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Author: Grafiati
Published: 11 March 2023

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1

Brescia, Francesca, Anthi Vlassi, Ana Bejarano, Bernard Seidl, Martina Marchetti-Deschmann, Rainer Schuhmacher, and Gerardo Puopolo. "Characterisation of the Antibiotic Profile of Lysobacter capsici AZ78, an Effective Biological Control Agent of Plant Pathogenic Microorganisms." Microorganisms 9, no. 6 (June 17, 2021): 1320. http://dx.doi.org/10.3390/microorganisms9061320.

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Determining the mode of action of microbial biocontrol agents plays a key role in their development and registration as commercial biopesticides. The biocontrol rhizobacterium Lysobacter capsici AZ78 (AZ78) is able to inhibit a vast array of plant pathogenic oomycetes and Gram-positive bacteria due to the release of antimicrobial secondary metabolites. A combination of MALDI-qTOF-MSI and UHPLC-HRMS/M was applied to finely dissect the AZ78 metabolome and identify the main secondary metabolites involved in the inhibition of plant pathogenic microorganisms. Under nutritionally limited conditions, MALDI-qTOF-MSI revealed that AZ78 is able to release a relevant number of antimicrobial secondary metabolites belonging to the families of 2,5-diketopiperazines, cyclic lipodepsipeptides, macrolactones and macrolides. In vitro tests confirmed the presence of secondary metabolites toxic against Pythium ultimum and Rhodococcus fascians in AZ78 cell-free extracts. Subsequently, UHPLC-HRMS/MS was used to confirm the results achieved with MALDI-qTOF-MSI and investigate for further putative antimicrobial secondary metabolites known to be produced by Lysobacter spp. This technique confirmed the presence of several 2,5-diketopiperazines in AZ78 cell-free extracts and provided the first evidence of the production of the cyclic depsipeptide WAP-8294A2 in a member of L. capsici species. Moreover, UHPLC-HRMS/MS confirmed the presence of dihydromaltophilin/Heat Stable Antifungal Factor (HSAF) in AZ78 cell-free extracts. Due to the production of HSAF by AZ78, cell-free supernatants were effective in controlling Plasmopara viticola on grapevine leaf disks after exposure to high temperatures. Overall, our work determined the main secondary metabolites involved in the biocontrol activity of AZ78 against plant pathogenic oomycetes and Gram-positive bacteria. These results might be useful for the future development of this bacterial strain as the active ingredient of a microbial biopesticide that might contribute to a reduction in the chemical input in agriculture.
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2

Vlassi, Anthi, Andrea Nesler, Alexandra Parich, Gerardo Puopolo, and Rainer Schuhmacher. "Volatile-Mediated Inhibitory Activity of Rhizobacteria as a Result of Multiple Factors Interaction: The Case of Lysobacter capsici AZ78." Microorganisms 8, no. 11 (November 9, 2020): 1761. http://dx.doi.org/10.3390/microorganisms8111761.

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Plant beneficial rhizobacteria may antagonize soilborne plant pathogens by producing a vast array of volatile organic compounds (VOCs). The production of these compounds depends on the medium composition used for bacterial cell growth. Accordingly, Lysobacter capsici AZ78 (AZ78) grown on a protein-rich medium was previously found to emit volatile pyrazines with toxic activity against soilborne phypathogenic fungi and oomycetes. However, the discrepancy between the quantity of pyrazines in the gaseous phase and the minimum quantity needed to achieve inhibition of plant pathogens observed, lead us to further investigate the volatile-mediated inhibitory activity of AZ78. Here, we show that, besides VOCs, AZ78 cells produce ammonia in increased amounts when a protein-rich medium is used for bacterial growth. The production of this volatile compound caused the alkalinization of the physically separated culture medium where Rhizoctonia solani was inoculated subsequently. Results achieved in this work clearly demonstrate that VOC, ammonia and the growth medium alkalinization contribute to the overall inhibitory activity of AZ78 against R. solani. Thus, our findings suggest that the volatile-mediated inhibitory activity of rhizobacteria in protein-rich substrates can be regarded as a result of multiple factors interaction, rather than exclusively VOCs production.
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3

Puopolo, Gerardo, Oscar Giovannini, and Ilaria Pertot. "Lysobacter capsici AZ78 can be combined with copper to effectively control Plasmopara viticola on grapevine." Microbiological Research 169, no. 7-8 (July 2014): 633–42. http://dx.doi.org/10.1016/j.micres.2013.09.013.

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4

Cimmino, A., G. Puopolo, M. Perazzolli, A. Andolfi, D. Melck, I. Pertot, and A. Evidente. "Cyclo(L-PRO-L-TYR), The Fungicide Isolated From Lysobacter Capsici AZ78: A Structure–Activity Relationship Study." Chemistry of Heterocyclic Compounds 50, no. 2 (April 23, 2014): 290–95. http://dx.doi.org/10.1007/s10593-014-1475-6.

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5

Puopolo, Gerardo, Maria Cristina Palmieri, Oscar Giovannini, and Ilaria Pertot. "Impact of temperature on the survival and the biocontrol efficacy of Lysobacter capsici AZ78 against Phytophthora infestans." BioControl 60, no. 5 (April 18, 2015): 681–89. http://dx.doi.org/10.1007/s10526-015-9672-5.

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6

Cimmino, A., G. Puopolo, M. Perazzolli, A. Andolfi, D. Melck, I. Pertot, and A. Evidente. "ChemInform Abstract: Cyclo(L-Pro-L-Tyr), the Fungicide Isolated from Lysobacter capsici AZ78: A Structure-Activity Relationship Study." ChemInform 45, no. 42 (October 2, 2014): no. http://dx.doi.org/10.1002/chin.201442226.

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7

Segarra, Guillem, Gerardo Puopolo, Oscar Giovannini, and Ilaria Pertot. "Stepwise flow diagram for the development of formulations of non spore-forming bacteria against foliar pathogens: The case of Lysobacter capsici AZ78." Journal of Biotechnology 216 (December 2015): 56–64. http://dx.doi.org/10.1016/j.jbiotec.2015.10.004.

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8

Puopolo, G., A. Cimmino, M. C. Palmieri, O. Giovannini, A. Evidente, and I. Pertot. "Lysobacter capsici AZ78 produces cyclo(l -Pro-l -Tyr), a 2,5-diketopiperazine with toxic activity against sporangia of Phytophthora infestans and Plasmopara viticola." Journal of Applied Microbiology 117, no. 4 (August 21, 2014): 1168–80. http://dx.doi.org/10.1111/jam.12611.

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9

Tomada, Selena, Paolo Sonego, Marco Moretto, Kristof Engelen, Ilaria Pertot, Michele Perazzolli, and Gerardo Puopolo. "Dual RNA-Seq of Lysobacter capsici AZ78 - Phytophthora infestans interaction shows the implementation of attack strategies by the bacterium and unsuccessful oomycete defense responses." Environmental Microbiology 19, no. 10 (August 14, 2017): 4113–25. http://dx.doi.org/10.1111/1462-2920.13861.

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10

Bejarano, Ana, Michele Perazzolli, Ilaria Pertot, and Gerardo Puopolo. "The Perception of Rhizosphere Bacterial Communication Signals Leads to Transcriptome Reprogramming in Lysobacter capsici AZ78, a Plant Beneficial Bacterium." Frontiers in Microbiology 12 (August 18, 2021). http://dx.doi.org/10.3389/fmicb.2021.725403.

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The rhizosphere is a dynamic region governed by complex microbial interactions where diffusible communication signals produced by bacteria continuously shape the gene expression patterns of individual species and regulate fundamental traits for adaptation to the rhizosphere environment. Lysobacter spp. are common bacterial inhabitants of the rhizosphere and have been frequently associated with soil disease suppressiveness. However, little is known about their ecology and how diffusible communication signals might affect their behavior in the rhizosphere. To shed light on the aspects determining rhizosphere competence and functioning of Lysobacter spp., we carried out a functional and transcriptome analysis on the plant beneficial bacterium Lysobacter capsici AZ78 (AZ78) grown in the presence of the most common diffusible communication signals released by rhizosphere bacteria. Mining the genome of AZ78 and other Lysobacter spp. showed that Lysobacter spp. share genes involved in the production and perception of diffusible signal factors, indole, diffusible factors, and N-acyl-homoserine lactones. Most of the tested diffusible communication signals (i.e., indole and glyoxylic acid) influenced the ability of AZ78 to inhibit the growth of the phytopathogenic oomycete Pythium ultimum and the Gram-positive bacterium Rhodococcus fascians. Moreover, RNA-Seq analysis revealed that nearly 21% of all genes in AZ78 genome were modulated by diffusible communication signals. 13-Methyltetradecanoic acid, glyoxylic acid, and 2,3-butanedione positively influenced the expression of genes related to type IV pilus, which might enable AZ78 to rapidly colonize the rhizosphere. Moreover, glyoxylic acid and 2,3-butanedione downregulated tRNA genes, possibly as a result of the elicitation of biological stress responses. On its behalf, indole downregulated genes related to type IV pilus and the heat-stable antifungal factor, which might result in impairment of twitching motility and antibiotic production in AZ78. These results show that diffusible communication signals may affect the ecology of Lysobacter spp. in the rhizosphere and suggest that diffusible communication signals might be used to foster rhizosphere colonization and functioning of plant beneficial bacteria belonging to the genus Lysobacter.
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11

Cimmino, Alessio, Ana Bejarano, Marco Masi, Gerardo Puopolo, and Antonio Evidente. "Isolation of 2,5-diketopiperazines from Lysobacter capsici AZ78 with activity against Rhodococcus fascians." Natural Product Research, April 30, 2020, 1–9. http://dx.doi.org/10.1080/14786419.2020.1756803.

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12

Puopolo, G., P. Sonego, K. Engelen, and I. Pertot. "Draft Genome Sequence of Lysobacter capsici AZ78, a Bacterium Antagonistic to Plant-Pathogenic Oomycetes." Genome Announcements 2, no. 2 (April 24, 2014). http://dx.doi.org/10.1128/genomea.00325-14.

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13

Vlassi, Anthi, Andrea Nesler, Michele Perazzolli, Valentina Lazazzara, Christoph Büschl, Alexandra Parich, Gerardo Puopolo, and Rainer Schuhmacher. "Volatile Organic Compounds From Lysobacter capsici AZ78 as Potential Candidates for Biological Control of Soilborne Plant Pathogens." Frontiers in Microbiology 11 (August 7, 2020). http://dx.doi.org/10.3389/fmicb.2020.01748.

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14

Puopolo, Gerardo, Selena Tomada, Paolo Sonego, Marco Moretto, Kristof Engelen, Michele Perazzolli, and Ilaria Pertot. "The Lysobacter capsici AZ78 Genome Has a Gene Pool Enabling it to Interact Successfully with Phytopathogenic Microorganisms and Environmental Factors." Frontiers in Microbiology 7 (February 5, 2016). http://dx.doi.org/10.3389/fmicb.2016.00096.

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15

Tomada, Selena, Gerardo Puopolo, Michele Perazzolli, Rita Musetti, Nazia Loi, and Ilaria Pertot. "Pea Broth Enhances the Biocontrol Efficacy of Lysobacter capsici AZ78 by Triggering Cell Motility Associated with Biogenesis of Type IV Pilus." Frontiers in Microbiology 7 (July 26, 2016). http://dx.doi.org/10.3389/fmicb.2016.01136.

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16

Markellou, Emilia, Eleftheria Kapaxidi, Filitsa Karamaouna, Maria Samara, Katerina Kyriakopoulou, Pelagia Anastasiadou, Evangelia Vavoulidou, et al. "Evaluation of plant protection efficacy in field conditions and side effects of Lysobacter capsici AZ78, a biocontrol agent of Plasmopara viticola." Biocontrol Science and Technology, April 25, 2022, 1–22. http://dx.doi.org/10.1080/09583157.2022.2064431.

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17

Markellou, Emilia, Eleftheria Kapaxidi, Filitsa Karamaouna, Maria Samara, Katerina Kyriakopoulou, Pelagia Anastasiadou, Evangelia Vavoulidou, et al. "Evaluation of plant protection efficacy in field conditions and side effects of Lysobacter capsici AZ78, a biocontrol agent of Plasmopara viticola." Biocontrol Science and Technology, April 25, 2022, 1–22. http://dx.doi.org/10.1080/09583157.2022.2064431.

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18

Markellou, Emilia, Eleftheria Kapaxidi, Filitsa Karamaouna, Maria Samara, Katerina Kyriakopoulou, Pelagia Anastasiadou, Evangelia Vavoulidou, et al. "Evaluation of plant protection efficacy in field conditions and side effects of Lysobacter capsici AZ78, a biocontrol agent of Plasmopara viticola." Biocontrol Science and Technology, April 25, 2022, 1–22. http://dx.doi.org/10.1080/09583157.2022.2064431.

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