Alicia I Pérez-Lorente, Carlos Molina-Santiago, David Vela-Corcía, Paolo Stincone, Jesús Hierrezuelo, Montserrat Grifé, Abzer K Pakkir Shah, Antonio de Vicente, Daniel Petras, Diego Romero
Bacterial–fungal interactions have traditionally been attributed to secondary metabolites, but the role of the bacterial extracellular matrix in shaping these relationships has remained unclear. Here, we demonstrate that the extracellular matrix protein TasA is a key mediator in the antagonistic interaction between Bacillus subtilis and Botrytis cinerea. TasA enables Bacillus to tightly adhere to fungal hyphae, disrupts the β-glucan layer, and compromises fungal cytoskeletal integrity synergistically with fengycin, which causes cytological damage. Additionally, TasA acts as a carrier for bacillaene, amplifying its fungistatic activity. In response, Botrytis mounts a multifaceted defense, enzymatically degrading fengycin, producing antibacterial oxylipins, and activating adaptive programs such as hyphal branching and chlamydospore formation. Our findings reveal the previously unrecognized role of extracellular matrix components in fungal suppression and the modulation of fungal adaptive responses. This study reveals the complex interplay between microbial aggression and defense, providing new insights into the ecological dynamics of microbial competition and coexistence.
{"title":"Offensive role of the Bacillus extracellular matrix in driving metabolite-mediated dialogue and adaptive strategies with the fungus Botrytis","authors":"Alicia I Pérez-Lorente, Carlos Molina-Santiago, David Vela-Corcía, Paolo Stincone, Jesús Hierrezuelo, Montserrat Grifé, Abzer K Pakkir Shah, Antonio de Vicente, Daniel Petras, Diego Romero","doi":"10.1093/ismejo/wraf277","DOIUrl":"https://doi.org/10.1093/ismejo/wraf277","url":null,"abstract":"Bacterial–fungal interactions have traditionally been attributed to secondary metabolites, but the role of the bacterial extracellular matrix in shaping these relationships has remained unclear. Here, we demonstrate that the extracellular matrix protein TasA is a key mediator in the antagonistic interaction between Bacillus subtilis and Botrytis cinerea. TasA enables Bacillus to tightly adhere to fungal hyphae, disrupts the β-glucan layer, and compromises fungal cytoskeletal integrity synergistically with fengycin, which causes cytological damage. Additionally, TasA acts as a carrier for bacillaene, amplifying its fungistatic activity. In response, Botrytis mounts a multifaceted defense, enzymatically degrading fengycin, producing antibacterial oxylipins, and activating adaptive programs such as hyphal branching and chlamydospore formation. Our findings reveal the previously unrecognized role of extracellular matrix components in fungal suppression and the modulation of fungal adaptive responses. This study reveals the complex interplay between microbial aggression and defense, providing new insights into the ecological dynamics of microbial competition and coexistence.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"12 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145770675","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Bradyrhizobium and Sinorhizobium are dominant soybean microsymbionts in acidic/neutral and alkaline soils, respectively. However, the molecular mechanisms underlying this pH-dependent adaptation remain elusive. In this study, phylogenomic analysis of 286 Bradyrhizobium and 322 Sinorhizobium genomes revealed that Bradyrhizobium possesses abundant xeno-siderophore receptors but has limited siderophore biosynthesis functions. In contrast, gene clusters directing siderophore biosynthesis are enriched in Sinorhizobium. As siderophores can chelate the prevalent insoluble Fe3+ under neutral and alkaline conditions, whereas being less important in acidic environments where soluble Fe2+ is readily accessible, we hypothesized that the genus-dependent phyletic distribution of siderophore biosynthesis and exploitation functions may contribute to the pH adaptation of these two genera. Indeed, Bradyrhizobium species barely grow under iron-limiting conditions, and this growth defect can be rescued by xeno-siderophores produced by Sinorhizobium. Using a xeno-siderophore-exploiting Bradyrhizobium diazoefficiens strain, an engineered xeno-siderophore exploiter, and an altruistic siderophore-producing strain derived from Sinorhizobium fredii, we revealed the competitive advantage of xeno-siderophore exploitation during soybean nodulation. Heterologous expression of certain Bradyrhizobium xeno-siderophore receptors, along with various adaptive mutations in the genome of the S. fredii receptor-lacking mutant, allowed this mutant to rapidly restore growth under iron-limiting conditions. These adaptive events in experimental evolution depend on the siderophore biosynthetic function of S. fredii. Taken together, these findings suggest that the siderophore utilization ability of soybean rhizobia can be positively selected under iron-limiting conditions: by maintaining abundant xeno-siderophore receptors in acid-tolerant Bradyrhizobium and by the rapid adaptive evolution of utilization machinery for self-produced siderophores in alkaline-tolerant Sinorhizobium.
{"title":"Evolution of rhizobial siderophore utilization via accessory xeno-siderophore receptors and flexible intake machinery for self-produced siderophores","authors":"You-Wei Si, Miao-Di Feng, Bo-Sen Yang, Yi-Ning Liu, Ke-Han Liu, Yin Wang, Jian Jiao, Chang-Fu Tian","doi":"10.1093/ismejo/wraf280","DOIUrl":"https://doi.org/10.1093/ismejo/wraf280","url":null,"abstract":"Bradyrhizobium and Sinorhizobium are dominant soybean microsymbionts in acidic/neutral and alkaline soils, respectively. However, the molecular mechanisms underlying this pH-dependent adaptation remain elusive. In this study, phylogenomic analysis of 286 Bradyrhizobium and 322 Sinorhizobium genomes revealed that Bradyrhizobium possesses abundant xeno-siderophore receptors but has limited siderophore biosynthesis functions. In contrast, gene clusters directing siderophore biosynthesis are enriched in Sinorhizobium. As siderophores can chelate the prevalent insoluble Fe3+ under neutral and alkaline conditions, whereas being less important in acidic environments where soluble Fe2+ is readily accessible, we hypothesized that the genus-dependent phyletic distribution of siderophore biosynthesis and exploitation functions may contribute to the pH adaptation of these two genera. Indeed, Bradyrhizobium species barely grow under iron-limiting conditions, and this growth defect can be rescued by xeno-siderophores produced by Sinorhizobium. Using a xeno-siderophore-exploiting Bradyrhizobium diazoefficiens strain, an engineered xeno-siderophore exploiter, and an altruistic siderophore-producing strain derived from Sinorhizobium fredii, we revealed the competitive advantage of xeno-siderophore exploitation during soybean nodulation. Heterologous expression of certain Bradyrhizobium xeno-siderophore receptors, along with various adaptive mutations in the genome of the S. fredii receptor-lacking mutant, allowed this mutant to rapidly restore growth under iron-limiting conditions. These adaptive events in experimental evolution depend on the siderophore biosynthetic function of S. fredii. Taken together, these findings suggest that the siderophore utilization ability of soybean rhizobia can be positively selected under iron-limiting conditions: by maintaining abundant xeno-siderophore receptors in acid-tolerant Bradyrhizobium and by the rapid adaptive evolution of utilization machinery for self-produced siderophores in alkaline-tolerant Sinorhizobium.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"43 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145777829","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Leonardo Mancini, Laila Saliekh, Rory Claydon, Jurij Kotar, Eva Bernadett Benyei, Carol A Munro, Tyler N Shendruk, Aidan Brown, Martin Welch, Pietro Cicuta
The bodies of macroorganisms host microbes living in multi-species communities. Sequencing approaches have revealed that different organs host different microbiota and tend to be infected by different pathogens, drawing correlations between environmental parameters at the organ level and microbial composition. However, less is known about the microscale dimension of microbial ecology, particularly during infection. In this study, we focus on the role of microscale spatial structure, studying its influence on the ecology of a polymicrobial infection of P. aeruginosa, S. aureus, and C. albicans. Although these pathogens are commonly found together in the lungs of chronically ill patients, it is unclear whether they coexist or compete and segregate in different niches. We find that, whereas P. aeruginosa quickly outcompetes C. albicans and S. aureus on large surfaces, robust spatial organization and coexistence emerges in spatially structured microenvironments. In confined spaces, slowly growing C. albicans is able to leverage rapid radial hyphal growth to conquer boundaries, where it establishes itself displacing the other pathogens. Similar outcomes are observed when the P. aeruginosa strain carries mexT-inactivating mutations, which are often found in clinical isolates. The observed spatial organization enables coexistence and potentially determines infection severity and outcomes. Our findings reveal a previously unrecognized role of mechanical forces in shaping infection dynamics, suggesting that microenvironmental structure might be a critical determinant of pathogen coexistence, virulence, and treatment outcomes. Because adaptations, such as changes in morphology, are widespread among microbes, these results are generalizable to other ecologies and environments.
{"title":"Hyphal growth determines spatial organization and coexistence in a pathogenic polymicrobial community in a spatially structured environment","authors":"Leonardo Mancini, Laila Saliekh, Rory Claydon, Jurij Kotar, Eva Bernadett Benyei, Carol A Munro, Tyler N Shendruk, Aidan Brown, Martin Welch, Pietro Cicuta","doi":"10.1093/ismejo/wraf279","DOIUrl":"https://doi.org/10.1093/ismejo/wraf279","url":null,"abstract":"The bodies of macroorganisms host microbes living in multi-species communities. Sequencing approaches have revealed that different organs host different microbiota and tend to be infected by different pathogens, drawing correlations between environmental parameters at the organ level and microbial composition. However, less is known about the microscale dimension of microbial ecology, particularly during infection. In this study, we focus on the role of microscale spatial structure, studying its influence on the ecology of a polymicrobial infection of P. aeruginosa, S. aureus, and C. albicans. Although these pathogens are commonly found together in the lungs of chronically ill patients, it is unclear whether they coexist or compete and segregate in different niches. We find that, whereas P. aeruginosa quickly outcompetes C. albicans and S. aureus on large surfaces, robust spatial organization and coexistence emerges in spatially structured microenvironments. In confined spaces, slowly growing C. albicans is able to leverage rapid radial hyphal growth to conquer boundaries, where it establishes itself displacing the other pathogens. Similar outcomes are observed when the P. aeruginosa strain carries mexT-inactivating mutations, which are often found in clinical isolates. The observed spatial organization enables coexistence and potentially determines infection severity and outcomes. Our findings reveal a previously unrecognized role of mechanical forces in shaping infection dynamics, suggesting that microenvironmental structure might be a critical determinant of pathogen coexistence, virulence, and treatment outcomes. Because adaptations, such as changes in morphology, are widespread among microbes, these results are generalizable to other ecologies and environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"5 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145770679","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ronja Marlonsdotter Sandholm, Gordon Jacob Boehlich, Ørjan Dahl, Ravindra R Chowreddy, Anton Stepnov, Gustav Vaaje-Kolstad, Sabina Leanti La Rosa
Plastics are widely used materials, yet their chemical stability hinders biodegradation, exacerbating pollution on a global scale. Contaminated soils may foster microbes adapted to degrade plastics or derivatives, and these organisms and their enzymes offer promising avenues for the development of biotechnological recycling strategies. Here, two microbial communities originating from soil collected at a plastic-contaminated site in Norway were enriched to select for bacteria involved in the decomposition of a widely used, model polyethylene (low molecular weight, LMWPE; average carbon chain length of 279). We leveraged genome-resolved metatranscriptomics to identify active population affiliated with Acinetobacter guillouiae and Pseudomonas sp., showing a suite of upregulated genes (including those encoding alkane 1-monooxygenases, Baeyer-Villiger monooxygenases, cytochrome P450 monooxygenases) with functions compatible with degradation of medium- and long-chain hydrocarbons and their oxidized derivatives. Spectroscopic, spectrometric and chromatographic analyses revealed the unexpected presence of medium- (C10–16) and long-chain (C17–34) alkanes and 2-ketones in the LMWPE substrate, preventing the erroneous conclusion that the microbial community was degrading the polymeric component. Consistently, only alkanes and 2-ketones of C10–27 were selectively degraded by an A. guillouiae isolate, as confirmed by proteomics analyses and substrate characterization following bacterial growth. Besides extending the knowledge on the enzymatic toolbox of soil-associated microbial systems for degrading alkanes and ketones likely arising from abiotic oxidation of polymeric LMWPE, our results provide an advanced compositional characterization of a widely used model “PE,” while offering valuable insight to support future studies aimed at unequivocally identifying organisms and their enzymes implicated in PE transformation.
{"title":"Microbial degradation of a widely used model polyethylene is restricted to medium- and long-chain alkanes and their oxidized derivatives","authors":"Ronja Marlonsdotter Sandholm, Gordon Jacob Boehlich, Ørjan Dahl, Ravindra R Chowreddy, Anton Stepnov, Gustav Vaaje-Kolstad, Sabina Leanti La Rosa","doi":"10.1093/ismejo/wraf276","DOIUrl":"https://doi.org/10.1093/ismejo/wraf276","url":null,"abstract":"Plastics are widely used materials, yet their chemical stability hinders biodegradation, exacerbating pollution on a global scale. Contaminated soils may foster microbes adapted to degrade plastics or derivatives, and these organisms and their enzymes offer promising avenues for the development of biotechnological recycling strategies. Here, two microbial communities originating from soil collected at a plastic-contaminated site in Norway were enriched to select for bacteria involved in the decomposition of a widely used, model polyethylene (low molecular weight, LMWPE; average carbon chain length of 279). We leveraged genome-resolved metatranscriptomics to identify active population affiliated with Acinetobacter guillouiae and Pseudomonas sp., showing a suite of upregulated genes (including those encoding alkane 1-monooxygenases, Baeyer-Villiger monooxygenases, cytochrome P450 monooxygenases) with functions compatible with degradation of medium- and long-chain hydrocarbons and their oxidized derivatives. Spectroscopic, spectrometric and chromatographic analyses revealed the unexpected presence of medium- (C10–16) and long-chain (C17–34) alkanes and 2-ketones in the LMWPE substrate, preventing the erroneous conclusion that the microbial community was degrading the polymeric component. Consistently, only alkanes and 2-ketones of C10–27 were selectively degraded by an A. guillouiae isolate, as confirmed by proteomics analyses and substrate characterization following bacterial growth. Besides extending the knowledge on the enzymatic toolbox of soil-associated microbial systems for degrading alkanes and ketones likely arising from abiotic oxidation of polymeric LMWPE, our results provide an advanced compositional characterization of a widely used model “PE,” while offering valuable insight to support future studies aimed at unequivocally identifying organisms and their enzymes implicated in PE transformation.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"14 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145760142","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Predation is a top-down regulator of ecosystem integrity and a key driver of community structure and evolution in plants and animals. Despite our awareness of these dynamics, our understanding of microbial top-down control by bacterial predators remains limited. Predatory Halobacteriovorax bacteria are common, low abundance members of many marine and estuarine microbiomes and are considered generalists with less specific prey ranges than most viruses, yet more selective targets than antibiotics. This "Goldilocks" prey range has huge potential to treat polymicrobial infections, particularly in complex microbiomes; however, few studies employing Halobacteriovorax as a tool to manipulate dysbiotic microbiomes have been pursued. We developed a single-pathogen disease mitigation model in the critically endangered Caribbean coral, Acropora cervicornis. We employed a strain of the highly versatile Vibrio coralliilyticus as our pathogen, which causes rapid tissue loss and death in stony corals and mortality in oyster larvae. To demonstrate that predatory bacteria can alter disease dynamics in corals we infected A. cervicornis with virulent V. coralliilyticus and upon the first signs of disease, treated corals with Halobacteriovorax cultures. Without predators, 100% of corals were bleached by 48 hours and 86% displayed tissue loss within five days; however with Halobacteriovorax, 57% of corals did not bleach beyond the inoculation site and no tissue loss was observed. This living probiotic successfully halted Vibrio-induced disease progression in A. cervicornis, suggesting that predatory bacteria broadly function as top-down regulators of community dynamics in eukaryotic microbiomes and microbial predators are a promising coral disease therapy.
{"title":"Halobacteriovorax halts disease progression in endangered Caribbean corals.","authors":"Lauren Speare,Chloe Manley,Sunni Patton,Eddie Fuques,Macey Coppinger,Rebecca Vega Thurber","doi":"10.1093/ismejo/wraf270","DOIUrl":"https://doi.org/10.1093/ismejo/wraf270","url":null,"abstract":"Predation is a top-down regulator of ecosystem integrity and a key driver of community structure and evolution in plants and animals. Despite our awareness of these dynamics, our understanding of microbial top-down control by bacterial predators remains limited. Predatory Halobacteriovorax bacteria are common, low abundance members of many marine and estuarine microbiomes and are considered generalists with less specific prey ranges than most viruses, yet more selective targets than antibiotics. This \"Goldilocks\" prey range has huge potential to treat polymicrobial infections, particularly in complex microbiomes; however, few studies employing Halobacteriovorax as a tool to manipulate dysbiotic microbiomes have been pursued. We developed a single-pathogen disease mitigation model in the critically endangered Caribbean coral, Acropora cervicornis. We employed a strain of the highly versatile Vibrio coralliilyticus as our pathogen, which causes rapid tissue loss and death in stony corals and mortality in oyster larvae. To demonstrate that predatory bacteria can alter disease dynamics in corals we infected A. cervicornis with virulent V. coralliilyticus and upon the first signs of disease, treated corals with Halobacteriovorax cultures. Without predators, 100% of corals were bleached by 48 hours and 86% displayed tissue loss within five days; however with Halobacteriovorax, 57% of corals did not bleach beyond the inoculation site and no tissue loss was observed. This living probiotic successfully halted Vibrio-induced disease progression in A. cervicornis, suggesting that predatory bacteria broadly function as top-down regulators of community dynamics in eukaryotic microbiomes and microbial predators are a promising coral disease therapy.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"39 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145710770","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The hadal trenches, the deepest regions of the ocean, serve as the final sinks for marine particles and "tunnels" for material exchange between the ocean and Earth's interior. Despite their extreme conditions, the trench sediments contain high content of organic carbon and active microbial carbon turnover, are hotspots for deep-sea organic carbon degradation and unique microbial processes. However, little is known about the organic carbon components and microbial metabolisms driving their degradation in trench sediments. This study provides the first comprehensive quantification of total halogenated organic compounds (organohalides) in Mariana Trench sediments. The measured bulk organic halogen concentrations exceeded all previously reported individual compounds by orders of magnitude, with a mean stoichiometric ratio of 1:49 (halogen:carbon) in the sedimentary organic carbon pool. These findings suggest the trench sediments may represent a significant reservoir for organohalides. Metagenomic analysis of global ocean data shows significant enrichment of the genes for organohalides biodegradation (dehalogenation) in trench microbiomes than those in other marine environments. Putative dehalogenating microorganisms in trench sediments encompassed 16 phyla and 52 orders, capable of metabolizing 18 structurally diverse organohalide compounds, revealing an unexpectedly broad phylogenetic distribution of organohalides metabolism and versatile substrate specificity among trench microbial communities. High pressure microcosm experiments demonstrated rapid degradation of typical organohalide compounds and transcription of genes related to organohalides metabolisms, confirming an active organohalides degradation by trench microorganisms. These findings underscore the role of organohalides metabolism in organic carbon remineralization in hadal trenches, advancing our understanding of deep-sea carbon cycling and microbial survival.
{"title":"Extensive halogenated organic compound reservoirs and active microbial dehalogenation in Mariana Trench sediments.","authors":"Rulong Liu,Hui Wei,Zhiao Xu,Yuheng Liu,Jiani He,Zhixuan Wang,Li Wang,Min Luo,Jiasong Fang,Federico Baltar,Yunping Xu,Qirui Liang,Liting Huang","doi":"10.1093/ismejo/wraf273","DOIUrl":"https://doi.org/10.1093/ismejo/wraf273","url":null,"abstract":"The hadal trenches, the deepest regions of the ocean, serve as the final sinks for marine particles and \"tunnels\" for material exchange between the ocean and Earth's interior. Despite their extreme conditions, the trench sediments contain high content of organic carbon and active microbial carbon turnover, are hotspots for deep-sea organic carbon degradation and unique microbial processes. However, little is known about the organic carbon components and microbial metabolisms driving their degradation in trench sediments. This study provides the first comprehensive quantification of total halogenated organic compounds (organohalides) in Mariana Trench sediments. The measured bulk organic halogen concentrations exceeded all previously reported individual compounds by orders of magnitude, with a mean stoichiometric ratio of 1:49 (halogen:carbon) in the sedimentary organic carbon pool. These findings suggest the trench sediments may represent a significant reservoir for organohalides. Metagenomic analysis of global ocean data shows significant enrichment of the genes for organohalides biodegradation (dehalogenation) in trench microbiomes than those in other marine environments. Putative dehalogenating microorganisms in trench sediments encompassed 16 phyla and 52 orders, capable of metabolizing 18 structurally diverse organohalide compounds, revealing an unexpectedly broad phylogenetic distribution of organohalides metabolism and versatile substrate specificity among trench microbial communities. High pressure microcosm experiments demonstrated rapid degradation of typical organohalide compounds and transcription of genes related to organohalides metabolisms, confirming an active organohalides degradation by trench microorganisms. These findings underscore the role of organohalides metabolism in organic carbon remineralization in hadal trenches, advancing our understanding of deep-sea carbon cycling and microbial survival.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"141 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145710792","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plasmids are mobile genetic elements that drive horizontal gene transfer among bacteria, influencing microbial community composition and functional traits in marine ecosystems. However, many marine plasmids remain unclassified due to unknown replication mechanisms. Here, we describe VBR1, a novel plasmid replicon family, widespread among species of the family Vibrionaceae. The minimal VBR1 replicon comprises a 570-bp AT-rich origin of replication (oriV) and two genes, vrp1AB, sufficient for autonomous replication in Escherichia coli and Photobacterium damselae. A comprehensive GenBank search revealed 158 previously untyped plasmids from Vibrionaceae species worldwide harboring this replicon, including relevant pathogens for animals and humans as well as environmental species. VBR1 plasmids share a syntenic set of backbone genes, are predominantly conjugative, and frequently encode antimicrobial resistance (AMR) genes, conferring resistance to multiple antibiotic classes. Most VBR1 plasmids also carry phage defense and anti-defense systems, underscoring their ecological and evolutionary significance. AMR and defense/antidefense gene repertoires are highly variable across VBR1 plasmids, suggesting frequent gene acquisition, recombination events, and rapid replacement and diversification of resistance and defense determinants. The co-localization of AMR and phage defense systems on many VBR1 plasmids highlights their role in shaping virus-host interactions and microbial community dynamics. Our findings establish VBR1 as a widespread, clinically and ecologically relevant replicon family, providing a framework for the classification and surveillance of previously orphan plasmids, and advancing our understanding of AMR and phage resistance dynamics in marine ecosystems.
{"title":"Replicon Family of Vibrionaceae Plasmids as a Reservoir of Antimicrobial and Phage Resistance Genes in Marine Ecosystems.","authors":"Soraya Fraga-Pampín,Carlos R Osorio,Ana Vences","doi":"10.1093/ismejo/wraf274","DOIUrl":"https://doi.org/10.1093/ismejo/wraf274","url":null,"abstract":"Plasmids are mobile genetic elements that drive horizontal gene transfer among bacteria, influencing microbial community composition and functional traits in marine ecosystems. However, many marine plasmids remain unclassified due to unknown replication mechanisms. Here, we describe VBR1, a novel plasmid replicon family, widespread among species of the family Vibrionaceae. The minimal VBR1 replicon comprises a 570-bp AT-rich origin of replication (oriV) and two genes, vrp1AB, sufficient for autonomous replication in Escherichia coli and Photobacterium damselae. A comprehensive GenBank search revealed 158 previously untyped plasmids from Vibrionaceae species worldwide harboring this replicon, including relevant pathogens for animals and humans as well as environmental species. VBR1 plasmids share a syntenic set of backbone genes, are predominantly conjugative, and frequently encode antimicrobial resistance (AMR) genes, conferring resistance to multiple antibiotic classes. Most VBR1 plasmids also carry phage defense and anti-defense systems, underscoring their ecological and evolutionary significance. AMR and defense/antidefense gene repertoires are highly variable across VBR1 plasmids, suggesting frequent gene acquisition, recombination events, and rapid replacement and diversification of resistance and defense determinants. The co-localization of AMR and phage defense systems on many VBR1 plasmids highlights their role in shaping virus-host interactions and microbial community dynamics. Our findings establish VBR1 as a widespread, clinically and ecologically relevant replicon family, providing a framework for the classification and surveillance of previously orphan plasmids, and advancing our understanding of AMR and phage resistance dynamics in marine ecosystems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"7 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145710796","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gavin M Douglas, Nicolas Tromas, Marinna Gaudin, Patrick Lypaczewski, Louis-Marie Bobay, B Jesse Shapiro, Samuel Chaffron
Understanding the drivers and consequences of horizontal gene transfer (HGT) is a key goal of microbial evolution research. Although co-occurring taxa have long been appreciated to undergo HGT more often, this association is confounded with other factors, most notably their phylogenetic relatedness. To disentangle these factors, we analyzed 15,339 marine prokaryotic genomes (mainly bacteria) and their distribution in the global ocean. We identified HGT events across these genomes and enrichments for functions previously shown to be prone to HGT. By mapping metagenomic reads from 1,862 ocean samples to these genomes, we also identified co-occurrence patterns and environmental associations. Although we observed an expected negative association between HGT rates and phylogenetic distance, we only detected an association between co-occurrence and phylogenetic distance for closely related taxa. This observation refines the previously reported trend to closely related taxa, rather than a consistent pattern across all taxonomic levels, at least here within marine environments. In addition, we identified a significant association between co-occurrence and HGT, which remains even after controlling for phylogenetic distance and measured environmental variables. In a subset of samples with extended environmental data, we identified higher HGT levels associated with particle-attached prokaryotes and associations of varying directions with specific environmental variables, such as chlorophyll a and photosynthetically available radiation. Overall, our findings demonstrate the significant influence of ecological associations in shaping marine prokaryotic evolution through HGT.
{"title":"Co-occurrence is associated with horizontal gene transfer across marine bacteria independent of phylogeny","authors":"Gavin M Douglas, Nicolas Tromas, Marinna Gaudin, Patrick Lypaczewski, Louis-Marie Bobay, B Jesse Shapiro, Samuel Chaffron","doi":"10.1093/ismejo/wraf275","DOIUrl":"https://doi.org/10.1093/ismejo/wraf275","url":null,"abstract":"Understanding the drivers and consequences of horizontal gene transfer (HGT) is a key goal of microbial evolution research. Although co-occurring taxa have long been appreciated to undergo HGT more often, this association is confounded with other factors, most notably their phylogenetic relatedness. To disentangle these factors, we analyzed 15,339 marine prokaryotic genomes (mainly bacteria) and their distribution in the global ocean. We identified HGT events across these genomes and enrichments for functions previously shown to be prone to HGT. By mapping metagenomic reads from 1,862 ocean samples to these genomes, we also identified co-occurrence patterns and environmental associations. Although we observed an expected negative association between HGT rates and phylogenetic distance, we only detected an association between co-occurrence and phylogenetic distance for closely related taxa. This observation refines the previously reported trend to closely related taxa, rather than a consistent pattern across all taxonomic levels, at least here within marine environments. In addition, we identified a significant association between co-occurrence and HGT, which remains even after controlling for phylogenetic distance and measured environmental variables. In a subset of samples with extended environmental data, we identified higher HGT levels associated with particle-attached prokaryotes and associations of varying directions with specific environmental variables, such as chlorophyll a and photosynthetically available radiation. Overall, our findings demonstrate the significant influence of ecological associations in shaping marine prokaryotic evolution through HGT.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"3 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145717319","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Caroline S Winther-Have,Jacob A Rasmussen,Xichuan Zhai,Dennis S Nielsen,Thomas Sicheritz-Pontén,Shyam Gopalakrishnan,Martha R J Clokie,Mathias Middelboe,Morten T Limborg
Understanding host-specific phage diversity is essential for deciphering the complex dynamics shaping microbial ecology and evolution. However, the lack of inherent host associations between uncultivated bacteria and their viruses remains a major limitation to understanding the drivers of viral diversity and its role in bacterial ecology, particularly given the intricate specificity of phage-host interactions. The naturally low complexity of the gut microbiota within piscivorous fish, such as Atlantic salmon (Salmo salar), makes it a valuable model for unravelling ecological patterns of viral diversity in the context of a limited bacterial species composition, and to explore the impact of an invading pathogen on the "steady-state" viral community. The intestinal microbiota of the salmon studied here, was in some cases dominated by a salmon-associated Mycoplasma or increasing levels of an opportunistic Aliivibrio, the latter observed in response to a disease outbreak. The two bacteria are distinctively different in their ecological strategies and their overall genomic and functional properties. A pronounced difference was observed in the gut viral communities and diversity, depending on whether it was dominated by a commensal or an invading bacterial species. Samples dominated by Mycoplasma sp. had few to no viruses, whereas samples dominated by Aliivibrio sp. had viral communities comprising up to 22 viral taxonomic operational units. This study provides unique insights into the significance of bacterial ecological trade-offs linked to niche adaptation and how these affect the associated viral communities in a natural host-controlled environment.
{"title":"Ecological strategies of bacteria shape inherent phage diversity in Atlantic salmon gut microbiomes.","authors":"Caroline S Winther-Have,Jacob A Rasmussen,Xichuan Zhai,Dennis S Nielsen,Thomas Sicheritz-Pontén,Shyam Gopalakrishnan,Martha R J Clokie,Mathias Middelboe,Morten T Limborg","doi":"10.1093/ismejo/wraf272","DOIUrl":"https://doi.org/10.1093/ismejo/wraf272","url":null,"abstract":"Understanding host-specific phage diversity is essential for deciphering the complex dynamics shaping microbial ecology and evolution. However, the lack of inherent host associations between uncultivated bacteria and their viruses remains a major limitation to understanding the drivers of viral diversity and its role in bacterial ecology, particularly given the intricate specificity of phage-host interactions. The naturally low complexity of the gut microbiota within piscivorous fish, such as Atlantic salmon (Salmo salar), makes it a valuable model for unravelling ecological patterns of viral diversity in the context of a limited bacterial species composition, and to explore the impact of an invading pathogen on the \"steady-state\" viral community. The intestinal microbiota of the salmon studied here, was in some cases dominated by a salmon-associated Mycoplasma or increasing levels of an opportunistic Aliivibrio, the latter observed in response to a disease outbreak. The two bacteria are distinctively different in their ecological strategies and their overall genomic and functional properties. A pronounced difference was observed in the gut viral communities and diversity, depending on whether it was dominated by a commensal or an invading bacterial species. Samples dominated by Mycoplasma sp. had few to no viruses, whereas samples dominated by Aliivibrio sp. had viral communities comprising up to 22 viral taxonomic operational units. This study provides unique insights into the significance of bacterial ecological trade-offs linked to niche adaptation and how these affect the associated viral communities in a natural host-controlled environment.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"4 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145696703","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Xinya Pan,Janne J Hageman,Daan A Weits,Lhais Caldas,Somayah S Elsayed,Lina M Bayona,Gilles P van Wezel,Roeland L Berendsen,Víctor J Carrión,Jos M Raaijmakers
Oxygen plays a crucial role in shaping microbial physiology, functions, and behavior. Endophytic bacteria, residing within plant tissues, inhabit microenvironments where oxygen availability can be limited. However, the magnitude of hypoxic conditions in the endosphere and how these affect functional microbial traits is largely unknown. Here, we showed with a microsensor that oxygen levels in roots of sugar beet seedlings drop drastically to variable, low oxygen levels when going from epidermal to endodermal root tissue into the vasculature. Subsequently, we investigated phenotypic and metabolic responses of endophytic Flavobacterium sp. 98 at oxygen levels of 100 ppm. Under these oxygen conditions, Flavobacterium sp. 98 showed reduced growth, enhanced motility, and an altered extracellular metabolite profile. Flavobacterium sp. 98 colonies spread out in response to oxygen limitation and more effectively restricted hyphal growth of the sugar beet root pathogen Rhizoctonia solani than Flavobacterium sp. 98 grown at ambient oxygen conditions. Exometabolome analysis revealed enhanced accumulation of lysophosphatidylethanolamine (lysoPE) and N-acetyl-phenylalanine under low-oxygen conditions, along with a reduced level of the antifungal compound 5,6-dimethylbenzimidazole. These responses reflect physiological and metabolic plasticity of Flavobacterium sp. 98, highlighting significant changes in the expression of specific traits under hypoxic conditions. Our findings provide insights into niche-adaptive strategies of endophytic bacteria and pinpoint functional traits in microbe-plant interactions operating inside plant tissue.
{"title":"Hypoxia Induces Phenotypic and Metabolic Shifts in Endophytic Flavobacterium sp. 98.","authors":"Xinya Pan,Janne J Hageman,Daan A Weits,Lhais Caldas,Somayah S Elsayed,Lina M Bayona,Gilles P van Wezel,Roeland L Berendsen,Víctor J Carrión,Jos M Raaijmakers","doi":"10.1093/ismejo/wraf269","DOIUrl":"https://doi.org/10.1093/ismejo/wraf269","url":null,"abstract":"Oxygen plays a crucial role in shaping microbial physiology, functions, and behavior. Endophytic bacteria, residing within plant tissues, inhabit microenvironments where oxygen availability can be limited. However, the magnitude of hypoxic conditions in the endosphere and how these affect functional microbial traits is largely unknown. Here, we showed with a microsensor that oxygen levels in roots of sugar beet seedlings drop drastically to variable, low oxygen levels when going from epidermal to endodermal root tissue into the vasculature. Subsequently, we investigated phenotypic and metabolic responses of endophytic Flavobacterium sp. 98 at oxygen levels of 100 ppm. Under these oxygen conditions, Flavobacterium sp. 98 showed reduced growth, enhanced motility, and an altered extracellular metabolite profile. Flavobacterium sp. 98 colonies spread out in response to oxygen limitation and more effectively restricted hyphal growth of the sugar beet root pathogen Rhizoctonia solani than Flavobacterium sp. 98 grown at ambient oxygen conditions. Exometabolome analysis revealed enhanced accumulation of lysophosphatidylethanolamine (lysoPE) and N-acetyl-phenylalanine under low-oxygen conditions, along with a reduced level of the antifungal compound 5,6-dimethylbenzimidazole. These responses reflect physiological and metabolic plasticity of Flavobacterium sp. 98, highlighting significant changes in the expression of specific traits under hypoxic conditions. Our findings provide insights into niche-adaptive strategies of endophytic bacteria and pinpoint functional traits in microbe-plant interactions operating inside plant tissue.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"5 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145689016","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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