Bacterial pathogens dynamic during multi-species infections

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 tuber...

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Main Authors: Barny, Marie-Anne, Thieffry, Sylvia, Gomes de Faria, Christelle, Thebault, Elisa, Pédron, Jacques
Format: Article
Language:English
Published: Peer Community In 2024-05-01
Series:Peer Community Journal
Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.418/
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author Barny, Marie-Anne
Thieffry, Sylvia
Gomes de Faria, Christelle
Thebault, Elisa
Pédron, Jacques
author_facet Barny, Marie-Anne
Thieffry, Sylvia
Gomes de Faria, Christelle
Thebault, Elisa
Pédron, Jacques
author_sort Barny, Marie-Anne
collection DOAJ
description 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.
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spelling doaj-art-15a87a51d0e44c3180259ebc671b33392025-02-07T10:17:18ZengPeer Community InPeer Community Journal2804-38712024-05-01410.24072/pcjournal.41810.24072/pcjournal.418Bacterial pathogens dynamic during multi-species infections Barny, Marie-Anne0https://orcid.org/0000-0002-2005-1388Thieffry, Sylvia1Gomes de Faria, Christelle2Thebault, Elisa3Pédron, Jacques4Sorbonne Université, INRAE, IRD, CNRS, UPEC, Institute of Ecology and Environmental Sciences-Paris (iEES-Paris), 4 place Jussieu, F-75252 Paris, FranceSorbonne Université, INRAE, IRD, CNRS, UPEC, Institute of Ecology and Environmental Sciences-Paris (iEES-Paris), 4 place Jussieu, F-75252 Paris, FranceSorbonne Université, INRAE, IRD, CNRS, UPEC, Institute of Ecology and Environmental Sciences-Paris (iEES-Paris), 4 place Jussieu, F-75252 Paris, FranceSorbonne Université, INRAE, IRD, CNRS, UPEC, Institute of Ecology and Environmental Sciences-Paris (iEES-Paris), 4 place Jussieu, F-75252 Paris, FranceSorbonne Université, INRAE, IRD, CNRS, UPEC, Institute of Ecology and Environmental Sciences-Paris (iEES-Paris), 4 place Jussieu, F-75252 Paris, FranceSoft 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. https://peercommunityjournal.org/articles/10.24072/pcjournal.418/
spellingShingle Barny, Marie-Anne
Thieffry, Sylvia
Gomes de Faria, Christelle
Thebault, Elisa
Pédron, Jacques
Bacterial pathogens dynamic during multi-species infections
Peer Community Journal
title Bacterial pathogens dynamic during multi-species infections
title_full Bacterial pathogens dynamic during multi-species infections
title_fullStr Bacterial pathogens dynamic during multi-species infections
title_full_unstemmed Bacterial pathogens dynamic during multi-species infections
title_short Bacterial pathogens dynamic during multi-species infections
title_sort bacterial pathogens dynamic during multi species infections
url https://peercommunityjournal.org/articles/10.24072/pcjournal.418/
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