Nitrogen and iron are essential yet often limiting nutrients in many ecosystems. Microbial nitrogen fixation by diazotrophs and dissimilatory ferric iron reduction are key processes that sustain nitrogen and iron availability. However, their interactions are not well understood. Here, we demonstrate a synergistic relationship between microbial nitrogen fixation and ferric iron reduction, observed in both laboratory cultures and environmental samples. In diazotrophic ferric iron-reducing bacteria, including Klebsiella grimontii N7 and Geobacter sulfurreducens PCA, nitrogen fixation enhanced heterotrophic ferric iron-reducing rates by 14.7- and 2.69-fold, respectively, and ferric iron reduction concurrently increased 15N2 fixation by up to 100%. A similar synergy was observed in an interspecies system comprising the diazotroph Azospirillum humicireducens SgZ-5 T and the dissimilatory ferric iron-reducing bacterium Shewanella oneidensis MR-1. Transcriptomic analysis revealed that nitrogen fixation upregulated pathways involved in carbon and nitrogen metabolism, including amino acid biosynthesis, glycolysis, and the tricarboxylic acid cycle (P < 0.01), thereby accelerating ferric iron reduction through nitrogen supply. In turn, ferric iron reduction stimulated organic carbon oxidation, generating the energy and reducing equivalents needed for microbial nitrogen fixation. These findings were further validated through microcosm experiments and meta-omics analyses of environmental samples from aquifers, marine sediments, hot springs, and soils, providing new insights into the coupled nitrogen, iron, and carbon cycles in natural ecosystems.
{"title":"Synergistic interaction between microbial nitrogen fixation and iron reduction in the environment.","authors":"Xiaohan Liu,Ping Li,Keman Bao,Yaqi Wang,Helin Wang,Yanhong Wang,Zhou Jiang,Yi Yang,Songhu Yuan,Andreas Kappler,Yanxin Wang","doi":"10.1093/ismejo/wraf212","DOIUrl":"https://doi.org/10.1093/ismejo/wraf212","url":null,"abstract":"Nitrogen and iron are essential yet often limiting nutrients in many ecosystems. Microbial nitrogen fixation by diazotrophs and dissimilatory ferric iron reduction are key processes that sustain nitrogen and iron availability. However, their interactions are not well understood. Here, we demonstrate a synergistic relationship between microbial nitrogen fixation and ferric iron reduction, observed in both laboratory cultures and environmental samples. In diazotrophic ferric iron-reducing bacteria, including Klebsiella grimontii N7 and Geobacter sulfurreducens PCA, nitrogen fixation enhanced heterotrophic ferric iron-reducing rates by 14.7- and 2.69-fold, respectively, and ferric iron reduction concurrently increased 15N2 fixation by up to 100%. A similar synergy was observed in an interspecies system comprising the diazotroph Azospirillum humicireducens SgZ-5 T and the dissimilatory ferric iron-reducing bacterium Shewanella oneidensis MR-1. Transcriptomic analysis revealed that nitrogen fixation upregulated pathways involved in carbon and nitrogen metabolism, including amino acid biosynthesis, glycolysis, and the tricarboxylic acid cycle (P < 0.01), thereby accelerating ferric iron reduction through nitrogen supply. In turn, ferric iron reduction stimulated organic carbon oxidation, generating the energy and reducing equivalents needed for microbial nitrogen fixation. These findings were further validated through microcosm experiments and meta-omics analyses of environmental samples from aquifers, marine sediments, hot springs, and soils, providing new insights into the coupled nitrogen, iron, and carbon cycles in natural ecosystems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"39 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145103567","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}
Marie Riisgaard-Jensen,Rodrigo Maia Valença,Miriam Peces,Per Halkjær Nielsen
The link between the sewer microbiome and microbial communities in activated sludge wastewater treatment plants is currently poorly understood despite the systems being directly interconnected. Microbial immigration from wastewater has been identified as a key factor determining activated sludge community assembly. Here, we present the first comprehensive study of the sewer microbiome and hypothesize that it harbors a process-critical activated sludge microbes, thus critical for activated sludge community assembly and performance. We integrated species-level microbial analyses of biofilm, sediment, and sewer wastewater in domestic gravity and pressure sewers in Aalborg, Denmark, with samples from influent wastewater and activated sludge from two downstream wastewater treatment plants. By tracing the sources of incoming bacteria and determining their growth fate in the activated sludge, we confirmed the hypothesis that most activated sludge process-critical bacteria were part of the sewer microbiome. Within the sewer system, a gradient was observed, from dominance of gut-bacteria in the wastewater upstream to prevalence of biofilm and sediment bacteria downstream at the wastewater treatment plants inlet, with the relative ratio strongly affected by rain events. A holistic understanding of the sewer system and activated sludge is essential, as the sewers hold massive amounts of active biomass serving as a major microbial source for community composition and dynamics in wastewater treatment plants. Sewer systems should be recognized as a crucial environmental filtration step, and the sewer microbiome as an important source community for activated sludge, helping to explain the observed regional and global differences in activated sludge community structure.
{"title":"Sewer microbiomes shape microbial community composition and dynamics of wastewater treatment plants.","authors":"Marie Riisgaard-Jensen,Rodrigo Maia Valença,Miriam Peces,Per Halkjær Nielsen","doi":"10.1093/ismejo/wraf213","DOIUrl":"https://doi.org/10.1093/ismejo/wraf213","url":null,"abstract":"The link between the sewer microbiome and microbial communities in activated sludge wastewater treatment plants is currently poorly understood despite the systems being directly interconnected. Microbial immigration from wastewater has been identified as a key factor determining activated sludge community assembly. Here, we present the first comprehensive study of the sewer microbiome and hypothesize that it harbors a process-critical activated sludge microbes, thus critical for activated sludge community assembly and performance. We integrated species-level microbial analyses of biofilm, sediment, and sewer wastewater in domestic gravity and pressure sewers in Aalborg, Denmark, with samples from influent wastewater and activated sludge from two downstream wastewater treatment plants. By tracing the sources of incoming bacteria and determining their growth fate in the activated sludge, we confirmed the hypothesis that most activated sludge process-critical bacteria were part of the sewer microbiome. Within the sewer system, a gradient was observed, from dominance of gut-bacteria in the wastewater upstream to prevalence of biofilm and sediment bacteria downstream at the wastewater treatment plants inlet, with the relative ratio strongly affected by rain events. A holistic understanding of the sewer system and activated sludge is essential, as the sewers hold massive amounts of active biomass serving as a major microbial source for community composition and dynamics in wastewater treatment plants. Sewer systems should be recognized as a crucial environmental filtration step, and the sewer microbiome as an important source community for activated sludge, helping to explain the observed regional and global differences in activated sludge community structure.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145103568","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}
Zimeng Zhang, Xing Liu, Zhiling Li, Xueqi Chen, Yunxia Zu, Shih-Hsin Ho, Bin Liang, Shungui Zhou, Aijie Wang
Energy acquisition presents a fundamental constraint for microbial survival in oligotrophic environments. Although heterotrophic organohalide-respiring bacteria (OHRB) are known to perform reductive dehalogenation in organohalide-contaminated oligotrophic ecosystems, their energy metabolism remains poorly understood. Here, we report that Pseudomonas sp. CP-1, an OHRB, can directly oxidize humin from diverse oligotrophic aquifers to drive organohalide respiration. Spectroscopy, electrochemistry and metabolic profiling demonstrated that electrons stored in phenolic hydroxyl and amino groups of humin were utilized by strain CP-1 for organohalide respiration. Mutational and chemical inhibition studies identified an extracellular electron uptake pathway involving a multiheme cytochrome EeuP, which transfers extracellular electrons into the organohalide-respiratory chain, thereby coupling humin oxidation with reductive dehalogenation. Phylogenetic analyses revealed the widespread distribution of EeuP homologs across environmental bacterial taxa, implying a broader ecological relevance. This discovery sheds light on the hidden world of subsurface microbiology, with implications for understanding microbial energy metabolism in the energy-scarce environments.
{"title":"Humin oxidation drives microbial dehalogenation in oligotrophic environments","authors":"Zimeng Zhang, Xing Liu, Zhiling Li, Xueqi Chen, Yunxia Zu, Shih-Hsin Ho, Bin Liang, Shungui Zhou, Aijie Wang","doi":"10.1093/ismejo/wraf207","DOIUrl":"https://doi.org/10.1093/ismejo/wraf207","url":null,"abstract":"Energy acquisition presents a fundamental constraint for microbial survival in oligotrophic environments. Although heterotrophic organohalide-respiring bacteria (OHRB) are known to perform reductive dehalogenation in organohalide-contaminated oligotrophic ecosystems, their energy metabolism remains poorly understood. Here, we report that Pseudomonas sp. CP-1, an OHRB, can directly oxidize humin from diverse oligotrophic aquifers to drive organohalide respiration. Spectroscopy, electrochemistry and metabolic profiling demonstrated that electrons stored in phenolic hydroxyl and amino groups of humin were utilized by strain CP-1 for organohalide respiration. Mutational and chemical inhibition studies identified an extracellular electron uptake pathway involving a multiheme cytochrome EeuP, which transfers extracellular electrons into the organohalide-respiratory chain, thereby coupling humin oxidation with reductive dehalogenation. Phylogenetic analyses revealed the widespread distribution of EeuP homologs across environmental bacterial taxa, implying a broader ecological relevance. This discovery sheds light on the hidden world of subsurface microbiology, with implications for understanding microbial energy metabolism in the energy-scarce environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"90 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145089629","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}
Thomas C A Hitch, Johanna Bosch, Silvia Bolsega, Charlotte Deschamps, Lucie Etienne-Mesmin, Nicole Treichel, Stephanie Blanquet-Diot, Soeren Ocvirk, Marijana Basic, Thomas Clavel
Understanding the complex interactions between microbes and their environment requires robust model systems such as synthetic communities (SynComs). We developed a functionally directed approach to generate SynComs by selecting strains that encode key functions identified in metagenomes. This approach enables the rapid construction of SynComs tailored to any ecosystem. To optimize community design, we implemented genome-scale metabolic models, providing in silico evidence for cooperative strain coexistence prior to experimental validation. Using this strategy, we designed multiple host-specific SynComs, including those for the rumen, mouse, and human microbiomes. By weighting functions differentially enriched in diseased versus healthy individuals, we constructed SynComs that capture complex host-microbe interactions. We designed an inflammatory bowel disease SynCom of 10 members that successfully induced colitis in gnotobiotic IL10-/- mice, demonstrating the potential of this method to model disease-associated microbiomes. Our study establishes a framework for designing functionally representative SynComs of any microbial ecosystem, facilitating mechanistic study.
{"title":"Function-Based Selection of Synthetic Communities Enables Mechanistic Microbiome Studies","authors":"Thomas C A Hitch, Johanna Bosch, Silvia Bolsega, Charlotte Deschamps, Lucie Etienne-Mesmin, Nicole Treichel, Stephanie Blanquet-Diot, Soeren Ocvirk, Marijana Basic, Thomas Clavel","doi":"10.1093/ismejo/wraf209","DOIUrl":"https://doi.org/10.1093/ismejo/wraf209","url":null,"abstract":"Understanding the complex interactions between microbes and their environment requires robust model systems such as synthetic communities (SynComs). We developed a functionally directed approach to generate SynComs by selecting strains that encode key functions identified in metagenomes. This approach enables the rapid construction of SynComs tailored to any ecosystem. To optimize community design, we implemented genome-scale metabolic models, providing in silico evidence for cooperative strain coexistence prior to experimental validation. Using this strategy, we designed multiple host-specific SynComs, including those for the rumen, mouse, and human microbiomes. By weighting functions differentially enriched in diseased versus healthy individuals, we constructed SynComs that capture complex host-microbe interactions. We designed an inflammatory bowel disease SynCom of 10 members that successfully induced colitis in gnotobiotic IL10-/- mice, demonstrating the potential of this method to model disease-associated microbiomes. Our study establishes a framework for designing functionally representative SynComs of any microbial ecosystem, facilitating mechanistic study.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"38 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145089630","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}
Huihui Song, Yuxiang Zhu, Zhelin Qu, Meixue Zhu, Xindong Li, Lijia Zhao, Kunpeng Wang, Ruizhen Zhang, Lei Cui, Yuying Li, Zeran Bian, Weijia Zhang, Yiliang Chen, Liangcheng Du, Jun-Lei Wang, Xian Zhao, Lu Deng, Yan Wang
Mechanisms of bacterial predation are crucial for revealing microbial adaptation strategies and interaction behaviors in the environment, yet they remain poorly understood. Previously, predators were reported to localize prey via specific cues. However, the process and mechanisms by which these cues, including signaling molecules, mediate predator localization remain unclear. Herein, we investigate the dynamic interaction between the predatory bacteria Lysobacter enzymogenes and its prey bacteria. By integrating genetic manipulation, transcriptomic analysis, biochemical assays, and live-cell tracking microscopy at the single-cell level, we present a novel predation strategy mediated by peptidoglycan hydrolase LssL, named peptidoglycan hydrolase-driven Prey Localization and Utilization System (phPLUS). In phPLUS, predators secrete LssL to initiate the Step I of the localization process. LssL then hydrolyzes prey and releases small molecules of glycine, which serve as signaling cues to guide the predator's directional movement and promote the Step II of localization. In turn, prey signals upregulate the expression of LssL, which synergize with type VI secretion system to ultimately mediate prey killing through a novel regulatory pathway. This study reveals a new two-step localization strategy in bacterial predation, highlighting a previously unrecognized predation process and signal regulation mechanism, and expanding our understanding of predator-prey interactions and microbial ecological dynamics.
{"title":"Two-step localization driven by peptidoglycan hydrolase in interbacterial predation","authors":"Huihui Song, Yuxiang Zhu, Zhelin Qu, Meixue Zhu, Xindong Li, Lijia Zhao, Kunpeng Wang, Ruizhen Zhang, Lei Cui, Yuying Li, Zeran Bian, Weijia Zhang, Yiliang Chen, Liangcheng Du, Jun-Lei Wang, Xian Zhao, Lu Deng, Yan Wang","doi":"10.1093/ismejo/wraf208","DOIUrl":"https://doi.org/10.1093/ismejo/wraf208","url":null,"abstract":"Mechanisms of bacterial predation are crucial for revealing microbial adaptation strategies and interaction behaviors in the environment, yet they remain poorly understood. Previously, predators were reported to localize prey via specific cues. However, the process and mechanisms by which these cues, including signaling molecules, mediate predator localization remain unclear. Herein, we investigate the dynamic interaction between the predatory bacteria Lysobacter enzymogenes and its prey bacteria. By integrating genetic manipulation, transcriptomic analysis, biochemical assays, and live-cell tracking microscopy at the single-cell level, we present a novel predation strategy mediated by peptidoglycan hydrolase LssL, named peptidoglycan hydrolase-driven Prey Localization and Utilization System (phPLUS). In phPLUS, predators secrete LssL to initiate the Step I of the localization process. LssL then hydrolyzes prey and releases small molecules of glycine, which serve as signaling cues to guide the predator's directional movement and promote the Step II of localization. In turn, prey signals upregulate the expression of LssL, which synergize with type VI secretion system to ultimately mediate prey killing through a novel regulatory pathway. This study reveals a new two-step localization strategy in bacterial predation, highlighting a previously unrecognized predation process and signal regulation mechanism, and expanding our understanding of predator-prey interactions and microbial ecological dynamics.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"54 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145089631","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}
Bisphenol F, a widely used primary raw material in the production of polycarbonate and epoxy resins, is frequently detected in the environment and poses significant risks to ecosystems and human health. Microorganisms play an important role in bisphenol F degradation in the natural environment; however, the genetic determinants involved remain unknown. A flavoprotein oxidase BpfA from Microbacterium sp. strain F2 was identified in this study, which is responsible for the crucial steps of bisphenol F degradation involving its conversion to 4,4'-dihydroxybenzophenone through three consecutive reactions. BpfA phylogenetically clusters within the 4-phenol oxidizing subfamily of the vanillyl alcohol oxidase/para-cresol methylhydroxylase flavoprotein family. Three homologs in this subfamily-vanillyl alcohol oxidase, eugenol oxidase, and flavoprotein oxidase-shared over 35.0% identity with BpfA and demonstrated bisphenol F-degrading activity, yet the catalytic efficiency of BpfA against bisphenol F (508.1 mM-1 s-1) was significantly higher than that of vanillyl alcohol oxidase (0.2 mM-1 s-1), eugenol oxidase (0.2 mM-1 s-1), and flavoprotein oxidase (0.3 mM-1 s-1). Structural analysis indicated that strong active site hydrophobicity was likely the reason for this high catalytic efficiency. Bioinformatics-based taxonomic profiling revealed that candidate bisphenol F degraders carrying bpfA mainly belonged to the Pseudomonadota and Actinomycetota phyla, and were predominantly found in metagenomes from cultivated land and forests. This study elucidated the function and distribution pattern of bpfA, enhancing our understanding of microbial bisphenol F degradation in the environment.
{"title":"Widespread distribution of BpfA-mediated bisphenol F degradation among members of the Pseudomonadota and Actinomycetota.","authors":"Mingliang Zhang,Changchang Wang,Yanni Huang,Qian Li,Junqiang Hu,Kaihua Pan,Qian Zhu,Wankui Jiang,Jiguo Qiu,Xin Yan,Qing Hong","doi":"10.1093/ismejo/wraf206","DOIUrl":"https://doi.org/10.1093/ismejo/wraf206","url":null,"abstract":"Bisphenol F, a widely used primary raw material in the production of polycarbonate and epoxy resins, is frequently detected in the environment and poses significant risks to ecosystems and human health. Microorganisms play an important role in bisphenol F degradation in the natural environment; however, the genetic determinants involved remain unknown. A flavoprotein oxidase BpfA from Microbacterium sp. strain F2 was identified in this study, which is responsible for the crucial steps of bisphenol F degradation involving its conversion to 4,4'-dihydroxybenzophenone through three consecutive reactions. BpfA phylogenetically clusters within the 4-phenol oxidizing subfamily of the vanillyl alcohol oxidase/para-cresol methylhydroxylase flavoprotein family. Three homologs in this subfamily-vanillyl alcohol oxidase, eugenol oxidase, and flavoprotein oxidase-shared over 35.0% identity with BpfA and demonstrated bisphenol F-degrading activity, yet the catalytic efficiency of BpfA against bisphenol F (508.1 mM-1 s-1) was significantly higher than that of vanillyl alcohol oxidase (0.2 mM-1 s-1), eugenol oxidase (0.2 mM-1 s-1), and flavoprotein oxidase (0.3 mM-1 s-1). Structural analysis indicated that strong active site hydrophobicity was likely the reason for this high catalytic efficiency. Bioinformatics-based taxonomic profiling revealed that candidate bisphenol F degraders carrying bpfA mainly belonged to the Pseudomonadota and Actinomycetota phyla, and were predominantly found in metagenomes from cultivated land and forests. This study elucidated the function and distribution pattern of bpfA, enhancing our understanding of microbial bisphenol F degradation in the environment.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"6 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145089787","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}
Porous ecosystems represent ubiquitous microbial habitats across natural settings including soil, gut tract, and food matrices, where microscale spatial architecture critically shapes microbial colonization and interactions. Yet, the mechanisms of how pore-scale physical constraints influence microbial community assembly and metabolic performance remain poorly understood. Here, we employed a microfluidic platform with tunable inter-pillar spacings, coupled with a multi-omics approach including in situ imaging, exometabolomics, metagenomics, and metatranscriptomics, to investigate how pore-size modulates microbial community dynamics. Comparing representative small (50 μm) and large (150 μm) pore-sizes, we found that larger pore-sizes promoted greater biomass accumulation and significantly enhanced exometabolite production, particularly of amino acids. Microscopy and quantitative assays revealed that 150 μm pores facilitated more efficient substrate degradation, especially of carbohydrates. Taxonomic profiling showed that increasing pore-size reduced community evenness while enhancing richness, selectively enriching carbohydrate-degrading and amino acid-producing taxa, and promoting more complex, positively correlated co-occurrence networks. Metatranscriptomic analysis further demonstrated that larger pore-size significantly upregulated key functional genes involved in substrate degradation, amino acid biosynthesis, and stress response pathways. Fluorescent tracer assays revealed pronounced mass transfer heterogeneity, where smaller pores exhibited prolonged solute persistence and steeper chemical gradients, ultimately restricting substrate availability and microbial activity. Collectively, our results reveal that alleviation of microscale spatial constraints enhances nutrient accessibility, metabolic function, and community organization in porous ecosystems, underscoring the pivotal role of physical microstructure in regulating both the taxonomic composition and functional capacity of microbial ecosystems.
{"title":"Pore-Scale Mass Transfer Heterogeneity Shapes Nutrient Accessibility and Functional Assembly in Porous Microbial Ecosystems.","authors":"Liming Wu,Daixiu Bao,Hui Liao,Meiyu Yan,Yitong Ge,Zinuan Han,Xiaole Xia","doi":"10.1093/ismejo/wraf205","DOIUrl":"https://doi.org/10.1093/ismejo/wraf205","url":null,"abstract":"Porous ecosystems represent ubiquitous microbial habitats across natural settings including soil, gut tract, and food matrices, where microscale spatial architecture critically shapes microbial colonization and interactions. Yet, the mechanisms of how pore-scale physical constraints influence microbial community assembly and metabolic performance remain poorly understood. Here, we employed a microfluidic platform with tunable inter-pillar spacings, coupled with a multi-omics approach including in situ imaging, exometabolomics, metagenomics, and metatranscriptomics, to investigate how pore-size modulates microbial community dynamics. Comparing representative small (50 μm) and large (150 μm) pore-sizes, we found that larger pore-sizes promoted greater biomass accumulation and significantly enhanced exometabolite production, particularly of amino acids. Microscopy and quantitative assays revealed that 150 μm pores facilitated more efficient substrate degradation, especially of carbohydrates. Taxonomic profiling showed that increasing pore-size reduced community evenness while enhancing richness, selectively enriching carbohydrate-degrading and amino acid-producing taxa, and promoting more complex, positively correlated co-occurrence networks. Metatranscriptomic analysis further demonstrated that larger pore-size significantly upregulated key functional genes involved in substrate degradation, amino acid biosynthesis, and stress response pathways. Fluorescent tracer assays revealed pronounced mass transfer heterogeneity, where smaller pores exhibited prolonged solute persistence and steeper chemical gradients, ultimately restricting substrate availability and microbial activity. Collectively, our results reveal that alleviation of microscale spatial constraints enhances nutrient accessibility, metabolic function, and community organization in porous ecosystems, underscoring the pivotal role of physical microstructure in regulating both the taxonomic composition and functional capacity of microbial ecosystems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"126 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145083443","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}
Maximilian Dreer,Thomas Pribasnig,Logan H Hodgskiss,Zhen-Hao Luo,Fran Pozaric,Christa Schleper
Although ammonia-oxidizing archaea (AOA) are globally distributed in nature, growth in biofilms has been relatively little explored. Here we investigated six representatives of three different terrestrial and marine clades of AOA in a longitudinal and quantitative study for their ability to form biofilm, and studied gene expression patterns of three representatives. Although all strains grew on a solid surface, soil strains of the genera Nitrosocosmicus and Nitrososphaera exhibited the highest capacity for biofilm formation. Based on microscopic and gene expression data, two different colonization strategies could be distinguished. S-layer containing AOA (from both soil and marine habitats) initialized attachment as single cells, subsequently forming denser layers, whereas the S-layer free species of the Nitrosocosmicus clade attached as suspended aggregates to the surface and henceforth showed fastest establishment of biofilm. Transcription profiles were significantly different between planktonic and biofilm growth in all strains, and revealed individual transcriptomic responses, albeit fulfilling shared functions. In particular, the strong expression of different types of multicopper oxidases was observed in all strains suggesting modifications of their cell coats. S-layer carrying AOA each additionally expressed a set of adhesion proteins supporting attachment. Detoxification of nitrous compounds, copper acquisition as well as the expression of transcription factor B were also shared responses among biofilm producing strains. However, the majority of differentially expressed protein families was distinct among the three strains, illustrating that individual solutions have evolved for the shared growth mode of biofilm formation in AOA, probably driven by the different ecological niches.
{"title":"Biofilm lifestyle across different lineages of ammonia-oxidizing archaea.","authors":"Maximilian Dreer,Thomas Pribasnig,Logan H Hodgskiss,Zhen-Hao Luo,Fran Pozaric,Christa Schleper","doi":"10.1093/ismejo/wraf182","DOIUrl":"https://doi.org/10.1093/ismejo/wraf182","url":null,"abstract":"Although ammonia-oxidizing archaea (AOA) are globally distributed in nature, growth in biofilms has been relatively little explored. Here we investigated six representatives of three different terrestrial and marine clades of AOA in a longitudinal and quantitative study for their ability to form biofilm, and studied gene expression patterns of three representatives. Although all strains grew on a solid surface, soil strains of the genera Nitrosocosmicus and Nitrososphaera exhibited the highest capacity for biofilm formation. Based on microscopic and gene expression data, two different colonization strategies could be distinguished. S-layer containing AOA (from both soil and marine habitats) initialized attachment as single cells, subsequently forming denser layers, whereas the S-layer free species of the Nitrosocosmicus clade attached as suspended aggregates to the surface and henceforth showed fastest establishment of biofilm. Transcription profiles were significantly different between planktonic and biofilm growth in all strains, and revealed individual transcriptomic responses, albeit fulfilling shared functions. In particular, the strong expression of different types of multicopper oxidases was observed in all strains suggesting modifications of their cell coats. S-layer carrying AOA each additionally expressed a set of adhesion proteins supporting attachment. Detoxification of nitrous compounds, copper acquisition as well as the expression of transcription factor B were also shared responses among biofilm producing strains. However, the majority of differentially expressed protein families was distinct among the three strains, illustrating that individual solutions have evolved for the shared growth mode of biofilm formation in AOA, probably driven by the different ecological niches.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"103 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145018214","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}
Kamal Md Mostafa, Yu-Hsuan Cheng, Li-Wen Chu, Phuong-Thao Nguyen, Chien-Fu Jeff Liu, Chia-Wei Liao, Thomas Posch, Jun-Yi Leu
Mutualistic endosymbiosis is a cornerstone of evolutionary innovation, enabling organisms to exploit diverse niches unavailable to individual species. However, our knowledge about the early evolutionary stage of this relationship remains limited. The association between the ciliate Tetrahymena utriculariae and its algal endosymbiont Micractinium tetrahymenae indicates an incipient stage of photoendosymbiosis. Although T. utriculariae cells rely on endosymbiotic algae to grow in low-oxygen conditions, they gradually lose the endosymbionts in oxic conditions. In this study, comparative phylogenomics revealed accelerated evolution in mitochondrial DNA and nucleus-encoded mitochondrial genes in T. utriculariae. Symbiotic cells displayed elongated mitochondria that interacted intimately with endosymbionts. Inhibition of mitochondrial fatty acid oxidation reduced host fitness but increased the endosymbiont population. Time-series transcriptomics revealed physiological fine-tuning of the host across day-night cycles, highlighting symbiosis-associated regulatory adjustments. Endosymbiotic algae downregulated photosynthesis-related genes compared with free-living cells, which correlated with reduced chlorophyll content, suggesting a shift toward host resource exploitation to compensate for diminished photosynthetic capacity. Under oxic conditions, symbiotic T. utriculariae cells exhibited lower fitness than aposymbiotic cells. Our results demonstrate that incipient endosymbioses employ mitochondrial remodeling and endosymbiont metabolic reprogramming to actively regulate transitions between mutualistic and parasitic states, revealing how symbiotic partnerships navigate environmental pressures during their incipient stage of evolutionary establishment.
{"title":"Environment-dependent mutualism–parasitism transitions in the incipient symbiosis between Tetrahymena utriculariae and Micractinium tetrahymenae","authors":"Kamal Md Mostafa, Yu-Hsuan Cheng, Li-Wen Chu, Phuong-Thao Nguyen, Chien-Fu Jeff Liu, Chia-Wei Liao, Thomas Posch, Jun-Yi Leu","doi":"10.1093/ismejo/wraf203","DOIUrl":"https://doi.org/10.1093/ismejo/wraf203","url":null,"abstract":"Mutualistic endosymbiosis is a cornerstone of evolutionary innovation, enabling organisms to exploit diverse niches unavailable to individual species. However, our knowledge about the early evolutionary stage of this relationship remains limited. The association between the ciliate Tetrahymena utriculariae and its algal endosymbiont Micractinium tetrahymenae indicates an incipient stage of photoendosymbiosis. Although T. utriculariae cells rely on endosymbiotic algae to grow in low-oxygen conditions, they gradually lose the endosymbionts in oxic conditions. In this study, comparative phylogenomics revealed accelerated evolution in mitochondrial DNA and nucleus-encoded mitochondrial genes in T. utriculariae. Symbiotic cells displayed elongated mitochondria that interacted intimately with endosymbionts. Inhibition of mitochondrial fatty acid oxidation reduced host fitness but increased the endosymbiont population. Time-series transcriptomics revealed physiological fine-tuning of the host across day-night cycles, highlighting symbiosis-associated regulatory adjustments. Endosymbiotic algae downregulated photosynthesis-related genes compared with free-living cells, which correlated with reduced chlorophyll content, suggesting a shift toward host resource exploitation to compensate for diminished photosynthetic capacity. Under oxic conditions, symbiotic T. utriculariae cells exhibited lower fitness than aposymbiotic cells. Our results demonstrate that incipient endosymbioses employ mitochondrial remodeling and endosymbiont metabolic reprogramming to actively regulate transitions between mutualistic and parasitic states, revealing how symbiotic partnerships navigate environmental pressures during their incipient stage of evolutionary establishment.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"64 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145002957","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}
Ramunas Stepanauskas,Julia M Brown,Shayesteh Arasti,Uyen Mai,Gregory Gavelis,Maria Pachiadaki,Oliver Bezuidt,Jacob H Munson-McGee,Tianyi Chang,Steven J Biller,Paul M Berube,Siavash Mirarab
Lateral gene transfer is a major evolutionary process in Bacteria and Archaea. Despite its importance, lateral gene transfer quantification in nature using traditional phylogenetic methods has been hampered by the rarity of most genes within the enormous microbial pangenomes. Here, we estimated lateral gene transfer rates within the epipelagic tropical and subtropical ocean using a global, randomized collection of single amplified genomes and a non-phylogenetic computational approach. By comparing the fraction of shared genes between pairs of genomes against a lateral gene transfer-free model, we show that an average cell line laterally acquires and retains ~13% of its genes every 1 million years. This translates to a net lateral gene transfer rate of ~250 genes L-1 seawater day-1 and involves both "flexible" and "core" genes. Our study indicates that whereas most genes are exchanged among closely related cells, the range of lateral gene transfer exceeds the contemporary definition of bacterial species, thus providing prokaryoplankton with extensive genetic resources for lateral gene transfer-based adaptation to environmental stressors. This offers an important starting point for the quantitative analysis of lateral gene transfer in natural settings and its incorporation into evolutionary and ecosystem studies and modeling.
{"title":"Net rate of lateral gene transfer in marine prokaryoplankton.","authors":"Ramunas Stepanauskas,Julia M Brown,Shayesteh Arasti,Uyen Mai,Gregory Gavelis,Maria Pachiadaki,Oliver Bezuidt,Jacob H Munson-McGee,Tianyi Chang,Steven J Biller,Paul M Berube,Siavash Mirarab","doi":"10.1093/ismejo/wraf159","DOIUrl":"https://doi.org/10.1093/ismejo/wraf159","url":null,"abstract":"Lateral gene transfer is a major evolutionary process in Bacteria and Archaea. Despite its importance, lateral gene transfer quantification in nature using traditional phylogenetic methods has been hampered by the rarity of most genes within the enormous microbial pangenomes. Here, we estimated lateral gene transfer rates within the epipelagic tropical and subtropical ocean using a global, randomized collection of single amplified genomes and a non-phylogenetic computational approach. By comparing the fraction of shared genes between pairs of genomes against a lateral gene transfer-free model, we show that an average cell line laterally acquires and retains ~13% of its genes every 1 million years. This translates to a net lateral gene transfer rate of ~250 genes L-1 seawater day-1 and involves both \"flexible\" and \"core\" genes. Our study indicates that whereas most genes are exchanged among closely related cells, the range of lateral gene transfer exceeds the contemporary definition of bacterial species, thus providing prokaryoplankton with extensive genetic resources for lateral gene transfer-based adaptation to environmental stressors. This offers an important starting point for the quantitative analysis of lateral gene transfer in natural settings and its incorporation into evolutionary and ecosystem studies and modeling.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"24 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144995771","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}
京公网安备 11010802042870号
京ICP备2023020795号-1
扫码关注我们
求助内容：
应助结果提醒方式：