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}
Heterotrophic nanoflagellates are the chief agents of bacterivory in the aquatic microbial loop but remain underrepresented in culture collections and in genomic databases. We isolated and characterised a representative of the previously uncultured freshwater Cryptomonad Group 1 (CRY1a) lineage using a genome-streamlined, ultrasmall and abundant microbe Planktophila versatilis as a prey and CARD-FISH probe-based screening. This isolate, Tyrannomonas regina, is one of the most dominant ubiquitous heterotrophic cryptomonads in freshwaters. It is a small heterotrophic nanoflagellate (ca. 3-5 μm) and has the smallest genome of any cryptomonad sequenced thus far. The compact genome (ca. 69 Mb) revealed no traces of a photosynthetic lifestyle, consistent with its phylogenomic placement as a sister-clade to cryptophytes that are characterised by the acquisition of a red-algal symbiont. Moreover, in comparison to its photosynthetic counterparts, its genome presents substantially lower repeat content and endogenous viral elements. Genomes of two giant viruses, Tyrannovirus reginensis GV1 and GV2, were also recovered from the same culture and represent a viral genus that has been described so far solely by metagenome-recovered genomes. Collectively, these findings provide insights into genomic ancestry and evolution, widespread ecological impact and interactions of an elusive protist lineage and illustrate the advantages of culture-centric approaches towards unfolding complex tapestries of life in the microbial world.
{"title":"Cultivation, genomics, and giant viruses of a ubiquitous and heterotrophic freshwater cryptomonad.","authors":"Indranil Mukherjee,Paul-Adrian Bulzu,Roudaina Boukheloua,Usman Asghar,Hongjae Park,Helena Henriques Vieira,Maria-Cecilia Chiriac,Vojtěch Kasalický,Petr Znachor,Pavel Rychtecký,Karel Šimek,Michaela M Salcher,Markus Haber,Rohit Ghai","doi":"10.1093/ismejo/wraf271","DOIUrl":"https://doi.org/10.1093/ismejo/wraf271","url":null,"abstract":"Heterotrophic nanoflagellates are the chief agents of bacterivory in the aquatic microbial loop but remain underrepresented in culture collections and in genomic databases. We isolated and characterised a representative of the previously uncultured freshwater Cryptomonad Group 1 (CRY1a) lineage using a genome-streamlined, ultrasmall and abundant microbe Planktophila versatilis as a prey and CARD-FISH probe-based screening. This isolate, Tyrannomonas regina, is one of the most dominant ubiquitous heterotrophic cryptomonads in freshwaters. It is a small heterotrophic nanoflagellate (ca. 3-5 μm) and has the smallest genome of any cryptomonad sequenced thus far. The compact genome (ca. 69 Mb) revealed no traces of a photosynthetic lifestyle, consistent with its phylogenomic placement as a sister-clade to cryptophytes that are characterised by the acquisition of a red-algal symbiont. Moreover, in comparison to its photosynthetic counterparts, its genome presents substantially lower repeat content and endogenous viral elements. Genomes of two giant viruses, Tyrannovirus reginensis GV1 and GV2, were also recovered from the same culture and represent a viral genus that has been described so far solely by metagenome-recovered genomes. Collectively, these findings provide insights into genomic ancestry and evolution, widespread ecological impact and interactions of an elusive protist lineage and illustrate the advantages of culture-centric approaches towards unfolding complex tapestries of life in the microbial world.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145689015","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}
Tingting Xiang,Stephanie L Peak,Eric C Huitt,Arthur R Grossman
Dinoflagellate algae in the family Symbiodiniaceae, symbionts of many marine cnidarians are critical for the metabolic integrity of reef ecosystems, which are increasingly threatened by environmental stress. The resilience of the cnidarian-dinoflagellate symbiosis depends on thermotolerance of the partner organisms; coral hosts that harbor heat-resistant symbionts exhibit greater resistance to bleaching. Although coral responses to heat stress are well-documented, transcriptomic adaptation/acclimation of Symbiodiniaceae to elevated temperatures are limited. Here, we compare thermal responses of two species representing two genera of Symbiodiniaceae, Symbiodinium linucheae (strain SSA01; ITS2 type A4) and Breviolum minutum (strain SSB01; ITS2 type B1). SSA01 in culture maintained photosynthetic function at elevated temperatures and mounted a rapid transcriptomic response characterized by early downregulation of a JMJ21-like histone demethylase coupled with prompt upregulation of transcripts associated with DNA repair and oxidative stress, which would likely contribute to enhanced resilience to heat stress. In contrast, SSB01 experienced a decline in photosynthetic efficiency and a delayed transcriptomic response that included upregulation of transcripts encoding proteasome subunits and reduced transcripts encoding proteins involved in photosynthesis and metabolite transport. These findings indicate that a rapid and moderate transcriptomic response that results in increased expression of genes related to the synthesis and repair of biomolecules might be crucial for thermal tolerance in the Symbiodiniaceae whereas sensitivity to elevated temperatures may be reflected by increased protein turnover and a marked decline in anabolic processes. Understanding these differences is vital for predicting coral responses to warming seas and developing strategies to mitigate heat-stress impacts on reefs.
{"title":"Distinct transcriptomic strategies underlie differential heat tolerance in Symbiodiniaceae symbionts.","authors":"Tingting Xiang,Stephanie L Peak,Eric C Huitt,Arthur R Grossman","doi":"10.1093/ismejo/wraf268","DOIUrl":"https://doi.org/10.1093/ismejo/wraf268","url":null,"abstract":"Dinoflagellate algae in the family Symbiodiniaceae, symbionts of many marine cnidarians are critical for the metabolic integrity of reef ecosystems, which are increasingly threatened by environmental stress. The resilience of the cnidarian-dinoflagellate symbiosis depends on thermotolerance of the partner organisms; coral hosts that harbor heat-resistant symbionts exhibit greater resistance to bleaching. Although coral responses to heat stress are well-documented, transcriptomic adaptation/acclimation of Symbiodiniaceae to elevated temperatures are limited. Here, we compare thermal responses of two species representing two genera of Symbiodiniaceae, Symbiodinium linucheae (strain SSA01; ITS2 type A4) and Breviolum minutum (strain SSB01; ITS2 type B1). SSA01 in culture maintained photosynthetic function at elevated temperatures and mounted a rapid transcriptomic response characterized by early downregulation of a JMJ21-like histone demethylase coupled with prompt upregulation of transcripts associated with DNA repair and oxidative stress, which would likely contribute to enhanced resilience to heat stress. In contrast, SSB01 experienced a decline in photosynthetic efficiency and a delayed transcriptomic response that included upregulation of transcripts encoding proteasome subunits and reduced transcripts encoding proteins involved in photosynthesis and metabolite transport. These findings indicate that a rapid and moderate transcriptomic response that results in increased expression of genes related to the synthesis and repair of biomolecules might be crucial for thermal tolerance in the Symbiodiniaceae whereas sensitivity to elevated temperatures may be reflected by increased protein turnover and a marked decline in anabolic processes. Understanding these differences is vital for predicting coral responses to warming seas and developing strategies to mitigate heat-stress impacts on reefs.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"198200 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145663929","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}
Ori Furman,Gil Sorek,Sarah Moraïs,Liron Levin,Omar Eduardo Tovar-Herrera,Sarah Winkler,Itzhak Mizrahi
The early life assembly of the rumen microbiome is a critical process with lasting implications for host development and function. Using high-resolution longitudinal metagenomics in calves tracked from birth to three years (∼800 days) of age, we reconstructed 2873 high-quality metagenome-assembled genomes (MAGs), including 517 novel genomes primarily detected in early life. These novel genomes, spanning 274 genera and largely classified as non-core taxa, reveal a diverse and functionally distinct auxiliary microbiome. Unlike in other ecosystems, this early microbial community persists into adulthood, retaining ecological and functional relevance despite a decline in abundance. Temporal clustering revealed strong associations between auxiliary taxa and dietary transitions, with functional enrichments in environmental sensing, nutrient biosynthesis, and volatile fatty acid metabolism. Metabolic network analyses showed that auxiliary genomes complement non-auxiliary community members in key functions, with potential effects on the host. Our findings suggest that early colonizers act as ecosystem engineers, with the potential to shape the developmental trajectory of the rumen microbiome. This study thus positions the early microbiome not as a transient feature of colonization, but as a structured, functionally coherent auxiliary community that interacts with the mature rumen ecosystem.
{"title":"Persistent auxiliary microbiome of early novel colonizers in the developing rumen with lasting functional significance.","authors":"Ori Furman,Gil Sorek,Sarah Moraïs,Liron Levin,Omar Eduardo Tovar-Herrera,Sarah Winkler,Itzhak Mizrahi","doi":"10.1093/ismejo/wraf252","DOIUrl":"https://doi.org/10.1093/ismejo/wraf252","url":null,"abstract":"The early life assembly of the rumen microbiome is a critical process with lasting implications for host development and function. Using high-resolution longitudinal metagenomics in calves tracked from birth to three years (∼800 days) of age, we reconstructed 2873 high-quality metagenome-assembled genomes (MAGs), including 517 novel genomes primarily detected in early life. These novel genomes, spanning 274 genera and largely classified as non-core taxa, reveal a diverse and functionally distinct auxiliary microbiome. Unlike in other ecosystems, this early microbial community persists into adulthood, retaining ecological and functional relevance despite a decline in abundance. Temporal clustering revealed strong associations between auxiliary taxa and dietary transitions, with functional enrichments in environmental sensing, nutrient biosynthesis, and volatile fatty acid metabolism. Metabolic network analyses showed that auxiliary genomes complement non-auxiliary community members in key functions, with potential effects on the host. Our findings suggest that early colonizers act as ecosystem engineers, with the potential to shape the developmental trajectory of the rumen microbiome. This study thus positions the early microbiome not as a transient feature of colonization, but as a structured, functionally coherent auxiliary community that interacts with the mature rumen ecosystem.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"125 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145644918","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}
Secretory Immunoglobulin A (SIgA) is the dominant mucosal antibody and a key regulator of the gut microbiota. In early life, infants rely on breastmilk as their primary source of SIgA, but the role of milk-derived SIgA in early life microbiota colonization dynamics remains incompletely understood. Here, we show that species-specific SIgA in milk is antigen-inducible and discriminates between closely related but immunologically diverging microbes in the neonatal gut. More specifically, milk species-specific SIgA promotes colonization by an anti-inflammatory Escherichia coli strain while restricting the expansion of pro-inflammatory Proteus mirabilis. These findings uncover a dual role of maternal milk SIgA in actively sculpting the early life gut microbiota with species-level precision.
{"title":"Milk IgA promotes symbionts and limits pathobionts in the early life gut.","authors":"Katherine Donald,Antonio Serapio-Palacios,Tahereh Bozorgmehr,Mahebali Tabusi,B Brett Finlay","doi":"10.1093/ismejo/wraf266","DOIUrl":"https://doi.org/10.1093/ismejo/wraf266","url":null,"abstract":"Secretory Immunoglobulin A (SIgA) is the dominant mucosal antibody and a key regulator of the gut microbiota. In early life, infants rely on breastmilk as their primary source of SIgA, but the role of milk-derived SIgA in early life microbiota colonization dynamics remains incompletely understood. Here, we show that species-specific SIgA in milk is antigen-inducible and discriminates between closely related but immunologically diverging microbes in the neonatal gut. More specifically, milk species-specific SIgA promotes colonization by an anti-inflammatory Escherichia coli strain while restricting the expansion of pro-inflammatory Proteus mirabilis. These findings uncover a dual role of maternal milk SIgA in actively sculpting the early life gut microbiota with species-level precision.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"16 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145644927","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}
Plant-associated microbial communities play a vital role in host adaptation to environmental stress, yet their contributions to plant nickel (Ni) tolerance strategies remain unclear. It is not understood whether the same microbial community elicits similar responses across different plant species or regulates stress adaptation in a host-specific manner. Although microorganisms influence plant responses to metal toxicity by altering metal bioavailability in the rhizosphere, their potential to optimize plant metal uptake is less explored. In this study, we evaluated whether synthetic microbial communities enhance (Ni) uptake in two species with contrasting metal strategies: the hyperaccumulator Odontarrhena chalcidica and the Ni-excluding Arabidopsis arenosa. We hypothesized that soil microorganisms support plant metal adaptation by improving physiological function rather than altering soil metal availability. Our results show that O. chalcidica reached its full hyperaccumulating potential only when co-cultivated with a soil-derived microbial community, regardless of the microorganisms' ability to mobilize Ni or promote plant growth. Microorganisms that enhanced Ni uptake had no effect on soil Ni availability. Microbial community analysis revealed species-specific microbiota assembly, with O. chalcidica being more responsive yet more selective. Serpentine-soil microbiota enhanced Ni uptake in O. chalcidica by upregulating iron-transporter genes, confirming reliance on Fe-transport pathways for Ni acquisition. In contrast, the same inoculum induced Zn-transporters and NRT2.1/NRT2.2 in A. arenosa, reflecting strategy of cation partitioning and nutrient-transport fine-tuning under Ni stress. These findings refine criteria for selecting microorganisms in phytoremediation and highlight that the functional impact of plant-associated microorganisms on metal handling outweigh their effects on metal solubility in soil.
{"title":"Regulation of plant Ni uptake by soil-borne microorganisms occurs independently of their Ni-solubilizing capabilities.","authors":"Agnieszka Domka,Maciej Gustab,Roman J Jędrzejczyk,Rafał Ważny,Alice Tognacchini,Markus Puschenreiter,Paweł Łabaj,Agata Muszyńska,Weronika Kosowicz,Kinga Jarosz,Piotr Rozpądek","doi":"10.1093/ismejo/wraf265","DOIUrl":"https://doi.org/10.1093/ismejo/wraf265","url":null,"abstract":"Plant-associated microbial communities play a vital role in host adaptation to environmental stress, yet their contributions to plant nickel (Ni) tolerance strategies remain unclear. It is not understood whether the same microbial community elicits similar responses across different plant species or regulates stress adaptation in a host-specific manner. Although microorganisms influence plant responses to metal toxicity by altering metal bioavailability in the rhizosphere, their potential to optimize plant metal uptake is less explored. In this study, we evaluated whether synthetic microbial communities enhance (Ni) uptake in two species with contrasting metal strategies: the hyperaccumulator Odontarrhena chalcidica and the Ni-excluding Arabidopsis arenosa. We hypothesized that soil microorganisms support plant metal adaptation by improving physiological function rather than altering soil metal availability. Our results show that O. chalcidica reached its full hyperaccumulating potential only when co-cultivated with a soil-derived microbial community, regardless of the microorganisms' ability to mobilize Ni or promote plant growth. Microorganisms that enhanced Ni uptake had no effect on soil Ni availability. Microbial community analysis revealed species-specific microbiota assembly, with O. chalcidica being more responsive yet more selective. Serpentine-soil microbiota enhanced Ni uptake in O. chalcidica by upregulating iron-transporter genes, confirming reliance on Fe-transport pathways for Ni acquisition. In contrast, the same inoculum induced Zn-transporters and NRT2.1/NRT2.2 in A. arenosa, reflecting strategy of cation partitioning and nutrient-transport fine-tuning under Ni stress. These findings refine criteria for selecting microorganisms in phytoremediation and highlight that the functional impact of plant-associated microorganisms on metal handling outweigh their effects on metal solubility in soil.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"150 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145644921","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}
Haidong Gu,Zhuxiu Liu,Song Liu,Xiaojing Hu,Zhenhua Yu,Yansheng Li,Lujun Li,Yueyu Sui,Jian Jin,Xiaobing Liu,Zhongjun Jia,Lei Sun,Jonathan M Adams,Marcel G A van der Heijden,Junjie Liu,Guanghua Wang
It is widely considered that conversion of natural landscapes to agriculture results in biotic homogenization. A recent study comparing soil biota of 27 paired natural steppe soil (NS) and agricultural soil (AS) sites across 900km in north-eastern China found that conversion to agriculture had increased spatial gradients in soil functional genes. Using the same shotgun metagenome samples, and bacterial amplicon data, we instead analyzed total observed variation at the between-site and within-site level. We found that from the perspective of community taxonomic composition, archaeal and fungal community variation was decreased in AS compared to NS at both within- and between-site scales. In contrast, the bacterial and metazoal community was homogenized only at the local scale. Total functional KEGG gene assemblage was homogenized in AS at both the local and regional scale, whereas "Y-A-S" strategies in bacteria were homogenized at the local scale but not the between-site scale. Overall, these results show a clear homogenizing effect of agriculture with respect to multiple aspects of soil taxonomic and functional diversity, though varying by scale. Certain abiotic soil properties showed homogenization in AS at within-site and between-site scales may explain this homogenization, and uniformity of plant cover in croplands likely contribute to the effect. These findings confirm and extend global-scale studies showing homogenization of soil biota in agricultural environments, revealing that effects extend to functional genes and the broad taxonomic spectrum of life - with potential loss of soil ecosystem resilience to environmental change resulting from agriculture.
{"title":"Land conversion to cropland homogenizes variation in soil biota, gene assemblages and ecological strategies on local and regional scales.","authors":"Haidong Gu,Zhuxiu Liu,Song Liu,Xiaojing Hu,Zhenhua Yu,Yansheng Li,Lujun Li,Yueyu Sui,Jian Jin,Xiaobing Liu,Zhongjun Jia,Lei Sun,Jonathan M Adams,Marcel G A van der Heijden,Junjie Liu,Guanghua Wang","doi":"10.1093/ismejo/wraf264","DOIUrl":"https://doi.org/10.1093/ismejo/wraf264","url":null,"abstract":"It is widely considered that conversion of natural landscapes to agriculture results in biotic homogenization. A recent study comparing soil biota of 27 paired natural steppe soil (NS) and agricultural soil (AS) sites across 900km in north-eastern China found that conversion to agriculture had increased spatial gradients in soil functional genes. Using the same shotgun metagenome samples, and bacterial amplicon data, we instead analyzed total observed variation at the between-site and within-site level. We found that from the perspective of community taxonomic composition, archaeal and fungal community variation was decreased in AS compared to NS at both within- and between-site scales. In contrast, the bacterial and metazoal community was homogenized only at the local scale. Total functional KEGG gene assemblage was homogenized in AS at both the local and regional scale, whereas \"Y-A-S\" strategies in bacteria were homogenized at the local scale but not the between-site scale. Overall, these results show a clear homogenizing effect of agriculture with respect to multiple aspects of soil taxonomic and functional diversity, though varying by scale. Certain abiotic soil properties showed homogenization in AS at within-site and between-site scales may explain this homogenization, and uniformity of plant cover in croplands likely contribute to the effect. These findings confirm and extend global-scale studies showing homogenization of soil biota in agricultural environments, revealing that effects extend to functional genes and the broad taxonomic spectrum of life - with potential loss of soil ecosystem resilience to environmental change resulting from agriculture.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"2 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145644919","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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