Journal articles on the topic 'Bacteroids'
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1
Karunakaran, R., V. K. Ramachandran, J. C. Seaman, A. K. East, B. Mouhsine, T. H. Mauchline, J. Prell, A. Skeffington, and P. S. Poole. "Transcriptomic Analysis of Rhizobium leguminosarum Biovar viciae in Symbiosis with Host Plants Pisum sativum and Vicia cracca." Journal of Bacteriology 191, no. 12 (April 17, 2009): 4002–14. http://dx.doi.org/10.1128/jb.00165-09.
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ABSTRACT Rhizobium leguminosarum bv. viciae forms nitrogen-fixing nodules on several legumes, including pea (Pisum sativum) and vetch (Vicia cracca), and has been widely used as a model to study nodule biochemistry. To understand the complex biochemical and developmental changes undergone by R. leguminosarum bv. viciae during bacteroid development, microarray experiments were first performed with cultured bacteria grown on a variety of carbon substrates (glucose, pyruvate, succinate, inositol, acetate, and acetoacetate) and then compared to bacteroids. Bacteroid metabolism is essentially that of dicarboxylate-grown cells (i.e., induction of dicarboxylate transport, gluconeogenesis and alanine synthesis, and repression of sugar utilization). The decarboxylating arm of the tricarboxylic acid cycle is highly induced, as is γ-aminobutyrate metabolism, particularly in bacteroids from early (7-day) nodules. To investigate bacteroid development, gene expression in bacteroids was analyzed at 7, 15, and 21 days postinoculation of peas. This revealed that bacterial rRNA isolated from pea, but not vetch, is extensively processed in mature bacteroids. In early development (7 days), there were large changes in the expression of regulators, exported and cell surface molecules, multidrug exporters, and heat and cold shock proteins. fix genes were induced early but continued to increase in mature bacteroids, while nif genes were induced strongly in older bacteroids. Mutation of 37 genes that were strongly upregulated in mature bacteroids revealed that none were essential for nitrogen fixation. However, screening of 3,072 mini-Tn5 mutants on peas revealed previously uncharacterized genes essential for nitrogen fixation. These encoded a potential magnesium transporter, an AAA domain protein, and proteins involved in cytochrome synthesis.
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Cooper, Bret, Kimberly B. Campbell, Hunter S. Beard, Wesley M. Garrett, Joseph Mowery, Gary R. Bauchan, and Patrick Elia. "A Proteomic Network for Symbiotic Nitrogen Fixation Efficiency in Bradyrhizobium elkanii." Molecular Plant-Microbe Interactions® 31, no. 3 (March 2018): 334–43. http://dx.doi.org/10.1094/mpmi-10-17-0243-r.
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Rhizobia colonize legumes and reduce N2 to NH3 in root nodules. The current model is that symbiotic rhizobia bacteroids avoid assimilating this NH3. Instead, host legume cells form glutamine from NH3, and the nitrogen is returned to the bacteroid as dicarboxylates, peptides, and amino acids. In soybean cells surrounding bacteroids, glutamine also is converted to ureides. One problem for soybean cultivation is inefficiency in symbiotic N2 fixation, the biochemical basis of which is unknown. Here, the proteomes of bacteroids of Bradyrhizobium elkanii USDA76 isolated from N2 fixation-efficient Peking and -inefficient Williams 82 soybean nodules were analyzed by mass spectrometry. Nearly half of the encoded bacterial proteins were quantified. Efficient bacteroids produced greater amounts of enzymes to form Nod factors and had increased amounts of signaling proteins, transporters, and enzymes needed to generate ATP to power nitrogenase and to acquire resources. Parallel investigation of nodule proteins revealed that Peking had no significantly greater accumulation of enzymes needed to assimilate NH3 than Williams 82. Instead, efficient bacteroids had increased amounts of enzymes to produce amino acids, including glutamine, and to form ureide precursors. These results support a model for efficient symbiotic N2 fixation in soybean where the bacteroid assimilates NH3 for itself.
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Strodtman, Kent N., Severin E. Stevenson, James K. Waters, Thomas P. Mawhinney, Jay J. Thelen, Joseph C. Polacco, and David W. Emerich. "The Bacteroid Periplasm in Soybean Nodules Is an Interkingdom Symbiotic Space." Molecular Plant-Microbe Interactions® 30, no. 12 (December 2017): 997–1008. http://dx.doi.org/10.1094/mpmi-12-16-0264-r.
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The functional role of the periplasm of nitrogen-fixing bacteroids has not been determined. Proteins were isolated from the periplasm and cytoplasm of Bradyrhizobium diazoefficiens bacteroids and were analyzed using liquid chromatography tandem mass spectrometry proteomics. Identification of bacteroid periplasmic proteins was aided by periplasm prediction programs. Approximately 40% of all the proteins identified as periplasmic in the B. diazoefficiens genome were found expressed in the bacteroid form of the bacteria, indicating the periplasm is a metabolically active symbiotic space. The bacteroid periplasm possesses many fatty acid metabolic enzymes, which was in contrast to the bacteroid cytoplasm. Amino acid analysis of the periplasm revealed an abundance of phosphoserine, phosphoethanolamine, and glycine, which are metabolites of phospholipid metabolism. These results suggest the periplasm is a unique space and not a continuum with the peribacteroid space. A number of plant proteins were found in the periplasm fraction, which suggested contamination. However, antibodies to two of the identified plant proteins, histone H2A and lipoxygenase, yielded immunogold labeling that demonstrated the plant proteins were specifically targeted to the bacteroids. This suggests that the periplasm is an interkingdom symbiotic space containing proteins from both the bacteroid and the plant.
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Borucki, Wojciech. "Some new aspects of the pea (Pisum sativum L.) root nodule ultrastructure." Acta Societatis Botanicorum Poloniae 65, no. 3-4 (2014): 221–33. http://dx.doi.org/10.5586/asbp.1996.035.
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Unequal cell divisions were observed in the meristem of pea root nodule. Since after such divisions only the bigger cells become infected then those divisions play a significant role in the formation of the three-dimensional structure of the bacteroidal tissue. In the infected cells of the young ineffective bacteroidal tissue the first host reaction to the incompatibility of the symbiotic system is the RER membranes aggregation. In effective symbiosis RER membranes form permanent sites of contact with the peribacteroidal membranes thus connecting all the symbiosoms in the cell. Possibly that ensures the synchronisation of the differentiation processes of the bacteroids and/or their simultaneous degeneration. The presence of membraneous structures in the form of rings is a characteristic feature of effective bacteroids. It is postulated that the structures are directly connected with nitrogen assimilation. Structures X and Y which are present in the bacteroids of the effective and ineffective symbiosis may be connected with the adaptation of bacterial cells to lowered oxygen pressure in bacteroidal tissue and their transformation (structures X) into bacteroids. The presence of the cytoplasm (or cytoplasmatic remnants) of the infected cells was observed in the intercellular spaces. It is sugested that it is a way, so far unknown, of the gas diffusion regulation in bacteroidal tissue.
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Brito, Belén, Annita Toffanin, Rosa-Isabel Prieto, Juan Imperial, Tomás Ruiz-Argüeso, and Jose M. Palacios. "Host-Dependent Expression of Rhizobium leguminosarum bv. viciae Hydrogenase Is Controlled at Transcriptional and Post-Transcriptional Levels in Legume Nodules." Molecular Plant-Microbe Interactions® 21, no. 5 (May 2008): 597–604. http://dx.doi.org/10.1094/mpmi-21-5-0597.
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The legume host affects the expression of Rhizobium leguminosarum hydrogenase activity in root nodules. High levels of symbiotic hydrogenase activity were detected in R. leguminosarum bacteroids from different hosts, with the exception of lentil (Lens culinaris). Transcription analysis showed that the NifA-regulated R. leguminosarum hydrogenase structural gene promoter (P1) is poorly induced in lentil root nodules. Replacement of the P1 promoter by the FnrN-dependent promoter of the fixN gene restored transcription of hup genes in lentil bacteroids, but not hydrogenase activity. In the PfixN-hupSL strain, additional copies of the hup gene cluster and nickel supplementation to lentil plants increased bacteroid hydrogenase activity. However, the level of activity in lentil still was significantly lower than in pea bacteroids, indicating that an additional factor is impairing hydrogenase expression inside lentil nodules. Immunological analysis revealed that lentil bacteroids contain reduced levels of both hydrogenase structural subunit HupL and nickel-binding protein HypB. Altogether, results indicate that hydrogenase expression is affected by the legume host at the level of both transcription of hydrogenase structural genes and biosynthesis or stability of nickel-related proteins HypB and HupL, and suggest the existence of a plant-dependent mechanism that affects hydrogenase activity during the symbiosis by limiting nickel availability to the bacteroid.
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Becana, Manuel, and Marvin L. Salin. "Superoxide dismutases in nodules of leguminous plants." Canadian Journal of Botany 67, no. 2 (February 1, 1989): 415–21. http://dx.doi.org/10.1139/b89-057.
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Isoenzymic composition of superoxide dismutases (SODs; EC 1.15.1.1) of legume nodules has been examined by using polyacrylamide gel electrophoresis. The study reveals that Cu plus Zn–SODs and Mn–SODs are widespread in the plant and bacteroidal fractions of nodules, respectively. The number of CuZn–isoenzymes, however, depends on the legume species: three or four in Lupinus, three in Phaseolus, two in Vigna, and one in Glycine, Trifolium, Pisum, and Medicago. The nodule plant fraction also exhibits Mn–SOD activity, which is, at least in Medicago, of plant origin. Two Mn–isoenzymes are present in most bacteroids as well as in all slow-growing rhizobia, but just one was observed in fast-growing rhizobia. Fe–SOD has not been found in free-living or symbiotic rhizobia. A faint CuZn–SOD activity was detected in the bacteroid fraction of Phaseolus, Trifolium, Lupinus, and Vigna. The high content and complex pattern of SOD isoenzymes in the host cells and bacteroids (despite their relatively anaerobic environment) indicate a substantial production of [Formula: see text] in nodules in vivo, and the necessity for nitrogenase and leghemoglobin protection.
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Gully, Djamel, Daniel Gargani, Katia Bonaldi, Cédric Grangeteau, Clémence Chaintreuil, Joël Fardoux, Phuong Nguyen, et al. "A Peptidoglycan-Remodeling Enzyme Is Critical for Bacteroid Differentiation in Bradyrhizobium spp. During Legume Symbiosis." Molecular Plant-Microbe Interactions® 29, no. 6 (June 2016): 447–57. http://dx.doi.org/10.1094/mpmi-03-16-0052-r.
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In response to the presence of compatible rhizobium bacteria, legumes form symbiotic organs called nodules on their roots. These nodules house nitrogen-fixing bacteroids that are a differentiated form of the rhizobium bacteria. In some legumes, the bacteroid differentiation comprises a dramatic cell enlargement, polyploidization, and other morphological changes. Here, we demonstrate that a peptidoglycan-modifying enzyme in Bradyrhizobium strains, a DD-carboxypeptidase that contains a peptidoglycan-binding SPOR domain, is essential for normal bacteroid differentiation in Aeschynomene species. The corresponding mutants formed bacteroids that are malformed and hypertrophied. However, in soybean, a plant that does not induce morphological differentiation of its symbiont, the mutation does not affect the bacteroids. Remarkably, the mutation also leads to necrosis in a large fraction of the Aeschynomene nodules, indicating that a normally formed peptidoglycan layer is essential for avoiding the induction of plant immune responses by the invading bacteria. In addition to exopolysaccharides, capsular polysaccharides, and lipopolysaccharides, whose role during symbiosis is well defined, our work demonstrates an essential role in symbiosis for yet another rhizobial envelope component, the peptidoglycan layer.
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Moris, Martine, Kristien Braeken, Eric Schoeters, Christel Verreth, Serge Beullens, Jos Vanderleyden, and Jan Michiels. "Effective Symbiosis between Rhizobium etli and Phaseolus vulgaris Requires the Alarmone ppGpp." Journal of Bacteriology 187, no. 15 (August 1, 2005): 5460–69. http://dx.doi.org/10.1128/jb.187.15.5460-5469.2005.
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ABSTRACT The symbiotic interaction between Rhizobium etli and Phaseolus vulgaris, the common bean plant, ultimately results in the formation of nitrogen-fixing nodules. Many aspects of the intermediate and late stages of this interaction are still poorly understood. The R. etli relA gene was identified through a genome-wide screening for R. etli symbiotic mutants. RelA has a pivotal role in cellular physiology, as it catalyzes the synthesis of (p)ppGpp, which mediates the stringent response in bacteria. The synthesis of ppGpp was abolished in an R. etli relA mutant strain under conditions of amino acid starvation. Plants nodulated by an R. etli relA mutant had a strongly reduced nitrogen fixation activity (75% reduction). Also, at the microscopic level, bacteroid morphology was altered, with the size of relA mutant bacteroids being increased compared to that of wild-type bacteroids. The expression of the σN-dependent nitrogen fixation genes rpoN2 and iscN was considerably reduced in the relA mutant. In addition, the expression of the relA gene was negatively regulated by RpoN2, the symbiosis-specific σN copy of R. etli. Therefore, an autoregulatory loop controlling the expression of relA and rpoN2 seems operative in bacteroids. The production of long- and short-chain acyl-homoserine-lactones by the cinIR and raiIR systems was decreased in an R. etli relA mutant. Our results suggest that relA may play an important role in the regulation of gene expression in R. etli bacteroids and in the adaptation of bacteroid physiology.
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Reuhs, Bradley L., Samuel B. Stephens, Daniel P. Geller, John S. Kim, Joshua Glenn, Jessica Przytycki, and Tuula Ojanen-Reuhs. "Epitope Identification for a Panel of Anti-Sinorhizobium meliloti Monoclonal Antibodies and Application to the Analysis of K Antigens and Lipopolysaccharides from Bacteroids." Applied and Environmental Microbiology 65, no. 11 (November 1, 1999): 5186–91. http://dx.doi.org/10.1128/aem.65.11.5186-5191.1999.
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ABSTRACT In two published reports using monoclonal antibodies (MAbs) generated against whole cells, Olsen et al. showed that strain-specific antigens on the surface of cultured cells of Sinorhizobium meliloti were diminished or absent in the endophytic cells (bacteroids) recovered from alfalfa nodules, whereas two common antigens were not affected by bacterial differentiation (P. Olsen, M. Collins, and W. Rice, Can. J. Microbiol. 38:506–509, 1992; P. Olsen, S. Wright, M. Collins, and W. Rice, Appl. Environ. Microbiol. 60:654–661, 1994). The nature of the antigens (i.e., the MAb epitopes), however, were not determined in those studies. For this report, the epitopes for five of the anti-S. meliloti MAbs were identified by polyacrylamide gel electrophoresis-immunoblot analyses of the polysaccharides extracted from S. melilotiand Sinorhizobium fredii. This showed that the strain-specific MAbs recognized K antigens, whereas the strain-cross-reactive MAbs recognized the lipopolysaccharide (LPS) core. The MAbs were then used in the analysis of the LPS and K antigens extracted from S. meliloti bacteroids, which had been recovered from the root nodules of alfalfa, and the results supported the findings of Olsen et al. The size range of the K antigens from bacteroids of S. meliloti NRG247 on polyacrylamide gels was altered, and the epitope was greatly diminished in abundance compared to those from the cultured cells, and no K antigens were detected in the S. meliloti NRG185 bacteroid extract. In contrast to the K antigens, the LPS core appeared to be similar in both cultured cells and bacteroids, although a higher proportion of the LPS fractionated into the organic phase during the phenol-water extraction of the bacteroid polysaccharides. Importantly, immunoblot analysis with an anti-LPS MAb showed that smooth LPS production was modified in the bacteroids.
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Lodwig, E. M., M. Leonard, S. Marroqui, T. R. Wheeler, K. Findlay, J. A. Downie, and P. S. Poole. "Role of Polyhydroxybutyrate and Glycogen as Carbon Storage Compounds in Pea and Bean Bacteroids." Molecular Plant-Microbe Interactions® 18, no. 1 (January 2005): 67–74. http://dx.doi.org/10.1094/mpmi-18-0067.
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Rhizobium leguminosarum synthesizes polyhydroxybutyrate and glycogen as its main carbon storage compounds. To examine the role of these compounds in bacteroid development and in symbiotic efficiency, single and double mutants of R. leguminosarum bv. viciae were made which lack poly-hydroxybutyrate synthase (phaC), glycogen synthase (glgA), or both. For comparison, a single phaC mutant also was isolated in a bean-nodulating strain of R. leguminosarum bv. phaseoli. In one large glasshouse trial, the growth of pea plants inoculated with the R. leguminosarum bv. viciae phaC mutant were significantly reduced compared with wild-type-inoculated plants. However, in subsequent glasshouse and growth-room studies, the growth of pea plants inoculated with the mutant were similar to wild-type-inoculated plants. Bean plants were unaffected by the loss of polyhydroxybutyrate biosynthesis in bacteroids. Pea plants nodulated by a glycogen synthase mutant, or the glgA/phaC double mutant, grew as well as the wild type in growth-room experiments. Light and electron micrographs revealed that pea nodules infected with the glgA mutant accumulated large amounts of starch in the II/III interzone. This suggests that glycogen may be the dominant carbon storage compound in pea bacteroids. Polyhydroxybutyrate was present in bacteria in the infection thread of pea plants but was broken down during bacteroid formation. In nodules infected with a phaC mutant of R. leguminosarum bv. viciae, there was a drop in the amount of starch in the II/III interzone, where bacteroids form. Therefore, we propose a carbon burst hypothesis for bacteroid formation, where polyhydroxybutyrate accumulated by bacteria is degraded to fuel bacteroid differentiation.
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Marchetti, Marta, Olivier Catrice, Jacques Batut, and Catherine Masson-Boivin. "Cupriavidus taiwanensisBacteroids inMimosa pudicaIndeterminate Nodules Are Not Terminally Differentiated." Applied and Environmental Microbiology 77, no. 6 (January 21, 2011): 2161–64. http://dx.doi.org/10.1128/aem.02358-10.
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ABSTRACTThe beta-rhizobiumCupriavidus taiwanensisforms indeterminate nodules onMimosa pudica. C. taiwanensisbacteroids resemble free-living bacteria in terms of genomic DNA content, cell size, membrane permeability, and viability, in contrast to bacteroids in indeterminate nodules of the galegoid clade. Bacteroid differentiation is thus unrelated to nodule ontogeny.
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Montiel, Jesús, J. Allan Downie, Attila Farkas, Péter Bihari, Róbert Herczeg, Balázs Bálint, Peter Mergaert, Attila Kereszt, and Éva Kondorosi. "Morphotype of bacteroids in different legumes correlates with the number and type of symbiotic NCR peptides." Proceedings of the National Academy of Sciences 114, no. 19 (April 24, 2017): 5041–46. http://dx.doi.org/10.1073/pnas.1704217114.
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In legume nodules, rhizobia differentiate into nitrogen-fixing forms called bacteroids, which are enclosed by a plant membrane in an organelle-like structure called the symbiosome. In the Inverted Repeat-Lacking Clade (IRLC) of legumes, this differentiation is terminal due to irreversible loss of cell division ability and is associated with genome amplification and different morphologies of the bacteroids that can be swollen, elongated, spherical, and elongated–branched, depending on the host plant. In Medicago truncatula, this process is orchestrated by nodule-specific cysteine-rich peptides (NCRs) delivered into developing bacteroids. Here, we identified the predicted NCR proteins in 10 legumes representing different subclades of the IRLC with distinct bacteroid morphotypes. Analysis of their expression and predicted sequences establishes correlations between the composition of the NCR family and the morphotypes of bacteroids. Although NCRs have a single origin, their evolution has followed different routes in individual lineages, and enrichment and diversification of cationic peptides has resulted in the ability to impose major morphological changes on the endosymbionts. The wide range of effects provoked by NCRs such as cell enlargement, membrane alterations and permeabilization, and biofilm and vesicle formation is dependent on the amino acid composition and charge of the peptides. These effects are strongly influenced by the rhizobial surface polysaccharides that affect NCR-induced differentiation and survival of rhizobia in nodule cells.
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Capela, Delphine, Cédric Filipe, Christine Bobik, Jacques Batut, and Claude Bruand. "Sinorhizobium meliloti Differentiation During Symbiosis with Alfalfa: A Transcriptomic Dissection." Molecular Plant-Microbe Interactions® 19, no. 4 (April 2006): 363–72. http://dx.doi.org/10.1094/mpmi-19-0363.
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Sinorhizobium meliloti is a soil bacterium able to induce the formation of nodules on the root of specific legumes, including alfalfa (Medicago sativa). Bacteria colonize nodules through infection threads, invade the plant intracellularly, and ultimately differentiate into bacteroids capable of reducing atmospheric nitrogen to ammonia, which is directly assimilated by the plant. As a first step to describe global changes in gene expression of S. meliloti during the symbiotic process, we used whole genome microarrays to establish the transcriptome profile of bacteria from nodules induced by a bacterial mutant blocked at the infection stage and from wild-type nodules harvested at various timepoints after inoculation. Comparison of these profiles to those of cultured bacteria grown either to log or stationary phase as well as examination of a number of genes with known symbiotic transcription patterns allowed us to correlate global gene-expression patterns to three known steps of symbiotic bacteria bacteroid differentiation, i.e., invading bacteria inside infection threads, young differentiating bacteroids, and fully differentiated, nitrogen-fixing bacteroids. Finally, analysis of individual gene transcription profiles revealed a number of new potential symbiotic genes.
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Chohan, Shahid N., and Les Copeland. "Acetoacetyl Coenzyme A Reductase and Polyhydroxybutyrate Synthesis in Rhizobium(Cicer) sp. Strain CC 1192." Applied and Environmental Microbiology 64, no. 8 (August 1, 1998): 2859–63. http://dx.doi.org/10.1128/aem.64.8.2859-2863.1998.
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ABSTRACT Biochemical controls that regulate the biosynthesis of poly-3-hydroxybutyrate (PHB) were investigated in Rhizobium(Cicer) sp. strain CC 1192. This species is of interest for studying PHB synthesis because the polymer accumulates to a large extent in free-living cells but not in bacteroids during nitrogen-fixing symbiosis with chickpea (Cicer arietinumL.) plants. Evidence is presented that indicates that CC 1192 cells retain the enzymic capacity to synthesize PHB when they differentiate from the free-living state to the bacteroid state. This evidence includes the incorporation by CC 1192 bacteroids of radiolabel from [14C]malate into 3-hydroxybutyrate which was derived by chemically degrading insoluble material from bacteroid pellets. Furthermore, the presence of an NADPH-dependent acetoacetyl coenzyme A (CoA) reductase, which was specific forR-(−)-3-hydroxybutyryl-CoA and NADP+ in the oxidative direction, was demonstrated in extracts from free-living and bacteroid cells of CC 1192. Activity of this enzyme in the reductive direction appeared to be regulated at the biochemical level mainly by the availability of substrates. The CC 1192 cells also contained an NADH-specific acetoacetyl-CoA reductase which oxidizedS-(+)-3-hydroxybutyryl-CoA. A membrane preparation from CC 1192 bacteroids readily oxidized NADH but not NADPH, which is suggested to be a major source of reductant for nitrogenase. Thus, a high ratio of NADPH to NADP+, which could enhance delivery of reductant to nitrogenase, could also favor the reduction of acetoacetyl-CoA for PHB synthesis. This would mean that fine controls that regulate the partitioning of acetyl-CoA between citrate synthase and 3-ketothiolase are important in determining whether PHB accumulates.
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Streeter, J. G., and M. L. Gomez. "Three Enzymes for Trehalose Synthesis in Bradyrhizobium Cultured Bacteria and in Bacteroids from Soybean Nodules." Applied and Environmental Microbiology 72, no. 6 (June 2006): 4250–55. http://dx.doi.org/10.1128/aem.00256-06.
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ABSTRACT α,α-Trehalose is a disaccharide accumulated by many microorganisms, including rhizobia, and a common role for trehalose is protection of membrane and protein structure during periods of stress, such as desiccation. Cultured Bradyrhizobium japonicum and B. elkanii were found to have three enzymes for trehalose synthesis: trehalose synthase (TS), maltooligosyltrehalose synthase (MOTS), and trehalose-6-phosphate synthetase. The activity level of the latter enzyme was much higher than those of the other two in cultured bacteria, but the reverse was true in bacteroids from nodules. Although TS was the dominant enzyme in bacteroids, the source of maltose, the substrate for TS, is not clear; i.e., the maltose concentration in nodules was very low and no maltose was formed by bacteroid protein preparations from maltooligosaccharides. Because bacteroid protein preparations contained high trehalase activity, it was imperative to inhibit this enzyme in studies of TS and MOTS in bacteroids. Validamycin A, a commonly used trehalase inhibitor, was found to also inhibit TS and MOTS, and other trehalase inhibitors, such as trehazolin, must be used in studies of these enzymes in nodules. The results of a survey of five other species of rhizobia indicated that most species sampled had only one major mechanism for trehalose synthesis. The presence of three totally independent mechanisms for the synthesis of trehalose by Bradyrhizobium species suggests that this disaccharide is important in the function of this organism both in the free-living state and in symbiosis.
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Shearer, G., and DH Kohl. "Natural 15N Abundance of NH4+, Amide N, and Total N in Various Fractions of Nodules of Peas, Soybeans and Lupins." Functional Plant Biology 16, no. 4 (1989): 305. http://dx.doi.org/10.1071/pp9890305.
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Nodules of certain N2-fixing root nodules are substantially enriched in 15N compared with non-nodular tissues. This enrichment usually resides largely within bacteroids. Isotope discrimination associated with export of ammonia(um) from the bacteroid would result in 15N enrichment of NH4+ within bac- teroids. Bacteroid protein synthesis from this pool of 15N enriched NH4+ would then account for enrichment of the bacteroids. Measurements of 15N abundances of total N and free NH4+ in nodule fractions from lupins (Lupinus luteus), soybeans (Glycine max) and peas (Pisum sativum) showed this was not the case. With the inocula used in experiments reported here, lupin and soybean nodules were enriched in 15N, while pea nodules were not. There was no correlation between 15N abundances of NH4+ and total N in the nodule fractions (r= 0.445, P> 0.2). We conclude that isotope discrimination associated with ammonia(um) transport does not explain the 15N elevation of lupin and soybean nodules. We also conclude, on the basis of the large isotope effect for the equilibrium between NH4+ and NH3, that most of the ammonia(um) is exported from bacteroids as NH4+ rather than NH3. We also measured the 15N abundance of free amide N. There was a strong correlation between 15N abundances of free amide N and total N in nodule fractions (r=0.924, P<0,001), suggesting that amide N is a significant source of N to the amino acid pools from which proteins are synthesised.
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Shen, San Chiun, Shui Ping Wang, Guan Qiao Yu, and Jia Bi Zhu. "Expression of the nodulation and nitrogen fixation genes in Rhizobium meliloti during development." Genome 31, no. 1 (January 1, 1989): 354–60. http://dx.doi.org/10.1139/g89-054.
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Genes that specify nodulation (nod genes) are only active in the free-living rhizobia or in the nodule initiation state of rhizobia. As soon as the repression of nod genes occurs in the bacteroids of the nodule, nifA is induced, while ntrC is inactivated and thus the nifA-mediated nif/fix genes are turned on. Limitation of available oxygen brings about the induction of nifA, which reflects the actual status of nif/fix gene activities in symbiotic state of rhizobia. Oxygen thus appears to be a major symbiotic signal to the expression of bacteroid nif/fix genes. Mutation of nifA or shortage of nifA product in wild-type rhizobia caused by the inhibition of multicopy nifH/fixA promoters leads to an abnormal development of nodules and premature degradation of bacteroids in nodules.Key words: nitrogen fixation, nodulation, nif/fix regulation, nifA mutant.
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Vercruysse, Maarten, Maarten Fauvart, Serge Beullens, Kristien Braeken, Lore Cloots, Kristof Engelen, Kathleen Marchal, and Jan Michiels. "A Comparative Transcriptome Analysis of Rhizobium etli Bacteroids: Specific Gene Expression During Symbiotic Nongrowth." Molecular Plant-Microbe Interactions® 24, no. 12 (December 2011): 1553–61. http://dx.doi.org/10.1094/mpmi-05-11-0140.
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Rhizobium etli occurs either in a nitrogen-fixing symbiosis with its host plant, Phaseolus vulgaris, or free-living in the soil. During both conditions, the bacterium has been suggested to reside primarily in a nongrowing state. Using genome-wide transcriptome profiles, we here examine the molecular basis of the physiological adaptations of rhizobia to nongrowth inside and outside of the host. Compared with exponentially growing cells, we found an extensive overlap of downregulated growth-associated genes during both symbiosis and stationary phase, confirming the essentially nongrowing state of nitrogen-fixing bacteroids in determinate nodules that are not terminally differentiated. In contrast, the overlap of upregulated genes was limited. Generally, actively growing cells have hitherto been used as reference to analyze symbiosis-specific expression. However, this prevents the distinction between differential expression arising specifically from adaptation to a symbiotic lifestyle and features associated with nongrowth in general. Using stationary phase as the reference condition, we report a distinct transcriptome profile for bacteroids, containing 203 induced and 354 repressed genes. Certain previously described symbiosis-specific characteristics, such as the downregulation of amino acid metabolism genes, were no longer observed, indicating that these features are more likely due to the nongrowing state of bacteroids rather than representing bacteroid-specific physiological adaptations.
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Mendoza, Alberto, Brenda Valderrama, Alfonso Leija, and Jaime Mora. "NifA-Dependent Expression of Glutamate Dehydrogenase in Rhizobium etli Modifies Nitrogen Partitioning During Symbiosis." Molecular Plant-Microbe Interactions® 11, no. 2 (February 1998): 83–90. http://dx.doi.org/10.1094/mpmi.1998.11.2.83.
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Constitutive expression of foreign glutamate dehydrogenase in Rhizobium etli inhibits bean plant nodulation (A. Mendoza, A. Leija, E. Martínez-Romero, G. Hernández, and J. Mora. Mol. Plant-Microbe Interact. 8:584-592, 1995). Here we report that this inhibition is overcome when controlling gdhA expression by NifA, thus delaying the GDH activity onset after nodule establishment. Expression of gdhA modifies the nitrogen partitioning inside the bacteroid, where newly synthesized ammonia is preferentially incorporated into the amino acid pool instead of being exported to the infected cells. As a consequence, the fixed nitrogen transport to the leaves, measured as the ureides content in xylem sap, is significantly reduced. Nitrogenase activity, although not nifHDK expression, is significantly reduced in bacteroids expressing gdhA, probably due to the utilization of energy and reducing power for nitrogen assimilation. Here we show that ammonia assimilation inside R. etli bacteroids is active, albeit at low levels, and when enhanced is deleterious to the symbiotic performance. This leads us to believe that further reduction of the basal nitrogen metabolism in the bacteroid might stimulate the nitrogenase activity and increase the nitrogen supply to the plant.
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Wheatley, Rachel M., Brandon L. Ford, Li Li, Samuel T. N. Aroney, Hayley E. Knights, Raphael Ledermann, Alison K. East, Vinoy K. Ramachandran, and Philip S. Poole. "Lifestyle adaptations ofRhizobiumfrom rhizosphere to symbiosis." Proceedings of the National Academy of Sciences 117, no. 38 (September 8, 2020): 23823–34. http://dx.doi.org/10.1073/pnas.2009094117.
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By analyzing successive lifestyle stages of a modelRhizobium–legume symbiosis using mariner-based transposon insertion sequencing (INSeq), we have defined the genes required for rhizosphere growth, root colonization, bacterial infection, N2-fixing bacteroids, and release from legume (pea) nodules. While only 27 genes are annotated asnifandfixinRhizobium leguminosarum, we show 603 genetic regions (593 genes, 5 transfer RNAs, and 5 RNA features) are required for the competitive ability to nodulate pea and fix N2. Of these, 146 are common to rhizosphere growth through to bacteroids. This large number of genes, defined as rhizosphere-progressive, highlights how critical successful competition in the rhizosphere is to subsequent infection and nodulation. As expected, there is also a large group (211) specific for nodule bacteria and bacteroid function. Nodule infection and bacteroid formation require genes for motility, cell envelope restructuring, nodulation signaling, N2fixation, and metabolic adaptation. Metabolic adaptation includes urea, erythritol and aldehyde metabolism, glycogen synthesis, dicarboxylate metabolism, and glutamine synthesis (GlnII). There are 17 separate lifestyle adaptations specific to rhizosphere growth and 23 to root colonization, distinct from infection and nodule formation. These results dramatically highlight the importance of competition at multiple stages of aRhizobium–legume symbiosis.
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Lodwig, Emma, Shalini Kumar, David Allaway, Alex Bourdes, Jürgen Prell, Ursula Priefer, and Philip Poole. "Regulation of l-Alanine Dehydrogenase in Rhizobium leguminosarum bv. viciae and Its Role in Pea Nodules." Journal of Bacteriology 186, no. 3 (February 1, 2004): 842–49. http://dx.doi.org/10.1128/jb.186.3.842-849.2004.
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ABSTRACT Alanine dehydrogenase (AldA) is the principal enzyme with which pea bacteroids synthesize alanine de novo. In free-living culture, AldA activity is induced by carboxylic acids (succinate, malate, and pyruvate), although the best inducer is alanine. Measurement of the intracellular concentration of alanine showed that AldA contributes to net alanine synthesis in laboratory cultures. Divergently transcribed from aldA is an AsnC type regulator, aldR. Mutation of aldR prevents induction of AldA activity. Plasmid-borne gusA fusions showed that aldR is required for transcription of both aldA and aldR; hence, AldR is autoregulatory. However, plasmid fusions containing the aldA-aldR intergenic region could apparently titrate out AldR, sometimes resulting in a complete loss of AldA enzyme activity. Therefore, integrated aldR::gusA and aldA::gusA fusions, as well as Northern blotting, were used to confirm the induction of aldA activity. Both aldA and aldR were expressed in the II/III interzone and zone III of pea nodules. Overexpression of aldA in bacteroids did not alter the ability of pea plants to fix nitrogen, as measured by acetylene reduction, but caused a large reduction in the size and dry weight of plants. This suggests that overexpression of aldA impairs the ability of bacteroids to donate fixed nitrogen that the plant can productively assimilate. We propose that the role of AldA may be to balance the alanine level for optimal functioning of bacteroid metabolism rather than to synthesize alanine as the sole product of N2 reduction.
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Terpolilli, Jason J., Shyam K. Masakapalli, Ramakrishnan Karunakaran, Isabel U. C. Webb, Rob Green, Nicholas J. Watmough, Nicholas J. Kruger, R. George Ratcliffe, and Philip S. Poole. "Lipogenesis and Redox Balance in Nitrogen-Fixing Pea Bacteroids." Journal of Bacteriology 198, no. 20 (August 8, 2016): 2864–75. http://dx.doi.org/10.1128/jb.00451-16.
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ABSTRACTWithin legume root nodules, rhizobia differentiate into bacteroids that oxidize host-derived dicarboxylic acids, which is assumed to occur via the tricarboxylic acid (TCA) cycle to generate NAD(P)H for reduction of N2. Metabolic flux analysis of laboratory-grownRhizobium leguminosarumshowed that the flux from [13C]succinate was consistent with respiration of an obligate aerobe growing on a TCA cycle intermediate as the sole carbon source. However, the instability of fragile pea bacteroids prevented their steady-state labeling under N2-fixing conditions. Therefore, comparative metabolomic profiling was used to compare free-livingR. leguminosarumwith pea bacteroids. While the TCA cycle was shown to be essential for maximal rates of N2fixation, levels of pyruvate (5.5-fold reduced), acetyl coenzyme A (acetyl-CoA; 50-fold reduced), free coenzyme A (33-fold reduced), and citrate (4.5-fold reduced) were much lower in bacteroids. Instead of completely oxidizing acetyl-CoA, pea bacteroids channel it into both lipid and the lipid-like polymer poly-β-hydroxybutyrate (PHB), the latter via a type III PHB synthase that is active only in bacteroids. Lipogenesis may be a fundamental requirement of the redox poise of electron donation to N2in all legume nodules. Direct reduction by NAD(P)H of the likely electron donors for nitrogenase, such as ferredoxin, is inconsistent with their redox potentials. Instead, bacteroids must balance the production of NAD(P)H from oxidation of acetyl-CoA in the TCA cycle with its storage in PHB and lipids.IMPORTANCEBiological nitrogen fixation by symbiotic bacteria (rhizobia) in legume root nodules is an energy-expensive process. Within legume root nodules, rhizobia differentiate into bacteroids that oxidize host-derived dicarboxylic acids, which is assumed to occur via the TCA cycle to generate NAD(P)H for reduction of N2. However, direct reduction of the likely electron donors for nitrogenase, such as ferredoxin, is inconsistent with their redox potentials. Instead, bacteroids must balance oxidation of plant-derived dicarboxylates in the TCA cycle with lipid synthesis. Pea bacteroids channel acetyl-CoA into both lipid and the lipid-like polymer poly-β-hydroxybutyrate, the latter via a type II PHB synthase. Lipogenesis is likely to be a fundamental requirement of the redox poise of electron donation to N2in all legume nodules.
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Oono, Ryoko, Carolyn G. Anderson, and R. Ford Denison. "Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates." Proceedings of the Royal Society B: Biological Sciences 278, no. 1718 (January 26, 2011): 2698–703. http://dx.doi.org/10.1098/rspb.2010.2193.
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The legume–rhizobia symbiosis is a classical mutualism where fixed carbon and nitrogen are exchanged between the species. Nonetheless, the plant carbon that fuels nitrogen (N 2 ) fixation could be diverted to rhizobial reproduction by ‘cheaters’—rhizobial strains that fix less N 2 but potentially gain the benefit of fixation by other rhizobia. Host sanctions can decrease the relative fitness of less-beneficial reproductive bacteroids and prevent cheaters from breaking down the mutualism. However, in certain legume species, only undifferentiated rhizobia reproduce, while only terminally differentiated rhizobial bacteroids fix nitrogen. Sanctions were, therefore, tested in two legume species that host non-reproductive bacteroids. We demonstrate that even legume species that host non-reproductive bacteroids, specifically pea and alfalfa, can severely sanction undifferentiated rhizobia when bacteroids within the same nodule fail to fix N 2 . Hence, host sanctions by a diverse set of legumes play a role in maintaining N 2 fixation.
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Natera, Siria H. A., Nelson Guerreiro, and Michael A. Djordjevic. "Proteome Analysis of Differentially Displayed Proteins As a Tool for the Investigation of Symbiosis." Molecular Plant-Microbe Interactions® 13, no. 9 (September 2000): 995–1009. http://dx.doi.org/10.1094/mpmi.2000.13.9.995.
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Two-dimensional gel electrophoresis was used to identify differentially displayed proteins expressed during the symbiotic interaction between the bacterium Sinorhizobium meliloti strain 1021 and the legume Melilotus alba (white sweetclover). Our aim was to characterize novel symbiosis proteins and to determine how the two symbiotic partners alter their respective metabolisms as part of the interaction, by identifying gene products that are differentially present between the symbiotic and non-symbiotic states. Proteome maps from control M. alba roots, wild-type nodules, cultured S. meliloti, and S. meliloti bacteroids were generated and compared. Over 250 proteins were induced or up-regulated in the nodule, compared with the root, and over 350 proteins were down-regulated in the bacteroid form of the rhizobia, compared with cultured cells. N-terminal amino acid sequencing and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry peptide mass fingerprint analysis, in conjunction with data base searching, were used to assign putative identity to nearly 100 nodule, bacterial, and bacteroid proteins. These included the previously identified nodule proteins leghemoglobin and NifH as well as proteins involved in carbon and nitrogen metabolism in S. meliloti. Bacteroid cells showed down-regulation of several proteins involved in nitrogen acquisition, including glutamine synthetase, urease, a urea-amide binding protein, and a PII isoform, indicating that the bacteroids were nitrogen proficient. The down-regulation of several enzymes involved in polyhydroxybutyrate synthesis and a cell division protein was also observed. This work shows that proteome analysis will be a useful strategy to link sequence information and functional genomics.
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Day, David A., and Penelope M. C. Smith. "Iron Transport across Symbiotic Membranes of Nitrogen-Fixing Legumes." International Journal of Molecular Sciences 22, no. 1 (January 4, 2021): 432. http://dx.doi.org/10.3390/ijms22010432.
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Iron is an essential nutrient for the legume-rhizobia symbiosis and nitrogen-fixing bacteroids within root nodules of legumes have a very high demand for the metal. Within the infected cells of nodules, the bacteroids are surrounded by a plant membrane to form an organelle-like structure called the symbiosome. In this review, we focus on how iron is transported across the symbiosome membrane and accessed by the bacteroids.
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Vedam, Vinata, Janine G. Haynes, Elmar L. Kannenberg, Russell W. Carlson, and D. Janine Sherrier. "A Rhizobium leguminosarum Lipopolysaccharide Lipid-A Mutant Induces Nitrogen-Fixing Nodules with Delayed and Defective Bacteroid Formation." Molecular Plant-Microbe Interactions® 17, no. 3 (March 2004): 283–91. http://dx.doi.org/10.1094/mpmi.2004.17.3.283.
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Lipopolysaccharides from pea-nodulating strain Rhizobium leguminosarum bv. viciae 3841, as all other members of the family Rhizobiaceae with the possible exception of Azorhizobium caulinodans, contains a very long chain fatty acid; 27-hydroxyoctacosanoic acid (27OHC28:0) in its lipid A region. The exact function and importance of this residue, however, is not known. In this work, a previously constructed mutant, Rhizobium leguminosarum bv. viciae 22, deficient in the fatty acid residue, was analyzed for its symbiotic phenotype. While the mutant was able to form nitrogen-fixing nodules, a detailed study of the timing and efficiency of nodulation using light and electron microscopy showed that there was a delay in the onset of nodulation and nodule tissue invasion. Further, microscopy showed that the mutant was unable to differentiate normally forming numerous irregularly shaped bacteroids, that the resultant mature bacteroids were unusually large, and that several bacteroids were frequently enclosed in a single symbiosome membrane, a feature not observed with parent bacteroids. In addition, the mutant nodules were delayed in the onset of nitrogenase production and showed reduced nitrogenase throughout the testing period. These results imply that the lack of 27OHC28:0 in the lipid A in mutant bacteroids results in altered membrane properties that are essential for the development of normal bacteroids.
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Barsch, Aiko, Verena Tellström, Thomas Patschkowski, Helge Küster, and Karsten Niehaus. "Metabolite Profiles of Nodulated Alfalfa Plants Indicate That Distinct Stages of Nodule Organogenesis Are Accompanied by Global Physiological Adaptations." Molecular Plant-Microbe Interactions® 19, no. 9 (September 2006): 998–1013. http://dx.doi.org/10.1094/mpmi-19-0998.
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An effective symbiosis between Sinorhizobium meliloti and its host plant Medicago sativa is dependent on a balanced physiological interaction enabling the microsymbiont to fix atmospheric nitrogen. Maintenance of the symbiotic interaction is regulated by still poorly understood control mechanisms. A first step toward a better understanding of nodule metabolism was the determination of characteristic metabolites for alfalfa root nodules. Furthermore, nodules arrested at different developmental stages were analyzed in order to address metabolic changes induced during the progression of nodule formation. Metabolite profiles of bacteroid-free pseudonodule extracts indicated that early nodule developmental processes are accompanied by photosynthate translocation but no massive organic acid formation. To determine metabolic adaptations induced by the presence of nonfixing bacteroids, nodules induced by mutant S. meliloti strains lacking the nitrogenase protein were analyzed. The bacteroids are unable to provide ammonium to the host plant, which is metabolically reflected by reduced levels of characteristic amino acids involved in ammonium fixation. Elevated levels of starch and sugars in Fix¯ nodules provide strong evidence that plant sanctions preventing a transformation from a symbiotic to a potentially parasitic interaction are not strictly realized via photo-synthate supply. Instead, metabolic and gene expression data indicate that alfalfa plants react to nitrogen-fixation-deficient bacteroids with a decreased organic acid synthesis and an early induction of senescence. Noneffective symbiotic interactions resulting from plants nodulated by mutant rhizobia also are reflected in characteristic metabolic changes in leaves. These are typical for nitrogen deficiency, but also highlight metabolites potentially involved in sensing the N status.
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Karunakaran, Ramakrishnan, Andreas F. Haag, Alison K. East, Vinoy K. Ramachandran, Jurgen Prell, Euan K. James, Marco Scocchi, Gail P. Ferguson, and Philip S. Poole. "BacA Is Essential for Bacteroid Development in Nodules of Galegoid, but not Phaseoloid, Legumes." Journal of Bacteriology 192, no. 11 (April 2, 2010): 2920–28. http://dx.doi.org/10.1128/jb.00020-10.
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ABSTRACT BacA is an integral membrane protein, the mutation of which leads to increased resistance to the antimicrobial peptides bleomycin and Bac71-35 and a greater sensitivity to SDS and vancomycin in Rhizobium leguminosarum bv. viciae, R. leguminosarum bv. phaseoli, and Rhizobium etli. The growth of Rhizobium strains on dicarboxylates as a sole carbon source was impaired in bacA mutants but was overcome by elevating the calcium level. While bacA mutants elicited indeterminate nodule formation on peas, which belong to the galegoid tribe of legumes, bacteria lysed after release from infection threads and mature bacteroids were not formed. Microarray analysis revealed almost no change in a bacA mutant of R. leguminosarum bv. viciae in free-living culture. In contrast, 45 genes were more-than 3-fold upregulated in a bacA mutant isolated from pea nodules. Almost half of these genes code for cell membrane components, suggesting that BacA is crucial to alterations that occur in the cell envelope during bacteroid development. In stark contrast, bacA mutants of R. leguminosarum bv. phaseoli and R. etli elicited the formation of normal determinate nodules on their bean host, which belongs to the phaseoloid tribe of legumes. Bacteroids from these nodules were indistinguishable from the wild type in morphology and nitrogen fixation. Thus, while bacA mutants of bacteria that infect galegoid or phaseoloid legumes have similar phenotypes in free-living culture, BacA is essential only for bacteroid development in indeterminate galegoid nodules.
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Libault, Marc, Manjula Govindarajulu, R. Howard Berg, Yee Tsuey Ong, Kari Puricelli, Christopher G. Taylor, Dong Xu, and Gary Stacey. "A Dual-Targeted Soybean Protein Is Involved in Bradyrhizobium japonicum Infection of Soybean Root Hair and Cortical Cells." Molecular Plant-Microbe Interactions® 24, no. 9 (September 2011): 1051–60. http://dx.doi.org/10.1094/mpmi-12-10-0281.
Full textAbstract:
The symbiotic interaction between legumes and soil bacteria (e.g., soybean [Glycine max L.] and Bradyrhizobium japonicum]) leads to the development of a new root organ, the nodule, where bacteria differentiate into bacteroids that fix atmospheric nitrogen for assimilation by the plant host. In exchange, the host plant provides a steady carbon supply to the bacteroids. This carbon can be stored within the bacteroids in the form of poly-3-hydroxybutyrate granules. The formation of this symbiosis requires communication between both partners to regulate the balance between nitrogen fixation and carbon utilization. In the present study, we describe the soybean gene GmNMNa that is specifically expressed during the infection of soybean cells by B. japonicum. GmNMNa encodes a protein of unknown function. The GmNMNa protein was localized to the nucleolus and also to the mitochondria. Silencing of GmNMNa expression resulted in reduced nodulation, a reduction in the number of bacteroids per infected cell in the nodule, and a clear reduction in the accumulation of poly-3-hydroxybutyrate in the bacteroids. Our results highlight the role of the soybean GmNMNa gene in regulating symbiotic bacterial infection, potentially through the regulation of the accumulation of carbon reserves.
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Pessi, Gabriella, Christian H. Ahrens, Hubert Rehrauer, Andrea Lindemann, Felix Hauser, Hans-Martin Fischer, and Hauke Hennecke. "Genome-Wide Transcript Analysis of Bradyrhizobium japonicum Bacteroids in Soybean Root Nodules." Molecular Plant-Microbe Interactions® 20, no. 11 (November 2007): 1353–63. http://dx.doi.org/10.1094/mpmi-20-11-1353.
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The transcriptome of endosymbiotic Bradyrhizobium japonicum bacteroids was assessed, using RNA extracted from determinate soybean root nodules. Results were compared with the transcript profiles of B. japonicum cells grown in either aerobic or microaerobic culture. Microoxia is a known trigger for the induction of symbiotically relevant genes. In fact, one third of the genes induced in bacteroids at day 21 after inoculation are congruent with those up-regulated in culture by a decreased oxygen concentration. The other induced genes, however, may be regulated by cues other than oxygen limitation. Both groups of genes provide a rich source for the possible discovery of novel functions related to symbiosis. Samples taken at different timepoints in nodule development have led to the distinction of genes expressed early and late in bacteroids. The experimental approach applied here is also useful for B. japonicum mutant analyses. As an example, we compared the transcriptome of wild-type bacteroids with that of bacteroids formed by a mutant defective in the RNA polymerase transcription factor σ54. This led to a collection of hitherto unrecognized B. japonicum genes potentially transcribed in planta in a σ54-dependent manner.
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Bradley, D. J., G. W. Butcher, G. Galfre, E. A. Wood, and N. J. Brewin. "Physical association between the peribacteroid membrane and lipopolysaccharide from the bacteroid outer membrane in Rhizobium-infected pea root nodule cells." Journal of Cell Science 85, no. 1 (September 1, 1986): 47–61. http://dx.doi.org/10.1242/jcs.85.1.47.
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Monoclonal antibodies were used as cytochemical markers to study surface interactions between endosymbiotic Rhizobium bacteroids from pea root nodules and the encircling peribacteroid membranes, which are of plant origin. Monoclonal antibodies that react with Rhizobium lipopolysaccharide (LPS) or with a plant membrane glycoprotein were used as markers for material from the bacteroid outer membrane or the peribacteroid membrane, respectively. Membrane-enclosed bacteroids were isolated from nodule homogenates by sucrose gradient centrifugation, and the encircling peribacteroid membrane was released by mild osmotic shock treatment. Using an immunochemical technique (sandwich ELISA), it was shown that 1–5% of the LPS antigen released into the peribacteroid fraction by mild osmotic shock treatment was physically associated with peribacteroid membrane through a detergent-sensitive linkage. This association could be visualized when freshly prepared peribacteroid material was immobilized on gold grids and examined by electron microscopy after dual antibody immunogold treatment and subsequent negative staining. The distribution of LPS antigen within infected nodule cells was also investigated by immunogold staining for thin sections of nodule tissue fixed in glutaraldehyde, and a close association between LPS antigen and peribacteroid membrane was often seen.
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Olsen, Perry, Mandy Collins, and Wendell Rice. "Surface antigens present on vegetative Rhizobium meliloti cells may be diminished or absent when cells are in the bacteroid form." Canadian Journal of Microbiology 38, no. 6 (June 1, 1992): 506–9. http://dx.doi.org/10.1139/m92-083.
Full textAbstract:
The results of fluorescent antibody staining of three Rhizobium meliloti strains using three "strain-cross-reactive" and three "strain-specific" monoclonal antibodies indicated that strain-specific antigens present on surfaces of laboratory-cultured vegetative cells were diminished or absent on surfaces of bacteroid cells extracted from alfalfa nodules formed by the respective strains. In contrast, the monoclonal antibody cross-reactive antigens appeared to be generally conserved during the transition from vegetative cells to bacteroids. These results offer a basis for observed reductions or complete loss of capability of some "strain-specific" monoclonal antibodies developed against vegetative Rhizobium cells to detect the strains in nodule squash material by enzyme-linked immunosorbent assay. Key words: Rhizobium, monoclonal antibody, bacteroid, surface antigen, fluorescent antibody.
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Boscari, Alexandre, Ghislaine Van de Sype, Daniel Le Rudulier, and Karine Mandon. "Overexpression of BetS, a Sinorhizobium meliloti High-Affinity Betaine Transporter, in Bacteroids from Medicago sativa Nodules Sustains Nitrogen Fixation During Early Salt Stress Adaptation." Molecular Plant-Microbe Interactions® 19, no. 8 (August 2006): 896–903. http://dx.doi.org/10.1094/mpmi-19-0896.
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Sinorhizobium meliloti possesses several betaine transporters to cope with salt stress, and BetS represents a crucial high-affinity glycine and proline betaine uptake system involved in the rapid acquisition of betaines by cells subjected to osmotic upshock. Using a transcriptional lacZ (β-galactosidase) fusion, we showed that betS is expressed during the establishment of the symbiosis and in mature nitrogen-fixing nodules. However, neither Nod nor Fix phenotypes were impaired in a betS mutant. BetS is functional in isolated bacteroids, and its activity is strongly activated by high osmolarity. In bacteroids from a betS mutant, glycine betaine and proline betaine uptake was reduced by 85 to 65%, indicating that BetS is a major component of the overall betaine uptake activity in bacteroids in response to osmotic stress. Upon betS overexpression (strain UNA349) in free-living cells, glycine betaine transport was 2.3-fold higher than in the wild-type strain. Interestingly, the accumulation of proline betaine, the endogenous betaine synthesized by alfalfa plants, was 41% higher in UNA349 bacteroids from alfalfa plants subjected to 1 week of salinization (0.3 M NaCl) than in wild-type bacteroids. In parallel, a much better maintenance of nitrogen fixation activity was observed in 7-day-salinized plants nodulated with the over-expressing strain than in wild-type nodulated plants. Taken altogether, these results are consistent with the major role of BetS as an emergency system involved in the rapid uptake of betaines in isolated and in planta osmotically stressed bacteroids of S. meliloti.
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Kim, Minsoo, Yuhui Chen, Jiejun Xi, Christopher Waters, Rujin Chen, and Dong Wang. "An antimicrobial peptide essential for bacterial survival in the nitrogen-fixing symbiosis." Proceedings of the National Academy of Sciences 112, no. 49 (November 23, 2015): 15238–43. http://dx.doi.org/10.1073/pnas.1500123112.
Full textAbstract:
In the nitrogen-fixing symbiosis between legume hosts and rhizobia, the bacteria are engulfed by a plant cell membrane to become intracellular organelles. In the model legume Medicago truncatula, internalization and differentiation of Sinorhizobium (also known as Ensifer) meliloti is a prerequisite for nitrogen fixation. The host mechanisms that ensure the long-term survival of differentiating intracellular bacteria (bacteroids) in this unusual association are unclear. The M. truncatula defective nitrogen fixation4 (dnf4) mutant is unable to form a productive symbiosis, even though late symbiotic marker genes are expressed in mutant nodules. We discovered that in the dnf4 mutant, bacteroids can apparently differentiate, but they fail to persist within host cells in the process. We found that the DNF4 gene encodes NCR211, a member of the family of nodule-specific cysteine-rich (NCR) peptides. The phenotype of dnf4 suggests that NCR211 acts to promote the intracellular survival of differentiating bacteroids. The greatest expression of DNF4 was observed in the nodule interzone II-III, where bacteroids undergo differentiation. A translational fusion of DNF4 with GFP localizes to the peribacteroid space, and synthetic NCR211 prevents free-living S. meliloti from forming colonies, in contrast to mock controls, suggesting that DNF4 may interact with bacteroids directly or indirectly for its function. Our findings indicate that a successful symbiosis requires host effectors that not only induce bacterial differentiation, but also that maintain intracellular bacteroids during the host–symbiont interaction. The discovery of NCR211 peptides that maintain bacterial survival inside host cells has important implications for improving legume crops.
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Taté, Rosarita, Michele Cermola, Anna Riccio, Maurizio Iaccarino, Mike Merrick, Reneé Favre, and Eduardo J. Patriarca. "Ectopic Expression of the Rhizobium etli amtB Gene Affects the Symbiosome Differentiation Process and Nodule Development." Molecular Plant-Microbe Interactions® 12, no. 6 (June 1999): 515–25. http://dx.doi.org/10.1094/mpmi.1999.12.6.515.
Full textAbstract:
Under conditions of nitrogen limitation, soil bacteria of the genus Rhizobium are able to induce the development of symbiotic nodules on the roots of leguminous plants. During nodule organogenesis, bacteria are released endocytotically inside the invaded plant cells where they differentiate into their endosymbiotic form called bacteroids. Bacteroids surrounded by a plant-derived peribacteroid membrane are nondividing, organelle-like structures, called symbiosomes, that use nitrogenase to reduce N2 to ammonia. Experiments performed in vitro with isolated symbiosomes have previously led to the suggestion that the NH3 produced by the bacteroids is released as NH4+ into the plant cytosol. Furthermore, it was observed that the bacterial amtB (ammonium/methylammonium transport B) gene is switched off very early during symbiosis, just when bacteria are released into the host cells. We report here that the ectopic expression of amtB in bacteroids alters the ability of bacteria to invade the host cells and the symbiosome differentiation process. Both the NtrC protein, which controls the expression of the bacterial genes involved in NH4+ assimilation, and the nitrogenase activity are essential to observe the amtB-mediated effect. Our results support the idea that in vivo bacteroids do not take up NH4+ and demonstrate that the transcriptional down-regulation of the amtB gene is essential for an effective symbiotic interaction.
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Schulte, Carolin C. M., Khushboo Borah, Rachel M. Wheatley, Jason J. Terpolilli, Gerhard Saalbach, Nick Crang, Daan H. de Groot, et al. "Metabolic control of nitrogen fixation in rhizobium-legume symbioses." Science Advances 7, no. 31 (July 2021): eabh2433. http://dx.doi.org/10.1126/sciadv.abh2433.
Full textAbstract:
Rhizobia induce nodule formation on legume roots and differentiate into bacteroids, which catabolize plant-derived dicarboxylates to reduce atmospheric N2 into ammonia. Despite the agricultural importance of this symbiosis, the mechanisms that govern carbon and nitrogen allocation in bacteroids and promote ammonia secretion to the plant are largely unknown. Using a metabolic model derived from genome-scale datasets, we show that carbon polymer synthesis and alanine secretion by bacteroids facilitate redox balance in microaerobic nodules. Catabolism of dicarboxylates induces not only a higher oxygen demand but also a higher NADH/NAD+ ratio than sugars. Modeling and 13C metabolic flux analysis indicate that oxygen limitation restricts the decarboxylating arm of the tricarboxylic acid cycle, which limits ammonia assimilation into glutamate. By tightly controlling oxygen supply and providing dicarboxylates as the energy and electron source donors for N2 fixation, legumes promote ammonia secretion by bacteroids. This is a defining feature of rhizobium-legume symbioses.
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Montiel, Jesús, Attila Szűcs, Iulian Z. Boboescu, Vasile D. Gherman, Éva Kondorosi, and Attila Kereszt. "Terminal Bacteroid Differentiation Is Associated With Variable Morphological Changes in Legume Species Belonging to the Inverted Repeat-Lacking Clade." Molecular Plant-Microbe Interactions® 29, no. 3 (March 2016): 210–19. http://dx.doi.org/10.1094/mpmi-09-15-0213-r.
Full textAbstract:
Medicago and closely related legume species from the inverted repeat–lacking clade (IRLC) impose terminal differentiation onto their bacterial endosymbionts, manifested in genome endoreduplication, cell enlargement, and loss of cell-division capacity. Nodule-specific cysteine-rich (NCR) secreted host peptides are plant effectors of this process. As bacteroids in other IRLC legumes, such as Cicer arietinum and Glycyrrhiza lepidota, were reported not to display features of terminal differentiation, we investigated the fate of bacteroids in species from these genera as well as in four other species representing distinct genera of the phylogenetic tree for this clade. Bacteroids in all tested legumes proved to be larger in size and DNA content than cultured cells; however, the degree of cell elongation was rather variable in the different species. In addition, the reproductive ability of the bacteroids isolated from these legumes was remarkably reduced. In all IRLC species with available sequence data, the existence of NCR genes was found. These results indicate that IRLC legumes provoke terminal differentiation of their endosymbionts with different morphotypes, probably with the help of NCR peptides.
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Taté, Rosarita, Anna Riccio, Mike Merrick, and Eduardo J. Patriarca. "The Rhizobium etli amtB Gene Coding for an NH4+ Transporter Is Down-Regulated Early During Bacteroid Differentiation." Molecular Plant-Microbe Interactions® 11, no. 3 (March 1998): 188–98. http://dx.doi.org/10.1094/mpmi.1998.11.3.188.
Full textAbstract:
During development of root nodules, Rhizobium bacteria differentiate inside the invaded plant cells into N2-fixing bacteroids. Terminally differentiated bacteroids are unable to grow using the ammonia (NH3 ) produced therein by the nitrogenase complex. Therefore, the nitrogen assimilation activities of bacteroids, including the ammonium (NH4 +) uptake activity, are expected to be repressed during symbiosis. By sequence homology the R. etli amtB (ammonium transport) gene was cloned and sequenced. As previously shown for its counterpart in other organisms, the R. etli amtB gene product mediates the transport of NH4 +. The amtB gene is cotranscribed with the glnK gene (coding for a PII-like protein) from a nitrogen-regulated σ54-dependent promoter, which requires the transcriptional activator NtrC. Expression of the glnKamtB operon was found to be activated under nitrogen-limiting, free-living conditions, but down-regulated just when bacteria are released from the infection threads and before transcription of the nitrogenase genes. Our data suggest that the uncoupling between N2-fixation and NH3 assimilation observed in symbiosomes is generated by a transcriptional regulatory mechanism(s) beginning with the inactivation of NtrC in younger bacteroids.
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Vedam, Vinata, Elmar Kannenberg, Anup Datta, Dusty Brown, Janine G. Haynes-Gann, D. Janine Sherrier, and Russell W. Carlson. "The Pea Nodule Environment Restores the Ability of a Rhizobium leguminosarum Lipopolysaccharide acpXL Mutant To Add 27-Hydroxyoctacosanoic Acid to Its Lipid A." Journal of Bacteriology 188, no. 6 (March 15, 2006): 2126–33. http://dx.doi.org/10.1128/jb.188.6.2126-2133.2006.
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ABSTRACT Members of the Rhizobiaceae contain 27-hydroxyoctacosanoic acid (27OHC28:0) in their lipid A. A Rhizobium leguminosarum 3841 acpXL mutant (named here Rlv22) lacking a functional specialized acyl carrier lacked 27OHC28:0 in its lipid A, had altered growth and physiological properties (e.g., it was unable to grow in the presence of an elevated salt concentration [0.5% NaCl]), and formed irregularly shaped bacteroids, and the synchronous division of this mutant and the host plant-derived symbiosome membrane was disrupted. In spite of these defects, the mutant was able to persist within the root nodule cells and eventually form, albeit inefficiently, nitrogen-fixing bacteroids. This result suggested that while it is in a host root nodule, the mutant may have some mechanism by which it adapts to the loss of 27OHC28:0 from its lipid A. In order to further define the function of this fatty acyl residue, it was necessary to examine the lipid A isolated from mutant bacteroids. In this report we show that addition of 27OHC28:0 to the lipid A of Rlv22 lipopolysaccharides is partially restored in Rlv22 acpXL mutant bacteroids. We hypothesize that R. leguminosarum bv. viciae 3841 contains an alternate mechanism (e.g., another acp gene) for the synthesis of 27OHC28:0, which is activated when the bacteria are in the nodule environment, and that it is this alternative mechanism which functionally replaces acpXL and is responsible for the synthesis of 27OHC28:0-containing lipid A in the Rlv22 acpXL bacteroids.
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Roy, Proyash, Mingkee Achom, Helen Wilkinson, Beatriz Lagunas, and Miriam L. Gifford. "Symbiotic Outcome Modified by the Diversification from 7 to over 700 Nodule-Specific Cysteine-Rich Peptides." Genes 11, no. 4 (March 25, 2020): 348. http://dx.doi.org/10.3390/genes11040348.
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Legume-rhizobium symbiosis represents one of the most successfully co-evolved mutualisms. Within nodules, the bacterial cells undergo distinct metabolic and morphological changes and differentiate into nitrogen-fixing bacteroids. Legumes in the inverted repeat lacking clade (IRLC) employ an array of defensin-like small secreted peptides (SSPs), known as nodule-specific cysteine-rich (NCR) peptides, to regulate bacteroid differentiation and activity. While most NCRs exhibit bactericidal effects in vitro, studies confirm that inside nodules they target the bacterial cell cycle and other cellular pathways to control and extend rhizobial differentiation into an irreversible (or terminal) state where the host gains control over bacteroids. While NCRs are well established as positive regulators of effective symbiosis, more recent findings also suggest that NCRs affect partner compatibility. The extent of bacterial differentiation has been linked to species-specific size and complexity of the NCR gene family that varies even among closely related species, suggesting a more recent origin of NCRs followed by rapid expansion in certain species. NCRs have diversified functionally, as well as in their expression patterns and responsiveness, likely driving further functional specialisation. In this review, we evaluate the functions of NCR peptides and their role as a driving force underlying the outcome of rhizobial symbiosis, where the plant is able to determine the outcome of rhizobial interaction in a temporal and spatial manner.
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Horváth, Beatrix, Ágota Domonkos, Attila Kereszt, Attila Szűcs, Edit Ábrahám, Ferhan Ayaydin, Károly Bóka, et al. "Loss of the nodule-specific cysteine rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf7 mutant." Proceedings of the National Academy of Sciences 112, no. 49 (September 23, 2015): 15232–37. http://dx.doi.org/10.1073/pnas.1500777112.
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Host compatible rhizobia induce the formation of legume root nodules, symbiotic organs within which intracellular bacteria are present in plant-derived membrane compartments termed symbiosomes. In Medicago truncatula nodules, the Sinorhizobium microsymbionts undergo an irreversible differentiation process leading to the development of elongated polyploid noncultivable nitrogen fixing bacteroids that convert atmospheric dinitrogen into ammonia. This terminal differentiation is directed by the host plant and involves hundreds of nodule specific cysteine-rich peptides (NCRs). Except for certain in vitro activities of cationic peptides, the functional roles of individual NCR peptides in planta are not known. In this study, we demonstrate that the inability of M. truncatula dnf7 mutants to fix nitrogen is due to inactivation of a single NCR peptide, NCR169. In the absence of NCR169, bacterial differentiation was impaired and was associated with early senescence of the symbiotic cells. Introduction of the NCR169 gene into the dnf7-2/NCR169 deletion mutant restored symbiotic nitrogen fixation. Replacement of any of the cysteine residues in the NCR169 peptide with serine rendered it incapable of complementation, demonstrating an absolute requirement for all cysteines in planta. NCR169 was induced in the cell layers in which bacteroid elongation was most pronounced, and high expression persisted throughout the nitrogen-fixing nodule zone. Our results provide evidence for an essential role of NCR169 in the differentiation and persistence of nitrogen fixing bacteroids in M. truncatula.
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Mulley, Geraldine, Miguel Lopez-Gomez, Ye Zhang, Jason Terpolilli, Jurgen Prell, Turlough Finan, and Philip Poole. "Pyruvate Is Synthesized by Two Pathways in Pea Bacteroids with Different Efficiencies for Nitrogen Fixation." Journal of Bacteriology 192, no. 19 (July 30, 2010): 4944–53. http://dx.doi.org/10.1128/jb.00294-10.
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ABSTRACT Nitrogen fixation in legume bacteroids is energized by the metabolism of dicarboxylic acids, which requires their oxidation to both oxaloacetate and pyruvate. In alfalfa bacteroids, production of pyruvate requires NAD+ malic enzyme (Dme) but not NADP+ malic enzyme (Tme). However, we show that Rhizobium leguminosarum has two pathways for pyruvate formation from dicarboxylates catalyzed by Dme and by the combined activities of phosphoenolpyruvate (PEP) carboxykinase (PckA) and pyruvate kinase (PykA). Both pathways enable N2 fixation, but the PckA/PykA pathway supports N2 fixation at only 60% of that for Dme. Double mutants of dme and pckA/pykA did not fix N2. Furthermore, dme pykA double mutants did not grow on dicarboxylates, showing that they are the only pathways for the production of pyruvate from dicarboxylates normally expressed. PckA is not expressed in alfalfa bacteroids, resulting in an obligate requirement for Dme for pyruvate formation and N2 fixation. When PckA was expressed from a constitutive nptII promoter in alfalfa dme bacteroids, acetylene was reduced at 30% of the wild-type rate, although this level was insufficient to prevent nitrogen starvation. Dme has N-terminal, malic enzyme (Me), and C-terminal phosphotransacetylase (Pta) domains. Deleting the Pta domain increased the peak acetylene reduction rate in 4-week-old pea plants to 140 to 150% of the wild-type rate, and this was accompanied by increased nodule mass. Plants infected with Pta deletion mutants did not have increased dry weight, demonstrating that there is not a sustained change in nitrogen fixation throughout growth. This indicates a complex relationship between pyruvate synthesis in bacteroids, nitrogen fixation, and plant growth.
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Booth, Nicholas J., Penelope M. C. Smith, Sunita A. Ramesh, and David A. Day. "Malate Transport and Metabolism in Nitrogen-Fixing Legume Nodules." Molecules 26, no. 22 (November 15, 2021): 6876. http://dx.doi.org/10.3390/molecules26226876.
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Legumes form a symbiosis with rhizobia, a soil bacterium that allows them to access atmospheric nitrogen and deliver it to the plant for growth. Biological nitrogen fixation occurs in specialized organs, termed nodules, that develop on the legume root system and house nitrogen-fixing rhizobial bacteroids in organelle-like structures termed symbiosomes. The process is highly energetic and there is a large demand for carbon by the bacteroids. This carbon is supplied to the nodule as sucrose, which is broken down in nodule cells to organic acids, principally malate, that can then be assimilated by bacteroids. Sucrose may move through apoplastic and/or symplastic routes to the uninfected cells of the nodule or be directly metabolised at the site of import within the vascular parenchyma cells. Malate must be transported to the infected cells and then across the symbiosome membrane, where it is taken up by bacteroids through a well-characterized dct system. The dicarboxylate transporters on the infected cell and symbiosome membranes have been functionally characterized but remain unidentified. Proteomic and transcriptomic studies have revealed numerous candidates, but more work is required to characterize their function and localise the proteins in planta. GABA, which is present at high concentrations in nodules, may play a regulatory role, but this remains to be explored.
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Mandal, Drishti, and Senjuti Sinharoy. "A Toolbox for Nodule Development Studies in Chickpea: A Hairy-Root Transformation Protocol and an Efficient Laboratory Strain of Mesorhizobium sp." Molecular Plant-Microbe Interactions® 32, no. 4 (April 2019): 367–78. http://dx.doi.org/10.1094/mpmi-09-18-0264-ta.
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A Mesorhizobium sp. produces root nodules in chickpea. Chickpea and model legume Medicago truncatula are members of the inverted repeat–lacking clade (IRLC). The rhizobia, after internalization into the plant cell, are called bacteroids. Nodule-specific cysteine-rich peptides in IRLC legumes guide bacteroids to a terminally differentiated swollen (TDS) form. Bacteroids in chickpea are less TDS than those in Medicago spp. Nodule development in chickpea indicates recent evolutionary diversification and merits further study. A hairy-root transformation protocol and an efficient laboratory strain are prerequisites for performing any genetic study on nodulation. We have standardized a protocol for composite plant generation in chickpea with a transformation frequency above 50%, as shown by fluorescent markers. This protocol also works well in different ecotypes of chickpea. Localization of subcellular markers in these transformed roots is similar to the localization observed in transformed Medicago roots. When checked inside transformed nodules, peroxisomes were concentrated along the periphery of the nodules, while endoplasmic reticulum and Golgi bodies surrounded the symbiosomes. Different Mesorhizobium strains were evaluated for their ability to initiate nodule development and efficiency of nitrogen fixation. Inoculation with different strains resulted in different shapes of TDS bacteroids with variable nitrogen fixation. Our study provides a toolbox to study nodule development in the crop legume chickpea.
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HERRADA, G., A. PUPPO, and J. RIGAUD. "Uptake of Metabolites by Bacteroid-containing Vesicles and by Free Bacteroids from French Bean Nodules." Microbiology 135, no. 11 (November 1, 1989): 3165. http://dx.doi.org/10.1099/00221287-135-11-3165.
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Maier, R. J., and L. Graham. "Molybdate transport by Bradyrhizobium japonicum bacteroids." Journal of Bacteriology 170, no. 12 (1988): 5613–19. http://dx.doi.org/10.1128/jb.170.12.5613-5619.1988.
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Kretovich, W. L., V. I. Romanov, B. R. Abdullaeva, B. F. Ivanov, I. E. Chermenskaya, and N. G. Fedulova. "14C-glucose utilization byRhizobium lupini bacteroids." Plant and Soil 85, no. 2 (June 1985): 211–17. http://dx.doi.org/10.1007/bf02139625.
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Xun Shen. "Spontaneous luminescence from soybean Rhizobium bacteroids." FEMS Microbiology Letters 81, no. 3 (July 1, 1991): 335–40. http://dx.doi.org/10.1016/0378-1097(91)90237-5.
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MCDERMOTT, T. "Carbon metabolism in Bradyrhizobium japonicum bacteroids." FEMS Microbiology Reviews 63, no. 4 (December 1989): 327–40. http://dx.doi.org/10.1016/0168-6445(89)90027-2.
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Fox, M. A., J. P. White, A. H. F. Hosie, E. M. Lodwig, and P. S. Poole. "Osmotic Upshift Transiently Inhibits Uptake via ABC Transporters in Gram-Negative Bacteria." Journal of Bacteriology 188, no. 14 (July 15, 2006): 5304–7. http://dx.doi.org/10.1128/jb.00262-06.
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ABSTRACT ATP-binding cassette transporters from several rhizobia and Salmonella enterica serovar Typhimurium, but not secondarily coupled systems, were inhibited by high concentrations (100 to 500 mM) of various osmolytes, an effect reversed by the removal of the osmolyte. ABC systems were also inactivated in isolated pea bacteroids, probably due to the obligatory use of high-osmolarity isolation media. Measurement of nutrient cycling in isolated pea bacteroids is impeded by this effect.