Deciphering the genomic basis of ecological diversification in activated sludge microbiomes is essential for optimizing treatment technology and advancing microbial ecology. Here, we present a global genome-resolved investigation of Candidatus Accumulibacter, the primary functional agent of enhanced biological phosphorus removal, based on 828 metagenomes from wastewater treatment plants across six continents. We recovered 104 high-quality Candidatus Accumulibacter metagenome-assembled genomes, discovering a new clade (Clade IV), substantially expanding the known phylogenetic diversity and revealing a ubiquitous yet geographically heterogeneous global distribution. Phylogenomic and pangenome analyses uncovered extensive clade-specific gene gain and loss, particularly in nitrogen metabolism, suggesting divergent evolutionary trajectories shaped by relaxed selection and niche adaptation. Genome-wide patterns of convergent streamlining and enriched antiviral defense systems indicate selective pressures from strong competition and viral predation. Constraint-based metabolic modeling revealed pervasive amino acid autotrophies and metabolic complementarity, coupled with distinct carbon utilization strategies that support ecological specialization across operational settings. Experimental validation reconciled model-phenotype discrepancies, highlighting the importance of transporter promiscuity and gene regulation in carbon substrate assimilation. Collectively, our findings redefine Candidatus Accumulibacter as a dynamic model of microbial genome plasticity, metabolic adaptation, and ecological resilience, providing an insight for understanding how microbial communities adapt and respond under engineered environmental conditions.
{"title":"Metagenomic characterization of the metabolism, evolution, and global distribution of Candidatus Accumulibacter members in wastewater treatment plants","authors":"Xiaojing Xie, Liping Chen, Jing Yuan, Haixin Zheng, Lanying Zhang, Xiaokai Yu, Xianghui Liu, Chaohai Wei, Guanglei Qiu","doi":"10.1093/ismejo/wraf278","DOIUrl":"https://doi.org/10.1093/ismejo/wraf278","url":null,"abstract":"Deciphering the genomic basis of ecological diversification in activated sludge microbiomes is essential for optimizing treatment technology and advancing microbial ecology. Here, we present a global genome-resolved investigation of Candidatus Accumulibacter, the primary functional agent of enhanced biological phosphorus removal, based on 828 metagenomes from wastewater treatment plants across six continents. We recovered 104 high-quality Candidatus Accumulibacter metagenome-assembled genomes, discovering a new clade (Clade IV), substantially expanding the known phylogenetic diversity and revealing a ubiquitous yet geographically heterogeneous global distribution. Phylogenomic and pangenome analyses uncovered extensive clade-specific gene gain and loss, particularly in nitrogen metabolism, suggesting divergent evolutionary trajectories shaped by relaxed selection and niche adaptation. Genome-wide patterns of convergent streamlining and enriched antiviral defense systems indicate selective pressures from strong competition and viral predation. Constraint-based metabolic modeling revealed pervasive amino acid autotrophies and metabolic complementarity, coupled with distinct carbon utilization strategies that support ecological specialization across operational settings. Experimental validation reconciled model-phenotype discrepancies, highlighting the importance of transporter promiscuity and gene regulation in carbon substrate assimilation. Collectively, our findings redefine Candidatus Accumulibacter as a dynamic model of microbial genome plasticity, metabolic adaptation, and ecological resilience, providing an insight for understanding how microbial communities adapt and respond under engineered environmental conditions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"22 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145807743","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}
Urea is an important alternative nitrogen source to ammonium for nitrification in oligotrophic oceans, yet its role in substrate-driven nitrous oxide (N2O) production remains poorly constrained. Here, we combined N2O isotopomer profiling, 15N-tracer incubations, and metagenomics to quantify and mechanistically resolve substrate-specific archaeal nitrification in the western tropical Pacific euphotic zone. Isotopomer-based mixing and fractionation model indicated that archaeal nitrification accounted for 69.6 ± 14.1% of microbial sources of N2O in oxygenated epipelagic waters. Depth-integrated urea-driven nitrification contributed 14–41% of total nitrification and 21–39% of nitrification-derived N2O, with contributions regulated by substrate proportions. Acidification experiments showed that pH decline inhibited ammonium-driven nitrification (median 21.9%) and enhanced urea oxidation (median 61.9%), whereas N2O production increased for both substrates (median 35.9% and 38.0%). In addition, experimental acidification induced opposite shifts in hybrid versus double-labelled N2O, suggesting pH-driven shifts N-intermediate chemistry and intracellular partitioning. Metagenomic results support the globally widespread urea-type AOA. Together, these results indicate that urea-driven nitrification constitutes a non-negligible, substrate-dependent source of N2O in oligotrophic euphotic zones. We recommend that Earth-system N-cycle models represent urea and ammonium oxidation as distinct pathways with pH-sensitive yields to improve projections of marine nitrification and N2O fluxes under acidification.
{"title":"Urea-driven nitrification contributes to N2O production in the oligotrophic euphotic ocean","authors":"Ting Gu, Zhuo Chen, David A Hutchins, Jun Sun","doi":"10.1093/ismejo/wraf281","DOIUrl":"https://doi.org/10.1093/ismejo/wraf281","url":null,"abstract":"Urea is an important alternative nitrogen source to ammonium for nitrification in oligotrophic oceans, yet its role in substrate-driven nitrous oxide (N2O) production remains poorly constrained. Here, we combined N2O isotopomer profiling, 15N-tracer incubations, and metagenomics to quantify and mechanistically resolve substrate-specific archaeal nitrification in the western tropical Pacific euphotic zone. Isotopomer-based mixing and fractionation model indicated that archaeal nitrification accounted for 69.6 ± 14.1% of microbial sources of N2O in oxygenated epipelagic waters. Depth-integrated urea-driven nitrification contributed 14–41% of total nitrification and 21–39% of nitrification-derived N2O, with contributions regulated by substrate proportions. Acidification experiments showed that pH decline inhibited ammonium-driven nitrification (median 21.9%) and enhanced urea oxidation (median 61.9%), whereas N2O production increased for both substrates (median 35.9% and 38.0%). In addition, experimental acidification induced opposite shifts in hybrid versus double-labelled N2O, suggesting pH-driven shifts N-intermediate chemistry and intracellular partitioning. Metagenomic results support the globally widespread urea-type AOA. Together, these results indicate that urea-driven nitrification constitutes a non-negligible, substrate-dependent source of N2O in oligotrophic euphotic zones. We recommend that Earth-system N-cycle models represent urea and ammonium oxidation as distinct pathways with pH-sensitive yields to improve projections of marine nitrification and N2O fluxes under acidification.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"4 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145801268","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}
William Monteith,Made A Krisna,Biel Garcias Puigserver,Elizabeth A Cummins,David J Kelly,Aidan J Taylor,Samuel K Sheppard
Pathogens that are harmless in one environment can cause serious disease in another. Among host-associated bacteria, transition between hosts can have serious consequences for animal and human health. However, much remains unknown about how adaptation shapes bacterial distribution in the wild. Here, investigating the ecological genomics of Escherichia coli from diverse hosts and environments, we address the idea that bacteria disperse freely, and challenge the "everything is everywhere" paradigm. Using comparative genomics and parallelised high throughout pangenome-wide association studies (900 experiments) we investigate lineage distribution and identify adaptive genomic signatures associated with host species, physiology and ecology. Our findings provide insights into bacterial niche adaptation, emphasize the impact of agriculture on microbial evolution, and inform One Health frameworks by linking genomics, host ecology, and the emergence of antimicrobial resistance.
{"title":"Everything is everywhere but Escherichia coli adapts to different niches.","authors":"William Monteith,Made A Krisna,Biel Garcias Puigserver,Elizabeth A Cummins,David J Kelly,Aidan J Taylor,Samuel K Sheppard","doi":"10.1093/ismejo/wraf267","DOIUrl":"https://doi.org/10.1093/ismejo/wraf267","url":null,"abstract":"Pathogens that are harmless in one environment can cause serious disease in another. Among host-associated bacteria, transition between hosts can have serious consequences for animal and human health. However, much remains unknown about how adaptation shapes bacterial distribution in the wild. Here, investigating the ecological genomics of Escherichia coli from diverse hosts and environments, we address the idea that bacteria disperse freely, and challenge the \"everything is everywhere\" paradigm. Using comparative genomics and parallelised high throughout pangenome-wide association studies (900 experiments) we investigate lineage distribution and identify adaptive genomic signatures associated with host species, physiology and ecology. Our findings provide insights into bacterial niche adaptation, emphasize the impact of agriculture on microbial evolution, and inform One Health frameworks by linking genomics, host ecology, and the emergence of antimicrobial resistance.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"111 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145771496","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}
Fergus Wright, Stéphanie Grand, Ian Sanders, Ricardo Arraiano-Castilho
Interactions between arbuscular mycorrhizal fungi (AMF) and soil microbial communities that support plant nutrient acquisition remain poorly understood. Here, we investigate how the model AMF species Rhizophagus irregularis influences microbial mRNA transcription and microbial taxonomic composition in rhizosphere and bulk soil compartments of Zea mays mesocosms. Using metatranscriptomic profiling alongside 16S rRNA and ITS amplicon sequencing, we show that AMF alter bacterial gene expression without shifting community composition and significantly increase fungal richness and evenness. We identify genotype-specific effects of AMF on microbial diversity and function and find that AMF colonisation stimulates microbial B-vitamin biosynthesis. We also link elevated plant leaf phosphorus levels under AMF colonisation with changes in root gene expression and increased abundance of AMF-stimulated rhizosphere bacterial taxa. These findings highlight the importance of feedback loops between plant, AMF and soil microorganisms and show how these interactions can contribute to increases in plant nutrient uptake. It is hoped these results will be useful for sustainable crop production and ecosystem regeneration through microbiome-informed management strategies.
{"title":"Mycorrhizal control of microbial gene transcription and taxonomic composition in the rhizosphere and bulk soil","authors":"Fergus Wright, Stéphanie Grand, Ian Sanders, Ricardo Arraiano-Castilho","doi":"10.1093/ismejo/wraf282","DOIUrl":"https://doi.org/10.1093/ismejo/wraf282","url":null,"abstract":"Interactions between arbuscular mycorrhizal fungi (AMF) and soil microbial communities that support plant nutrient acquisition remain poorly understood. Here, we investigate how the model AMF species Rhizophagus irregularis influences microbial mRNA transcription and microbial taxonomic composition in rhizosphere and bulk soil compartments of Zea mays mesocosms. Using metatranscriptomic profiling alongside 16S rRNA and ITS amplicon sequencing, we show that AMF alter bacterial gene expression without shifting community composition and significantly increase fungal richness and evenness. We identify genotype-specific effects of AMF on microbial diversity and function and find that AMF colonisation stimulates microbial B-vitamin biosynthesis. We also link elevated plant leaf phosphorus levels under AMF colonisation with changes in root gene expression and increased abundance of AMF-stimulated rhizosphere bacterial taxa. These findings highlight the importance of feedback loops between plant, AMF and soil microorganisms and show how these interactions can contribute to increases in plant nutrient uptake. It is hoped these results will be useful for sustainable crop production and ecosystem regeneration through microbiome-informed management strategies.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"10 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145777828","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}
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}
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