Section: Microbiology
Topic: Agricultural sciences, Microbiology, Population biology

Bacterial pathogens dynamic during multi-species infections

10.24072/pcjournal.418 - Peer Community Journal, Volume 4 (2024), article no. e49.

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Soft rot Pectobacteriacea (SRP) gathers more than 30 bacterial species that collectively rot a wide range of plants by producing and secreting a large set of plant cell wall degrading enzymes (PCWDEs). Worldwide potato field surveys identified 15 different SRP species on symptomatic plants and tubers. The abundance of each species observed during outbreaks varies over space and time and the mechanisms driving species shift during outbreak are unknown. Furthermore, multi-species infections are frequently observed and the dynamics of these coinfections are not well understood.

To understand the dynamics of coinfections, we set up 16 different synthetic communities of 6 SRP strains to mimic coinfections. The bacteria present in each tested community were representative of 2 different species, with 3 strains per species. These communities were inoculated in potato tubers or on synthetic media and their outcome was followed by amplification and Illumina sequencing of the discriminatory housekeeping gene gapA. We also compared disease incidence and bacterial multiplication in potato tubers during mixed-species infection and single-species infection. A species that was unable to induce disease in potato was efficiently maintained and eventually became dominant in some of the communities tested, indicating that cheating can shape dominant species. Modeling indicates that the cost of PCWDEs production and secretion, the rate of potato degradation and the diffusion rate of degraded substrate could favor the cheater species. Interaction outcomes differed between potato tuber and synthetic medium, highlighting the driving effect of environmental conditions, with higher antagonistic interactions observed in potato tubers. Antagonistic interactions were strain specific and not species specific. Toxicity interference was also observed within some communities, allowing the maintenance of strains otherwise sensitive to toxic compounds. Overall, the results indicate that intraspecific competition, cooperation through trophic interaction and toxicity interference contribute to the maintenance of SRP diversity. The implications of these processes for epidemiological surveillance are discussed.

Published online:
DOI: 10.24072/pcjournal.418
Type: Research article

Barny, Marie-Anne 1; Thieffry, Sylvia 1; Gomes de Faria, Christelle 1; Thebault, Elisa 1; Pédron, Jacques 1

1 Sorbonne Université, INRAE, IRD, CNRS, UPEC, Institute of Ecology and Environmental Sciences-Paris (iEES-Paris), 4 place Jussieu, F-75252 Paris, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Barny, Marie-Anne; Thieffry, Sylvia; Gomes de Faria, Christelle; Thebault, Elisa; Pédron, Jacques. Bacterial pathogens dynamic during multi-species infections. Peer Community Journal, Volume 4 (2024), article  no. e49. doi : 10.24072/pcjournal.418. https://peercommunityjournal.org/articles/10.24072/pcjournal.418/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.microbiol.100082

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Arizala, D.; Arif, M. Genome-Wide Analyses Revealed Remarkable Heterogeneity in Pathogenicity Determinants, Antimicrobial Compounds, and CRISPR-Cas Systems of Complex Phytopathogenic Genus Pectobacterium, Pathogens, Volume 8 (2019) no. 4, p. 247 | DOI

[2] Babujee, L.; Apodaca, J.; Balakrishnan, V.; Liss, P.; Kiley, P. J.; Charkowski, A. O.; Glasner, J. D.; Perna, N. T. Evolution of the metabolic and regulatory networks associated with oxygen availability in two phytopathogenic enterobacteria, BMC Genomics, Volume 13 (2012) no. 1, p. 110 | DOI

[3] Bellieny-Rabelo, D.; Tanui, C. K.; Miguel, N.; Kwenda, S.; Shyntum, D. Y.; Moleleki, L. N. Transcriptome and Comparative Genomics Analyses Reveal New Functional Insights on Key Determinants of Pathogenesis and Interbacterial Competition in Pectobacterium and Dickeya spp, Applied and Environmental Microbiology, Volume 85 (2019) no. 2, p. e02050 | DOI

[4] Ben Moussa, H.; Bertrand, C.; Rochelle-Newall, E.; Fiorini, S.; Pédron, J.; Barny, M.-A. The Diversity and Abundance of Soft Rot Pectobacteriaceae Along the Durance River Stream in the Southeast of France Revealed by Multiple Seasonal Surveys, Phytopathology, Volume 112 (2022) no. 8, pp. 1676-1685 | DOI

[5] Ben Moussa, H.; Pédron, J.; Hugouvieux‐Cotte‐Pattat, N.; Barny, M. Two species with a peculiar evolution within the genus Pectobacterium suggest adaptation to a new environmental niche, Environmental Microbiology, Volume 25 (2023) no. 11, pp. 2465-2480 | DOI

[6] Blin, P.; Robic, K.; Khayi, S.; Cigna, J.; Munier, E.; Dewaegeneire, P.; Laurent, A.; Jaszczyszyn, Y.; Hong, K.; Chan, K.; Beury, A.; Reverchon, S.; Giraud, T.; Hélias, V.; Faure, D. Pattern and causes of the establishment of the invasive bacterial potato pathogen Dickeya solani and of the maintenance of the resident pathogen D. dianthicola, Molecular Ecology, Volume 30 (2021) no. 2, pp. 608-624 | DOI

[7] Brual, T.; Effantin, G.; Baltenneck, J.; Attaiech, L.; Grosbois, C.; Royer, M.; Cigna, J.; Faure, D.; Hugouvieux-Cotte-Pattat, N.; Gueguen, E. A natural single nucleotide mutation in the small regulatory RNA ArcZ of Dickeya solani switches off the antimicrobial activities against yeast and bacteria, PLOS Genetics, Volume 19 (2023) no. 4, p. e1010725 | DOI

[8] Chan, Y.-C.; Wu, J.-L.; Wu, H.-P.; Tzeng, K.-C.; Chuang, D.-Y. Cloning, purification, and functional characterization of Carocin S2, a ribonuclease bacteriocin produced by Pectobacterium carotovorum, BMC Microbiology, Volume 11 (2011) no. 1, p. 99 | DOI

[9] Charkowski, A. O. The Changing Face of Bacterial Soft-Rot Diseases, Annual Review of Phytopathology, Volume 56 (2018) no. 1, pp. 269-288 | DOI

[10] Cheng, Y.; Liu, X.; An, S.; Chang, C.; Zou, Y.; Huang, L.; Zhong, J.; Liu, Q.; Jiang, Z.; Zhou, J.; Zhang, L.-H. A Nonribosomal Peptide Synthase Containing a Stand-Alone Condensation Domain Is Essential for Phytotoxin Zeamine Biosynthesis, Molecular Plant-Microbe Interactions, Volume 26 (2013) no. 11, pp. 1294-1301 | DOI

[11] Chuang, D.-y.; Chien, Y.-c.; Wu, H.-P. Cloning and Expression of the Erwinia carotovora subsp. carotovora Gene Encoding the Low-Molecular-Weight Bacteriocin Carocin S1, Journal of Bacteriology, Volume 189 (2007) no. 2, pp. 620-626 | DOI

[12] Cigna, J.; Dewaegeneire, P.; Beury, A.; Gobert, V.; Faure, D. A gapA PCR-sequencing Assay for Identifying the Dickeya and Pectobacterium Potato Pathogens, Plant Disease, Volume 101 (2017) no. 7, pp. 1278-1282 | DOI

[13] Coulthurst, S. J.; Barnard, A. M. L.; Salmond, G. P. C. Regulation and biosynthesis of carbapenem antibiotics in bacteria, Nature Reviews Microbiology, Volume 3 (2005) no. 4, pp. 295-306 | DOI

[14] Curland, R. D.; Mainello, A.; Perry, K. L.; Hao, J.; Charkowski, A. O.; Bull, C. T.; McNally, R. R.; Johnson, S. B.; Rosenzweig, N.; Secor, G. A.; Larkin, R. P.; Gugino, B. K.; Ishimaru, C. A. Species of Dickeya and Pectobacterium Isolated during an Outbreak of Blackleg and Soft Rot of Potato in Northeastern and North Central United States, Microorganisms, Volume 9 (2021) no. 8, p. 1733 | DOI

[15] Czárán, T. L.; Hoekstra, R. F.; Pagie, L. Chemical warfare between microbes promotes biodiversity, Proceedings of the National Academy of Sciences, Volume 99 (2002) no. 2, pp. 786-790 | DOI

[16] Degefu, Y. Co-occurrence of latent Dickeya and Pectobacterium species in potato seed tuber samples from northern Finland, Agricultural and Food Science, Volume 30 (2021) no. 1 | DOI

[17] Ge, T.; Ekbataniamiri, F.; Johnson, S. B.; Larkin, R. P.; Hao, J. Interaction between Dickeya dianthicola and Pectobacterium parmentieri in Potato Infection under Field Conditions, Microorganisms, Volume 9 (2021) no. 2, p. 316 | DOI

[18] Gralka, M.; Szabo, R.; Stocker, R.; Cordero, O. X. Trophic Interactions and the Drivers of Microbial Community Assembly, Current Biology, Volume 30 (2020) no. 19, p. R1176-R1188 | DOI

[19] Grinter, R.; Milner, J.; Walker, D. Ferredoxin Containing Bacteriocins Suggest a Novel Mechanism of Iron Uptake in Pectobacterium spp, PLoS ONE, Volume 7 (2012) no. 3, p. e33033 | DOI

[20] Holden, M. T. G.; McGowan, S. J.; Bycroft, B. W.; Stewart, G. S. A. B.; Williams, P.; Salmond, G. P. C. Cryptic carbapenem antibiotic production genes are widespread in Erwinia carotovora: facile trans activation by the carR transcriptional regulator, Microbiology, Volume 144 (1998) no. 6, pp. 1495-1508 | DOI

[21] Hugouvieux-Cotte-Pattat, N.; Pédron, J.; Van Gijsegem, F. Insight into biodiversity of the recently rearranged genus Dickeya, Frontiers in Plant Science, Volume 14 (2023), p. 1168480 | DOI

[22] Hugouvieux-Cotte-Pattat, N.; des-Combes, C. J.; Briolay, J.; Pritchard, L. Proposal for the creation of a new genus Musicola gen. nov., reclassification of Dickeya paradisiaca (Samson et al. 2005) as Musicola paradisiaca comb. nov. and description of a new species Musicola keenii sp. nov., International Journal of Systematic and Evolutionary Microbiology, Volume 71 (2021) no. 10 | DOI

[23] Hugouvieux‐Cotte‐Pattat, N.; Condemine, G.; Shevchik, V. E. Bacterial pectate lyases, structural and functional diversity, Environmental Microbiology Reports, Volume 6 (2014) no. 5, pp. 427-440 | DOI

[24] Itoh, Y.; Izaki, K.; Takahashi, H. Purification And Characterization Of A Bacteriocin From Erwinia Carotovora, The Journal of General and Applied Microbiology, Volume 24 (1978) no. 1, pp. 27-39 | DOI

[25] Jonkheer, E. M.; Brankovics, B.; Houwers, I. M.; Van Der Wolf, J. M.; Bonants, P. J. M.; Vreeburg, R. A. M.; Bollema, R.; De Haan, J. R.; Berke, L.; Smit, S.; De Ridder, D.; Van Der Lee, T. A. J. The Pectobacterium pangenome, with a focus on Pectobacterium brasiliense, shows a robust core and extensive exchange of genes from a shared gene pool, BMC Genomics, Volume 22 (2021) no. 1, p. 265 | DOI

[26] Kelsic, E. D.; Zhao, J.; Vetsigian, K.; Kishony, R. Counteraction of antibiotic production and degradation stabilizes microbial communities, Nature, Volume 521 (2015) no. 7553, pp. 516-519 | DOI

[27] Khayi, S.; Blin, P.; Pédron, J.; Chong, T.-M.; Chan, K.-G.; Moumni, M.; Hélias, V.; Van Gijsegem, F.; Faure, D. Population genomics reveals additive and replacing horizontal gene transfers in the emerging pathogen Dickeya solani, BMC Genomics, Volume 16 (2015) no. 1, p. 788 | DOI

[28] Li, X.; Ma, Y.; Liang, S.; Tian, Y.; Yin, S.; Xie, S.; Xie, H. Comparative genomics of 84 Pectobacterium genomes reveals the variations related to a pathogenic lifestyle, BMC Genomics, Volume 19 (2018) no. 1, p. 889 | DOI

[29] Ma, B.; Hibbing, M. E.; Kim, H.-S.; Reedy, R. M.; Yedidia, I.; Breuer, J.; Breuer, J.; Glasner, J. D.; Perna, N. T.; Kelman, A.; Charkowski, A. O. Host Range and Molecular Phylogenies of the Soft Rot Enterobacterial Genera Pectobacterium and Dickeya, Phytopathology, Volume 97 (2007) no. 9, pp. 1150-1163 | DOI

[30] Ma, X.; Brazil, J.; Rivedal, H.; Perry, K. L.; Frost, K.; Swingle, B. First Report of Pectobacterium versatile Causing Potato Soft Rot in Oregon and Washington, Plant Disease, Volume 106 (2022) no. 4, p. 1292 | DOI

[31] Mansfield, J.; Genin, S.; Magori, S.; Citovsky, V.; Sriariyanum, M.; Ronald, P.; Dow, M.; Verdier, V.; Beer, S. V.; Machado, M. A.; Toth, I.; Salmond, G.; Foster, G. D. Top 10 plant pathogenic bacteria in molecular plant pathology, Molecular Plant Pathology, Volume 13 (2012) no. 6, pp. 614-629 | DOI

[32] Mattinen, L.; Nissinen, R.; Riipi, T.; Kalkkinen, N.; Pirhonen, M. Host‐extract induced changes in the secretome of the plant pathogenic bacterium Pectobacterium atrosepticum , PROTEOMICS, Volume 7 (2007) no. 19, pp. 3527-3537 | DOI

[33] McGowan, S. J.; Sebaihia, M.; O'Leary, S.; Hardie, K. R.; Williams, P.; Stewart, G. S. A. B.; Bycroft, B. W.; Salmond, G. P. C. Analysis of the carbapenem gene cluster of Erwinia carotovora : definition of the antibiotic biosynthetic genes and evidence for a novel β‐lactam resistance mechanism, Molecular Microbiology, Volume 26 (1997) no. 3, pp. 545-556 | DOI

[34] Motyka-Pomagruk, A.; Zoledowska, S.; Sledz, W.; Lojkowska, E. The occurrence of bacteria from different species of Pectobacteriaceae on seed potato plantations in Poland, European Journal of Plant Pathology, Volume 159 (2021) no. 2, pp. 309-325 | DOI

[35] Nguyen, A. H.; Tomita, T.; Hirota, M.; Sato, T.; Kamio, Y. A Simple Purification Method and Morphology and Component Analyses for Carotovoricin Er, a Phage-tail-like Bacteriocin from the Plant Pathogen Erwinia carotovora Er, Bioscience, Biotechnology, and Biochemistry, Volume 63 (1999) no. 8, pp. 1360-1369 | DOI

[36] Pasanen, M.; Waleron, M.; Schott, T.; Cleenwerck, I.; Misztak, A.; Waleron, K.; Pritchard, L.; Bakr, R.; Degefu, Y.; Van Der Wolf, J.; Vandamme, P.; Pirhonen, M. Pectobacterium parvum sp. nov., having a Salmonella SPI-1-like Type III secretion system and low virulence, International Journal of Systematic and Evolutionary Microbiology, Volume 70 (2020) no. 4, pp. 2440-2448 | DOI

[37] Pédron, J.; Thieffry, S.; de Faria, C.; Thebault, E.; Barny, M.-A. Bacterial pathogens dynamic during multi-species infections: Supplementals, Zenodo (2024) | DOI

[38] Pédron, J.; Thieffry, S.; de Faria, C.; Thebault, E.; Barny, M.-A. Bacterial pathogens dynamic during multi-species infections, Zenodo (2023) | DOI

[39] Pédron, J.; Bertrand, C.; Taghouti, G.; Portier, P.; Barny, M.-A. Pectobacterium aquaticum sp. nov., isolated from waterways, International Journal of Systematic and Evolutionary Microbiology, Volume 69 (2019) no. 3, pp. 745-751 | DOI

[40] Portier, P.; Pédron, J.; Taghouti, G.; Dutrieux, C.; Barny, M.-A. Updated Taxonomy of Pectobacterium Genus in the CIRM-CFBP Bacterial Collection: When Newly Described Species Reveal “Old” Endemic Population, Microorganisms, Volume 8 (2020) no. 9, p. 1441 | DOI

[41] Portier, P.; Pédron, J.; Taghouti, G.; Fischer-Le Saux, M.; Caullireau, E.; Bertrand, C.; Laurent, A.; Chawki, K.; Oulgazi, S.; Moumni, M.; Andrivon, D.; Dutrieux, C.; Faure, D.; Hélias, V.; Barny, M.-A. Elevation of Pectobacterium carotovorum subsp. odoriferum to species level as Pectobacterium odoriferum sp. nov., proposal of Pectobacterium brasiliense sp. nov. and Pectobacterium actinidiae sp. nov., emended description of Pectobacterium carotovorum and description of Pectobacterium versatile sp. nov., isolated from streams and symptoms on diverse plants, International Journal of Systematic and Evolutionary Microbiology, Volume 69 (2019) no. 10, pp. 3207-3216 | DOI

[42] Roh, E.; Park, T.-H.; Kim, M.-i.; Lee, S.; Ryu, S.; Oh, C.-S.; Rhee, S.; Kim, D.-H.; Park, B.-S.; Heu, S. Characterization of a New Bacteriocin, Carocin D, from Pectobacterium carotovorum subsp. carotovorum Pcc21, Applied and Environmental Microbiology, Volume 76 (2010) no. 22, pp. 7541-7549 | DOI

[43] Royer, G.; Dixit, Z.; Pédron, J.; Pierrat, G.; Demontant, V.; Berçot, B.; Rodriguez, C.; Barny, M.-A.; Jacquier, H.; Woerther, P.-L. Genetic and Phenotypic Study of the Pectobacterium versatile Beta-Lactamase, the Enzyme Most Similar to the Plasmid-Encoded TEM-1, Applied and Environmental Microbiology, Volume 88 (2022) no. 11, pp. e00220-22 | DOI

[44] Shyntum, D. Y.; Nkomo, N. P.; Shingange, N. L.; Gricia, A. R.; Bellieny-Rabelo, D.; Moleleki, L. N. The Impact of Type VI Secretion System, Bacteriocins and Antibiotics on Bacterial Competition of Pectobacterium carotovorum subsp. brasiliense and the Regulation of Carbapenem Biosynthesis by Iron and the Ferric-Uptake Regulator, Frontiers in Microbiology, Volume 10 (2019), p. 2379 | DOI

[45] Smoktunowicz, M.; Jonca, J.; Stachowska, A.; May, M.; Waleron, M. M.; Waleron, M.; Waleron, K. The International Trade of Ware Vegetables and Orna-Mental Plants—An Underestimated Risk of Accelerated Spreading of Phytopathogenic Bacteria in the Era of Globalisation and Ongoing Climatic Changes, Pathogens, Volume 11 (2022) no. 7, p. 728 | DOI

[46] Taillefumier, T.; Posfai, A.; Meir, Y.; Wingreen, N. S. Microbial consortia at steady supply, eLife, Volume 6 (2017), p. e22644 | DOI

[47] Toth, I. K.; Barny, M.-a.; Brurberg, M. B.; Condemine, G.; Czajkowski, R.; Elphinstone, J. G.; Helias, V.; Johnson, S. B.; Moleleki, L. N.; Pirhonen, M.; Rossmann, S.; Tsror, L.; Van Der Waals, J. E.; Van Der Wolf, J. M.; Van Gijsegem, F.; Yedidia, I. Pectobacterium and Dickeya: Environment to Disease Development, Plant Diseases Caused by Dickeya and Pectobacterium Species, Springer International Publishing, Cham, 2021, pp. 39-84 | DOI

[48] Weiss, A. S.; Burrichter, A. G.; Durai Raj, A. C.; Von Strempel, A.; Meng, C.; Kleigrewe, K.; Münch, P. C.; Rössler, L.; Huber, C.; Eisenreich, W.; Jochum, L. M.; Göing, S.; Jung, K.; Lincetto, C.; Hübner, J.; Marinos, G.; Zimmermann, J.; Kaleta, C.; Sanchez, A.; Stecher, B. In vitro interaction network of a synthetic gut bacterial community, The ISME Journal, Volume 16 (2022) no. 4, pp. 1095-1109 | DOI

[49] De Werra, P.; Debonneville, C.; Kellenberger, I.; Dupuis, B. Pathogenicity and Relative Abundance of Dickeya and Pectobacterium Species in Switzerland: An Epidemiological Dichotomy, Microorganisms, Volume 9 (2021) no. 11, p. 2270 | DOI

[50] van der Wolf, J. M.; Acuña, I.; De Boer, S. H.; Brurberg, M. B.; Cahill, G.; Charkowski, A. O.; Coutinho, T.; Davey, T.; Dees, M. W.; Degefu, Y.; Dupuis, B.; Elphinstone, J. G.; Fan, J.; Fazelisanagri, E.; Fleming, T.; Gerayeli, N.; Gorshkov, V.; Helias, V.; le Hingrat, Y.; Johnson, S. B.; Keiser, A.; Kellenberger, I.; Li, X.; Lojkowska, E.; Martin, R.; Perminow, J. I.; Petrova, O.; Motyka-Pomagruk, A.; Rossmann, S.; Schaerer, S.; Sledz, W.; Toth, I. K.; Tsror, L.; van der Waals, J. E.; de Werra, P.; Yedidia, I. Diseases Caused by Pectobacterium and Dickeya Species Around the World, Plant Diseases Caused by Dickeya and Pectobacterium Species (eds Van Gijsegem F, van der Wolf JM, Toth IK), Springer International Publishing, Cham, 2021, pp. 215-261 | DOI

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