Pentatomidae)." Environmental Entomology 48, no. 5 (July 30, 2019): 1079–87. http://dx.doi.org/10.1093/ee/nvz089.
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Abstract The pistachio green stink bug, Brachynema germari Kolenati, is an abundant and economic insect pest in most pistachio-growing regions. Some physiological and ecological features of this pest have been studied, but the microbiological nature of symbiotic bacteria and biological aspects of this host–symbiont interaction have been poorly understood. In the present study, we explored the host-associated environment, phylogeny, and acquisition features of the bacterial symbiont of the insect. Furthermore, the importance of the symbiont on the biological (i.e., lifespan, stage composition, and body weight) and behavioral characteristics (i.e., resting/wandering behaviors of the newborn nymphs) of the host were investigated. We found that a rod-shaped gammaproteobacterium was persistently colonized the fourth midgut region of the insect. Molecular phylogenetic and fluorescence in situ hybridization analyses strongly suggest that this symbiont should be placed in the genus Pantoea of the Enterobacteriales. Egg surface sterilization resulted in the aposymbiotic insects suggesting the vertical transmission of symbiont via egg surface smearing upon oviposition. Symbiotic and aposymbiotic B. germari showed no significant differences in the wandering behaviors of the first nymphal stages, whereas the symbiont-free insects exhibited retarded growth, lower longevity, and adult body weight. Taken together, these data provide a better understanding of the relationship between the bacterial symbiont and B. germari and demonstrate that the insect is heavily affected by the deprival of its gut symbionts.
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Koga, Ryuichi, Masahiko Tanahashi, Naruo Nikoh, Takahiro Hosokawa, Xian-Ying Meng, Minoru Moriyama, and Takema Fukatsu. "Host’s guardian protein counters degenerative symbiont evolution." Proceedings of the National Academy of Sciences 118, no. 25 (June 14, 2021): e2103957118. http://dx.doi.org/10.1073/pnas.2103957118.
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Microbial symbioses significantly contribute to diverse organisms, where long-lasting associations tend to result in symbiont genome erosion, uncultivability, extinction, and replacement. How such inherently deteriorating symbiosis can be harnessed to stable partnership is of general evolutionary interest. Here, we report the discovery of a host protein essential for sustaining symbiosis. Plataspid stinkbugs obligatorily host an uncultivable and genome-reduced gut symbiont, Ishikawaella. Upon oviposition, females deposit “capsules” for symbiont delivery to offspring. Within the capsules, the fragile symbiotic bacteria survive the harsh conditions outside the host until acquired by newborn nymphs to establish vertical transmission. We identified a single protein dominating the capsule content, which is massively secreted by female-specific intestinal organs, embedding the symbiont cells, and packaged into the capsules. Knockdown of the protein resulted in symbiont degeneration, arrested capsule production, symbiont transmission failure, and retarded nymphal growth, unveiling its essential function for ensuring symbiont survival and vertical transmission. The protein originated from a lineage of odorant-binding protein-like multigene family, shedding light on the origin of evolutionary novelty regarding symbiosis. Experimental suppression of capsule production extended the female’s lifespan, uncovering a substantial cost for maintaining symbiosis. In addition to the host’s guardian protein, the symbiont’s molecular chaperone, GroEL, was overproduced in the capsules, highlighting that the symbiont’s eroding functionality is compensated for by stabilizer molecules of host and symbiont origins. Our finding provides insight into how intimate host–symbiont associations can be maintained over evolutionary time despite the symbiont’s potential vulnerability to degeneration and malfunctioning.
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Gordon, Eric Robert Lucien, Quinn McFrederick, and Christiane Weirauch. "Phylogenetic Evidence for Ancient and Persistent Environmental Symbiont Reacquisition in Largidae (Hemiptera: Heteroptera)." Applied and Environmental Microbiology 82, no. 24 (September 30, 2016): 7123–33. http://dx.doi.org/10.1128/aem.02114-16.
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ABSTRACTThe insect order Hemiptera, one of the best-studied insect lineages with respect to bacterial symbioses, still contains major branches that lack comprehensive characterization of associated bacterial symbionts. The Pyrrhocoroidea (Largidae [220 species] and Pyrrhocoridae [∼300 species]) is a clade of the hemipteran infraorder Pentatomomorpha. Studies on bacterial symbionts of this group have focused on members of Pyrrhocoridae, but recent examination of species of two genera of Largidae demonstrated divergent symbiotic complexes in these putative sister families. We surveyed the associated bacterial diversity of this group using paired-end Illumina sequencing and targeted Sanger sequencing of bacterial 16S rRNA amplicons of 30 pyrrhocoroid taxa, including 17 species of Largidae, in order to determine bacterial associates and the similarity of associated microbial communities among species. We also used molecular data (4,800 bp in 5 loci, for 57 ingroup and 12 outgroup taxa) to infer a phylogeny of the host superfamily, in order to trace the evolution of symbiotic complexes among Pentatomomorpha species. We undertook multiple lines of investigation (i.e., experimental rearing, fluorescencein situhybridization microscopy, and phylogenetic and coevolutionary analyses) to elucidate potential transmission routes for largid symbionts. We found a prevalent and specific association of Largidae withBurkholderiastrains of the plant-associated beneficial and environmental clade, housed in midgut tubules. As in other distantly related Heteroptera, symbiotic bacteria seem to be acquired from the environment every generation. We review the current understanding of symbiotic complexes within Pentatomomorpha and discuss means to further investigate the evolution and function of these symbioses.IMPORTANCEObligate symbioses with bacteria are common in insects, particularly Hemiptera, in which various forms of symbiosis occur. However, knowledge regarding symbionts remains incomplete for major hemipteran lineages. Thus, an accurate understanding of how these partnerships evolved and changed over millions of years is not yet achievable. We contribute to our understanding of the evolution of symbiotic complexes in Hemiptera by characterizing bacterial associates of Pyrrhocoroidea, focusing on the family Largidae. Members of Largidae are associated with specific symbioticBurkholderiastrains from a different clade thanBurkholderiasymbionts in otherBurkholderia-associated Hemiptera. Evidence suggests that species of Largidae reacquire specific symbiotic bacteria from the environment every generation, which is a rare strategy for insects, with potentially volatile evolutionary ramifications, but one that must have persisted in Largidae and related lineages since their origin in the Cretaceous Period.
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Chepkemoi, Sharon T., Enock Mararo, Hellen Butungi, Juan Paredes, Daniel K. Masiga, Steven P. Sinkins, and Jeremy K. Herren. "Identification of Spiroplasma insolitum symbionts in Anopheles gambiae." Wellcome Open Research 2 (September 26, 2017): 90. http://dx.doi.org/10.12688/wellcomeopenres.12468.1.
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Background: Insect symbionts have the potential to block the transmission of vector-borne diseases by their hosts. The advancement of a symbiont-based transmission blocking strategy for malaria requires the identification and study of Anopheles symbionts. Methods: High throughput 16S amplicon sequencing was used to profile the bacteria associated with Anopheles gambiae sensu lato and identify potential symbionts. The polymerase chain reaction (PCR) with specific primers were subsequently used to monitor symbiont prevalence in field populations, as well as symbiont transmission patterns. Results: We report the discovery of the bacterial symbiont, Spiroplasma, in Anopheles gambiae in Kenya. We determine that geographically dispersed Anopheles gambiae populations in Kenya are infected with Spiroplasma at low prevalence levels. Molecular phylogenetics indicates that this Anopheles gambiae associated Spiroplasma is a member of the insolitum clade. We demonstrate that this symbiont is stably maternally transmitted across at least two generations and does not significantly affect the fecundity or egg to adult survival of its host. Conclusions: In diverse insect species, Spiroplasma has been found to render their host resistant to infection by pathogens. The identification of a maternally transmitted strain of Spiroplasma in Anopheles gambiae may therefore open new lines of investigation for the development of symbiont-based strategies for blocking malaria transmission.
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Skelton, James, Robert P. Creed, and Bryan L. Brown. "A symbiont's dispersal strategy: condition-dependent dispersal underlies predictable variation in direct transmission among hosts." Proceedings of the Royal Society B: Biological Sciences 282, no. 1819 (November 22, 2015): 20152081. http://dx.doi.org/10.1098/rspb.2015.2081.
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Direct horizontal transmission of pathogenic and mutualistic symbionts has profound consequences for host and symbiont fitness alike. While the importance of contact rates for transmission is widely recognized, the processes that underlie variation in transmission during contact are rarely considered. Here, we took a symbiont's perspective of transmission as a form of dispersal and adopted the concept of condition-dependent dispersal strategies from the study of free-living organisms to understand and predict variation in transmission in the cleaning symbiosis between crayfish and ectosymbiotic branchiobdellidan worms. Field study showed that symbiont reproductive success was correlated with host size and competition among worms for microhabitats. Laboratory experiments demonstrated high variability in transmission among host contacts. Moreover, symbionts were more likely to disperse when host size and competition for microhabitat created a fitness environment below a discrete minimum threshold. A predictive model based on a condition-dependent symbiont dispersal strategy correctly predicted transmission in 95% of experimental host encounters and the exact magnitude of transmission in 67%, both significantly better than predictions that assumed a fixed transmission rate. Our work provides a dispersal-based understanding of symbiont transmission and suggests adaptive symbiont dispersal strategies can explain variation in transmission dynamics and complex patterns of host infection.
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Lorion, Julien, Sébastien Duperron, Olivier Gros, Corinne Cruaud, and Sarah Samadi. "Several deep-sea mussels and their associated symbionts are able to live both on wood and on whale falls." Proceedings of the Royal Society B: Biological Sciences 276, no. 1654 (September 16, 2008): 177–85. http://dx.doi.org/10.1098/rspb.2008.1101.
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Bathymodiolin mussels occur at hydrothermal vents and cold seeps, where they thrive thanks to symbiotic associations with chemotrophic bacteria. Closely related genera Idas and Adipicola are associated with organic falls, ecosystems that have been suggested as potential evolutionary ‘stepping stones’ in the colonization of deeper and more sulphide-rich environments. Such a scenario should result from specializations to given environments from species with larger ecological niches. This study provides molecular-based evidence for the existence of two mussel species found both on sunken wood and bones. Each species specifically harbours one bacterial phylotype corresponding to thioautotrophic bacteria related to other bathymodiolin symbionts. Phylogenetic patterns between hosts and symbionts are partially congruent. However, active endocytosis and occurrences of minor symbiont lineages within species which are not their usual host suggest an environmental or horizontal rather than strictly vertical transmission of symbionts. Although the bacteria are close relatives, their localization is intracellular in one mussel species and extracellular in the other, suggesting that habitat choice is independent of the symbiont localization. The variation of bacterial densities in host tissues is related to the substrate on which specimens were sampled and could explain the abilities of host species to adapt to various substrates.
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Espada-Hinojosa, Salvador, Judith Drexel, Julia Kesting, Edwin Kniha, Iason Pifeas, Lukas Schuster, Jean-Marie Volland, Helena C. Zambalos, and Monika Bright. "Host-symbiont stress response to lack-of-sulfide in the giant ciliate mutualism." PLOS ONE 17, no. 2 (February 25, 2022): e0254910. http://dx.doi.org/10.1371/journal.pone.0254910.
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The mutualism between the thioautotrophic bacterial ectosymbiont Candidatus Thiobius zoothamnicola and the giant ciliate Zoothamnium niveum thrives in a variety of shallow-water marine environments with highly fluctuating sulfide emissions. To persist over time, both partners must reproduce and ensure the transmission of symbionts before the sulfide stops, which enables carbon fixation of the symbiont and nourishment of the host. We experimentally investigated the response of this mutualism to depletion of sulfide. We found that colonies released some initially present but also newly produced macrozooids until death, but in fewer numbers than when exposed to sulfide. The symbionts on the colonies proliferated less without sulfide, and became larger and more rod-shaped than symbionts from freshly collected colonies that were exposed to sulfide and oxygen. The symbiotic monolayer was severely disturbed by growth of other microbes and loss of symbionts. We conclude that the response of both partners to the termination of sulfide emission was remarkably quick. The development and the release of swarmers continued until host died and thus this behavior contributed to the continuation of the association.
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Kenkel, Carly D., and Line K. Bay. "Exploring mechanisms that affect coral cooperation: symbiont transmission mode, cell density and community composition." PeerJ 6 (December 3, 2018): e6047. http://dx.doi.org/10.7717/peerj.6047.
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The coral symbiosis is the linchpin of the reef ecosystem, yet the mechanisms that promote and maintain cooperation between hosts and symbionts have not been fully resolved. We used a phylogenetically controlled design to investigate the role of vertical symbiont transmission, an evolutionary mechanism in which symbionts are inherited directly from parents, predicted to enhance cooperation and holobiont fitness. Six species of coral, three vertical transmitters and their closest horizontally transmitting relatives, which exhibit environmental acquisition of symbionts, were fragmented and subjected to a 2-week thermal stress experiment. Symbiont cell density, photosynthetic function and translocation of photosynthetically fixed carbon between symbionts and hosts were quantified to assess changes in physiological performance and cooperation. All species exhibited similar decreases in symbiont cell density and net photosynthesis in response to elevated temperature, consistent with the onset of bleaching. Yet baseline cooperation, or translocation of photosynthate, in ambient conditions and the reduction in cooperation in response to elevated temperature differed among species. Although Porites lobata and Galaxea acrhelia did exhibit the highest levels of baseline cooperation, we did not observe universally higher levels of cooperation in vertically transmitting species. Post hoc sequencing of the Symbiodinium ITS-2 locus was used to investigate the potential role of differences in symbiont community composition. Interestingly, reductions in cooperation at the onset of bleaching tended to be associated with increased symbiont community diversity among coral species. The theoretical benefits of evolving vertical transmission are based on the underlying assumption that the host-symbiont relationship becomes genetically uniform, thereby reducing competition among symbionts. Taken together, our results suggest that it may not be vertical transmission per se that influences host-symbiont cooperation, but genetic uniformity of the symbiont community, although additional work is needed to test this hypothesis.
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Coomans, August, Myriam Claeys, and Tom T. M. Vandekerckhove. "Transovarial transmission of symbionts in Xiphinema brevicollum (Nematoda: Longidoridae)." Nematology 2, no. 4 (2000): 443–49. http://dx.doi.org/10.1163/156854100509303.
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AbstractTransovarial transmission of bacterial symbionts in Xiphinema brevicollum was examined by means of electron microscopical- and fluorescence microscopical observations of intra-uterine and freshly laid non-embryonated eggs, as well as of embryonated eggs. The symbionts are mainly aggregated near one of the egg poles and this is observed in non-embryonated as well as in embryonated eggs. The bacteria are present in intestinal cells of first stage juveniles that are still enclosed by the egg-shell. In subsequent juvenile developmental stages their number increases and the intestinal cells are filled with the symbionts. Bacteria were not present in the genital primordium. It is hypothesised that the aggregated symbionts at one of the egg poles become enclosed in the E founder cell during embryogenesis and subsequently are distributed to the endodermal daughter cells. The bacteria become enclosed in the ovarial wall through an unknown mechanism only during the later stages of gonad development. Transmission transovarienne des symbiontes de Xiphinema brevicollum (Nematoda: Longidoridae) - La transmission transovarienne des symbiontes bactériens de Xiphinema brevicollum a été étudiée par observations en microscopie électronique et à fluorescence d'œufs non embryonnés, encore contenus dans l'utérus ou fraichement pondus, et d'œufs embryonnés. Les symbiontes sont en majorité agrégés à l'un des pôles de l'œuf, que celui-ci soit embryonné ou non. Les bactéries sont présentes dans les cellules intestinales du premier stade juvénile encore contenu à l'intérieur de la coque de l'œuf. Chez les stades juvéniles ultérieurs leur nombre croît et les cellules intestinales sont remplies de symbiontes. Ces bactéries sont absentes du primordium génital. L'hypothèse est avancée que les symbiontes agrégés à l'un des pôles de l'œuf se retrouvent, au cours de l'embryogenèse, dans la cellule fondatrice E et sont par la suite répartis dans les cellules endodermiques filles. Les bactéries ne se retrouvent dans la paroi ovarienne que lors des derniers stades du développement de la gonade par un mécanisme encore inconnu.
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Zhang, Yan Kai, and Jing Ze Liu. "Maternally inherited symbiotic bacteria in ticks: incidence and biological importance." Systematic and Applied Acarology 24, no. 1 (January 29, 2019): 158. http://dx.doi.org/10.11158/saa.24.1.12.
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Ticks are exclusive blood-feeding parasites that are of medical and veterinary importance. Ticks are also host for several maternally inherited symbiotic bacteria that are non-pathogenic bacteria and have potential roles in tick biology and the transmission of co-infecting pathogens. In order to gain a comprehensive view of these symbionts in ticks, we overviewed their incidence and biological importance within ticks based on available data. The symbionts in ticks are diverse, and their incidence and frequency vary across different tick species and different geographical populations of the same species. In some cases, symbionts of Coxiella, Francisella and Rickettsia genera may provide tick hosts essential nutrients absent from the exclusive food source of ticks and exhibit mutualistic relationships with their hosts. However, most symbionts are facultative and affect the biological phenotypes of their tick hosts through various ways. For some strains of Coxiella and Francisella, advanced genomic data and phylogenetic investigations have revealed their interactions with hosts and their evolutionary transitions of pathogenic and mutualistic forms. These findings are valuable for understanding tick-symbiont associations, and may help to develop new strategies to control ticks and tick-borne diseases.
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Sina, Haziz, Kamirou Chabi-Sika, Razaki Ossè, Akim Socohou, Ibrahim A. Abibou, Hafiz Salami, Germain Gil Padonou, Adolphe Adjanonhoun, and Lamine Baba-Moussa. "Bacteria Load Determination of the Intestinal Microbiota and Identification of Spiroplasma and Wolbachia in Anopheles gambiae." International Journal of Zoology 2022 (July 19, 2022): 1–9. http://dx.doi.org/10.1155/2022/1491648.
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The gut microbiota of mosquitoes is composed of a range of microorganisms. Among its microorganisms, some affect the vectorial capacity of mosquitoes. The aim of this study was to characterize some bacteria of the intestinal microbiota in Anopheles gambiae (An. gambiae) females, a major vector of malaria transmission in Benin. The symbiote bacteria of the microbiota of female laboratory An. gambiae and female wild An. gambiae were identified by the culture method. The count was done on media plate count agar (PCA), and subsequently, the bacterial load was calculated. Comparison of batches bacterial load was carried out with the variance analysis test (ANOVA). Finally, polymerase chain reaction (PCR) was performed to investigate the presence of a few bacterial genera influencing the vector capacity of An. gambiae. The study found that the microbiota of female An. gambiae is home to the bacteria belonging to the Staphylococcus, Enterobacteriaceae, and other unidentified bacterial gene regardless of its nature and condition. Similarly, there was no statistically significant difference between the bacterial load of the laboratory and wild mosquitoes depending on the parous and gorged states; on the other hand, there was a significant difference between the bacterial loads of the laboratory and wild mosquitoes according to the nulliparous and nongorged states. The search for a few bacterial genera influencing the vector capacity of female An. gambiae has been negative for Spiroplasma bacteria regardless of its nature and condition. PCR revealed the presence of Wolbachia bacteria for only gorged Kisumu sensitive An. gambiae. Wolbachia’s presence at An. gambiae suggests that this type of bacteria could be used to develop new effective and sustainable approaches in the vector control.
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Enríquez, Susana, Eugenio R. Méndez, Ove Hoegh-Guldberg, and Roberto Iglesias-Prieto. "Key functional role of the optical properties of coral skeletons in coral ecology and evolution." Proceedings of the Royal Society B: Biological Sciences 284, no. 1853 (April 26, 2017): 20161667. http://dx.doi.org/10.1098/rspb.2016.1667.
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Multiple scattering of light on coral skeleton enhances light absorption efficiency of coral symbionts and plays a key role in the regulation of their internal diffuse light field. To understand the dependence of this enhancement on skeleton meso- and macrostructure, we analysed the scattering abilities of naked coral skeletons for 74 Indo-Pacific species. Sensitive morphotypes to thermal and light stress, flat-extraplanate and branching corals, showed the most efficient structures, while massive-robust species were less efficient. The lowest light-enhancing scattering abilities were found for the most primitive colonial growth form: phaceloid. Accordingly, the development of highly efficient light-collecting structures versus the selection of less efficient but more robust holobionts to cope with light stress may constitute a trade-off in the evolution of modern symbiotic scleractinian corals, characterizing two successful adaptive solutions. The coincidence of the most important structural modifications with epitheca decline supports the importance of the enhancement of light transmission across coral skeleton in modern scleractinian diversification, and the central role of these symbioses in the design and optimization of coral skeleton. Furthermore, the same ability that lies at the heart of the success of symbiotic corals as coral-reef-builders can also explain the ‘Achilles's heel’ of these symbioses in a warming ocean.
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Wu, Wei, Jia-Ning Lei, Qianzhuo Mao, Yan-Zhen Tian, Hong-Wei Shan, and Jian-Ping Chen. "Distribution, Vertical Transmission, and Cooperative Mechanisms of Obligate Symbiotic Bacteria in the Leafhopper Maiestas dorsalis (Hemiptera, Cicadellidea)." Insects 14, no. 8 (August 14, 2023): 710. http://dx.doi.org/10.3390/insects14080710.
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Many insects rely on ancient symbiotic bacterial associations for essential nutrition. Auchenorrhyncha commonly harbor two obligate symbionts: Sulcia (Bacteroidetes) and a proteobacterial partner that supplies essential amino acids lacking in their plant-sap diets. In this study focusing on Maiestas dorsalis, we investigated the distribution and vertical transmission of two obligate symbiotic bacteria, Sulcia and Nasuia, within the leafhopper. Sulcia primarily inhabits the external region of the bacteriome, while Nasuia is restricted to the internal region. Both symbionts progressively infiltrate the ovary through the epithelial plug, ultimately reaching the developing primary oocyte. Furthermore, co-phylogenetic analysis suggests a close correlation between the evolution of Auchenorrhyncha insects and the presence of their obligate symbiotic bacteria. Genomic analysis further unveiled the extreme genome reduction of the obligate symbiotic bacteria, with Sulcia retaining genes involved in basic cellular processes and limited energy synthesis, while Nasuia exhibited further gene loss in replication, transcription, translation, and energy synthesis. However, both symbionts retained the genes for synthesizing the essential amino acids required by the host insect. Our study highlights the coevolutionary dynamics between Sulcia, proteobacterial partners, and their insect hosts, shedding light on the intricate nutritional interactions and evolutionary adaptations in Auchenorrhyncha insects.
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Ranger, Christopher M., Peter H. W. Biedermann, Vipaporn Phuntumart, Gayathri U. Beligala, Satyaki Ghosh, Debra E. Palmquist, Robert Mueller, et al. "Symbiont selection via alcohol benefits fungus farming by ambrosia beetles." Proceedings of the National Academy of Sciences 115, no. 17 (April 9, 2018): 4447–52. http://dx.doi.org/10.1073/pnas.1716852115.
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Animal–microbe mutualisms are typically maintained by vertical symbiont transmission or partner choice. A third mechanism, screening of high-quality symbionts, has been predicted in theory, but empirical examples are rare. Here we demonstrate that ambrosia beetles rely on ethanol within host trees for promoting gardens of their fungal symbiont and producing offspring. Ethanol has long been known as the main attractant for many of these fungus-farming beetles as they select host trees in which they excavate tunnels and cultivate fungal gardens. More than 300 attacks by Xylosandrus germanus and other species were triggered by baiting trees with ethanol lures, but none of the foundresses established fungal gardens or produced broods unless tree tissues contained in vivo ethanol resulting from irrigation with ethanol solutions. More X. germanus brood were also produced in a rearing substrate containing ethanol. These benefits are a result of increased food supply via the positive effects of ethanol on food-fungus biomass. Selected Ambrosiella and Raffaelea fungal isolates from ethanol-responsive ambrosia beetles profited directly and indirectly by (i) a higher biomass on medium containing ethanol, (ii) strong alcohol dehydrogenase enzymatic activity, and (iii) a competitive advantage over weedy fungal garden competitors (Aspergillus, Penicillium) that are inhibited by ethanol. As ambrosia fungi both detoxify and produce ethanol, they may maintain the selectivity of their alcohol-rich habitat for their own purpose and that of other ethanol-resistant/producing microbes. This resembles biological screening of beneficial symbionts and a potentially widespread, unstudied benefit of alcohol-producing symbionts (e.g., yeasts) in other microbial symbioses.
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Usher, Kayley M., David C. Sutton, Simon Toze, John Kuo, and Jane Fromont. "Inter-generational transmission of microbial symbionts in the marine sponge Chondrilla australiensis (Demospongiae)." Marine and Freshwater Research 56, no. 2 (2005): 125. http://dx.doi.org/10.1071/mf04304.
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Mechanisms for the biparental transmission of microbial symbionts to offspring in the marine sponge Chondrilla australiensis are reported. The observation of microbial mutualists in the sperm of C. australiensis is the first report of this kind in any organism, as far as we are aware. The developing eggs were shown by transmission electron microscopy (TEM) to incorporate intercellular cyanobacterial and bacterial symbionts. Nurse cells appeared to transport cyanobacterial symbionts from the surface layers of the sponge to eggs deeper in the matrix, where they were incorporated into the egg cytoplasm prior to spawning. This suggests that a host mechanism exists to actively recognise and incorporate symbionts, ensuring that larvae contain these mutualists before settlement. In addition, an average of 1.64% of mature sperm of C. australiensis contained cyanobacterial symbionts in their cytoplasm. The successful transmission of cyanobacterial symbionts to larvae was demonstrated by autofluorescent microscopy and TEM. The occurrence of organisms with functional mechanisms for transmission of symbionts from both parents to offspring provides the potential for new insights into the nature of host–symbiont interactions.
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Gibson, Cara M., and Martha S. Hunter. "Negative Fitness Consequences and Transmission Dynamics of a Heritable Fungal Symbiont of a Parasitic Wasp." Applied and Environmental Microbiology 75, no. 10 (March 13, 2009): 3115–19. http://dx.doi.org/10.1128/aem.00361-09.
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ABSTRACT Heritable bacterial symbionts are widespread in insects and can have many important effects on host ecology and fitness. Fungal symbionts are also important in shaping their hosts' behavior, interactions, and evolution, but they have been largely overlooked. Experimental tests to determine the relevance of fungal symbionts to their insect hosts are currently extremely rare, and to our knowledge, there have been no such tests for strictly predacious insects. We investigated the fitness consequences for a parasitic wasp (Comperia merceti) of an inherited fungal symbiont in the Saccharomycotina (Ascomycota) that was long presumed to be a mutualist. In comparisons of wasp lines with and without this symbiont, we found no evidence of mutualism. Instead, there were significant fitness costs to the wasps in the presence of the yeast; infected wasps attacked fewer hosts and had longer development times. We also examined the relative competitive abilities of the larval progeny of infected and uninfected mothers, as well as horizontal transmission of the fungal symbiont among larval wasps that shared a single host cockroach egg case. We found no difference in larval competitive ability when larvae whose infection status differed shared a single host. We did find high rates of horizontal transmission of the fungus, and we suggest that this transmission is likely responsible for the maintenance of this infection in wasp populations.
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Voth, Peter D., Linah Mairura, Ben E. Lockhart, and Georgiana May. "Phylogeography of Ustilago maydis virus H1 in the USA and Mexico." Journal of General Virology 87, no. 11 (November 1, 2006): 3433–41. http://dx.doi.org/10.1099/vir.0.82149-0.
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Ustilago maydis virus H1 (Umv-H1) is a mycovirus that infects Ustilago maydis, a fungal pathogen of maize. As Zea mays was domesticated, it carried with it many associated symbionts, such that the subsequent range expansion and cultivation of maize should have affected maize symbionts' evolutionary history dramatically. Because transmission of Umv-H1 takes place only through cytoplasmic fusion during mating of U. maydis individuals, the population dynamics of U. maydis and maize are expected to affect the population structure of the viral symbiont strongly. Here, the impact of changes in the evolutionary history of U. maydis on that of Umv-H1 was investigated. The high mutation rate of this virus allows inferences to be made about the evolution and divergence of Umv-H1 lineages as a result of the recent changes in U. maydis geographical and genetic structure. The phylogeographical history and genetic structure of Umv-H1 populations in the USA and Mexico were determined by using analyses of viral nucleotide sequence variation. Infection and recombination frequencies, genetic diversity and rates of neutral evolution were also assessed, to make inferences regarding evolutionary processes underlying the population genetic structure of ancestral and descendent populations. The results suggest that Mexico represents the ancestral population of Umv-H1, from which the virus has been carried with U. maydis populations into the USA. Thus, the population dynamics of one symbiont represent a major evolutionary force on the co-evolutionary dynamics of symbiotic partners.
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Fernández-González, Sofía, Antón Pérez-Rodríguez, Heather C. Proctor, Iván De la Hera, and Javier Pérez-Tris. "High diversity and low genetic structure of feather mites associated with a phenotypically variable bird host." Parasitology 145, no. 9 (January 17, 2018): 1243–50. http://dx.doi.org/10.1017/s0031182017002360.
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AbstractObligate symbionts may be genetically structured among host individuals and among phenotypically distinct host populations. Such processes may in turn determine within-host genetic diversity of symbionts, which is relevant for understanding symbiont population dynamics. We analysed the population genetic structure of two species of feather mites (Proctophyllodes sylviae and Trouessartia bifurcata) in migratory and resident blackcaps Sylvia atricapilla that winter sympatrically. Resident and migratory hosts may provide mites with habitats of different qualities, what might promote specialization of mite populations. We found high genetic diversity of within-host populations for both mite species, but no sign of genetic structure of mites between migratory and resident hosts. Our results suggest that, although dispersal mechanisms between hosts during the non-breeding season are unclear, mite populations are not limited by transmission bottlenecks that would reduce genetic diversity among individuals that share a host. Additionally, there is no evidence that host phenotypic divergence (associated with the evolution of migration and residency) has promoted the evolution of host-specialist mite populations. Unrestricted dispersal among host types may allow symbiotic organisms to avoid inbreeding and to persist in the face of habitat heterogeneity in phenotypically diverse host populations.
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Zhou, G., H. Huang, J. Lian, C. Zhang, and X. Li. "Habitat correlation of Symbiodinium diversity in two reef-building coral species in an upwelling region, eastern Hainan Island, China." Journal of the Marine Biological Association of the United Kingdom 92, no. 6 (October 21, 2011): 1309–16. http://dx.doi.org/10.1017/s0025315411001548.
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Reef-building corals are fundamental to the most diverse marine ecosystems, and the coral–dinoflagellate (zooxanthellae) associations on fine scale remains largely unknown. Spatial variation in the diversity of symbiotic dinoflagellates of two scleractinian coral species was studied in an upwelling region near Qinlan Harbor in eastern Hainan Island, China. Results showed that stress-tolerant Symbiodinium trenchi in individual colonies of Galaxea fascicularis occurred more frequently in shallow back-reef than in deep fore-reef. The higher symbiont diversity was found in colonies of G. fascicularis in shallow and close to the harbour mouth whereas the coral Pocillipora damicornis always harboured Symbiodinium internal transcribed spacer 2 (ITS2) types C1c or C42a. Furthermore, both corals were found to simultaneously contain Symbiodinium ITS2 types belonging to two distinct phylogenetic clades (C and D). This indicates that the distribution of genetically distinct Symbiodinium may correlate with light regime and possibly temperature in some (but not all) colonies at particular locations, which we interpret as holobiont acclimation to the local environmental conditions. Therefore, we conclude that reef-building corals can adapt to the local environment by harbouring genetically distinct symbionts but depend on their respective symbiont transmission modes.
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Won, Yong-Jin, Steven J. Hallam, Gregory D. O'Mullan, Irvin L. Pan, Kurt R. Buck, and Robert C. Vrijenhoek. "Environmental Acquisition of Thiotrophic Endosymbionts by Deep-Sea Mussels of the Genus Bathymodiolus." Applied and Environmental Microbiology 69, no. 11 (November 2003): 6785–92. http://dx.doi.org/10.1128/aem.69.11.6785-6792.2003.
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ABSTRACT Deep-sea Bathymodiolus mussels, depending on species and location, have the capacity to host sulfur-oxidizing (thiotrophic) and methanotrophic eubacteria in gill bacteriocytes, although little is known about the mussels' mode of symbiont acquisition. Previous studies of Bathymodiolus host and symbiont relationships have been based on collections of nonoverlapping species across wide-ranging geographic settings, creating an apparent model for vertical transmission. We present genetic and cytological evidence for the environmental acquisition of thiotrophic endosymbionts by vent mussels from the Mid-Atlantic Ridge. Open pit structures in cell membranes of the gill surface revealed likely sites for endocytosis of free-living bacteria. A population genetic analysis of the thiotrophic symbionts exploited a hybrid zone where two Bathymodiolus species intergrade. Northern Bathymodiolus azoricus and southern Bathymodiolus puteoserpentis possess species-specific DNA sequences that identify both their symbiont strains (internal transcribed spacer regions) and their mitochondria (ND4). However, the northern and southern symbiont-mitochondrial pairs were decoupled in the hybrid zone. Such decoupling of symbiont-mitochondrial pairs would not occur if the two elements were transmitted strictly vertically through the germ line. Taken together, these findings are consistent with an environmental source of thiotrophic symbionts in Bathymodiolus mussels, although an environmentally “leaky” system of vertical transmission could not be excluded.
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Koga, Ryuichi, Minoru Moriyama, Naoko Onodera-Tanifuji, Yoshiko Ishii, Hiroki Takai, Masaki Mizutani, Kohei Oguchi, et al. "Single mutation makes Escherichia coli an insect mutualist." Nature Microbiology 7, no. 8 (August 4, 2022): 1141–50. http://dx.doi.org/10.1038/s41564-022-01179-9.
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AbstractMicroorganisms often live in symbiosis with their hosts, and some are considered mutualists, where all species involved benefit from the interaction. How free-living microorganisms have evolved to become mutualists is unclear. Here we report an experimental system in which non-symbiotic Escherichia coli evolves into an insect mutualist. The stinkbug Plautia stali is typically associated with its essential gut symbiont, Pantoea sp., which colonizes a specialized symbiotic organ. When sterilized newborn nymphs were infected with E. coli rather than Pantoea sp., only a few insects survived, in which E. coli exhibited specific localization to the symbiotic organ and vertical transmission to the offspring. Through transgenerational maintenance with P. stali, several hypermutating E. coli lines independently evolved to support the host’s high adult emergence and improved body colour; these were called ‘mutualistic’ E. coli. These mutants exhibited slower bacterial growth, smaller size, loss of flagellar motility and lack of an extracellular matrix. Transcriptomic and genomic analyses of ‘mutualistic’ E. coli lines revealed independent mutations that disrupted the carbon catabolite repression global transcriptional regulator system. Each mutation reproduced the mutualistic phenotypes when introduced into wild-type E. coli, confirming that single carbon catabolite repression mutations can make E. coli an insect mutualist. These findings provide an experimental system for future work on host–microbe symbioses and may explain why microbial mutualisms are omnipresent in nature.