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}
Lauren M Hemara, Mark T Andersen, Haileigh R Patterson, Marion Wood, Matthew D Templeton, Jay Jayaraman
Host specificity of a plant pathogen is defined by its effector complement. However, it remains unclear whether the full complement is required for pathogenicity. Pseudomonas syringae pv. actinidiae (Psa) is an emerging model pathogen of kiwifruit with over 30 functional effectors, providing a unique opportunity to understand how host-mediated selection shapes pathogen evolution. The majority of Psa’s effectors previously appeared non-essential in single knockout contexts. Why, then, does Psa maintain such a large repertoire? We sought to examine effector requirements, redundancies, and repertoire refinement across host genotypes through a mutated effector-leveraging evolution experiment (MELEE), serially passaging competitive populations of effector knockout strains. Competition suggests that all effectors are collectively required for successful virulence, demonstrated by the dominance of wild-type. Host-specific effector requirements identified may further explain the maintenance of this large effector repertoire, providing important insights into the dynamics of effector redundancy following incursions.
{"title":"Individually redundant effectors are collectively required for bacterial pathogen virulence","authors":"Lauren M Hemara, Mark T Andersen, Haileigh R Patterson, Marion Wood, Matthew D Templeton, Jay Jayaraman","doi":"10.1093/ismejo/wraf262","DOIUrl":"https://doi.org/10.1093/ismejo/wraf262","url":null,"abstract":"Host specificity of a plant pathogen is defined by its effector complement. However, it remains unclear whether the full complement is required for pathogenicity. Pseudomonas syringae pv. actinidiae (Psa) is an emerging model pathogen of kiwifruit with over 30 functional effectors, providing a unique opportunity to understand how host-mediated selection shapes pathogen evolution. The majority of Psa’s effectors previously appeared non-essential in single knockout contexts. Why, then, does Psa maintain such a large repertoire? We sought to examine effector requirements, redundancies, and repertoire refinement across host genotypes through a mutated effector-leveraging evolution experiment (MELEE), serially passaging competitive populations of effector knockout strains. Competition suggests that all effectors are collectively required for successful virulence, demonstrated by the dominance of wild-type. Host-specific effector requirements identified may further explain the maintenance of this large effector repertoire, providing important insights into the dynamics of effector redundancy following incursions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"7 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145599051","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}
Organismal life cycles are influenced by Earth’s rotation and orbit, generating daily and seasonal light cycles that vary with latitude, especially in temperate and polar zones. Photoperiodism relies on organisms’ ability to measure time via the circadian clock and detect light through specific photoreceptors. Molecular basis of photoperiodism is well-characterized in plants, but photoperiod adaptation in phytoplankton remain largely unexplored. Here, we investigated circadian clock components, photoreceptors, and associated effectors in eukaryote picoalga species from Ostreococcus, Bathycoccus, and Micromonas. We showed that the investigated species shared a conserved set of homologous circadian clock-related genes that appeared in the early evolution of Mamielalles order. Furthermore, gene duplication events account for the specific occurrences and uneven gene copy numbers among these genera. Through metagenomic and metatranscriptomic analyses, we assessed the gene expression profiles of candidate photoperiod-related genes across the global ocean. Our findings reveal an unexpected diversity in photoreceptors, particularly within Micromonas, and highlight the CCT domain family, a key group of transcription factors governing circadian rhythms (TOC1 family) and photoperiodism (CONSTANS family) in plants. TOC1, a central component of the circadian clock in Ostreococcus tauri, is either absent or truncated in tropical species. Functional assays further indicate that the TOC1/CCA1 oscillator is non-functional in the tropical strain of Ostreococcus sp. RCC809. These results imply that certain circadian mechanisms may be dispensable at low latitudes, underscoring the diversity of photoperiod adaptations in marine phytoplankton. These results provide valuable insights into the molecular evolution of cosmopolitan plankton groups, particularly their mechanisms of local adaptation.
{"title":"Latitudinal Diversity in Circadian and Light-Sensing Genes in an Ecologically Vital Group of Marine Picoeukaryote Algae","authors":"Janaina Rigonato, Jean-Claude Lozano, Valérie Vergé, Olivier Jaillon, François-Yves Bouget","doi":"10.1093/ismejo/wraf263","DOIUrl":"https://doi.org/10.1093/ismejo/wraf263","url":null,"abstract":"Organismal life cycles are influenced by Earth’s rotation and orbit, generating daily and seasonal light cycles that vary with latitude, especially in temperate and polar zones. Photoperiodism relies on organisms’ ability to measure time via the circadian clock and detect light through specific photoreceptors. Molecular basis of photoperiodism is well-characterized in plants, but photoperiod adaptation in phytoplankton remain largely unexplored. Here, we investigated circadian clock components, photoreceptors, and associated effectors in eukaryote picoalga species from Ostreococcus, Bathycoccus, and Micromonas. We showed that the investigated species shared a conserved set of homologous circadian clock-related genes that appeared in the early evolution of Mamielalles order. Furthermore, gene duplication events account for the specific occurrences and uneven gene copy numbers among these genera. Through metagenomic and metatranscriptomic analyses, we assessed the gene expression profiles of candidate photoperiod-related genes across the global ocean. Our findings reveal an unexpected diversity in photoreceptors, particularly within Micromonas, and highlight the CCT domain family, a key group of transcription factors governing circadian rhythms (TOC1 family) and photoperiodism (CONSTANS family) in plants. TOC1, a central component of the circadian clock in Ostreococcus tauri, is either absent or truncated in tropical species. Functional assays further indicate that the TOC1/CCA1 oscillator is non-functional in the tropical strain of Ostreococcus sp. RCC809. These results imply that certain circadian mechanisms may be dispensable at low latitudes, underscoring the diversity of photoperiod adaptations in marine phytoplankton. These results provide valuable insights into the molecular evolution of cosmopolitan plankton groups, particularly their mechanisms of local adaptation.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"150 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145610940","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}
Yang Zhou, Yongqiang Yang, Yuqi Mao, Zhangqun Hou, Yiyang Xu, Kelei Zhao, Yiwen Chu, Xinrong Wang, Can Wang, Shun Li, Fei Xu, Likai Hao, Binbin Xie, Jiafu Lin, Tao Song
Macrolide antibiotics are vital for controlling infections in humans, animals, and agriculture, yet their effectiveness is increasingly compromised by antimicrobial resistance. Macrolide esterases (MLEs) are key mediators of macrolide resistance but have only been detected in Gram-negative bacteria, with no evidence in Gram-positive species. Here, we mined over 500,000 Gram-positive genomes and identified 8,707 candidate proteins. Six representative MLEs were functionally validated, conferring resistance to 16-membered macrolides and increasing minimum inhibitory concentrations up to 16-fold in Escherichia coli and 128-fold in Bacillus subtilis. Moreover, two exhibited broad-spectrum activity against all clinically and veterinary relevant 16-membered macrolides. Temporal analysis revealed that Gram-positive MLEs originated at least 2.7 million years ago, contrasting with their emergence in Gram-negative bacteria after the introduction of antibiotics. Genomic surveys further demonstrated the global distribution of MLE-carrying Gram-positive bacteria across 97 countries and diverse ecosystems, including clinical, food, agricultural, and natural environments. These findings highlight Gram-positive MLEs as an underrecognized risk and underscore the need for a One Health–oriented strategy to monitor, assess, and mitigate the spread of macrolide resistance across interconnected ecosystems.
{"title":"Global distribution of α/β hydrolase family macrolide esterases in Gram-positive bacteria","authors":"Yang Zhou, Yongqiang Yang, Yuqi Mao, Zhangqun Hou, Yiyang Xu, Kelei Zhao, Yiwen Chu, Xinrong Wang, Can Wang, Shun Li, Fei Xu, Likai Hao, Binbin Xie, Jiafu Lin, Tao Song","doi":"10.1093/ismejo/wraf261","DOIUrl":"https://doi.org/10.1093/ismejo/wraf261","url":null,"abstract":"Macrolide antibiotics are vital for controlling infections in humans, animals, and agriculture, yet their effectiveness is increasingly compromised by antimicrobial resistance. Macrolide esterases (MLEs) are key mediators of macrolide resistance but have only been detected in Gram-negative bacteria, with no evidence in Gram-positive species. Here, we mined over 500,000 Gram-positive genomes and identified 8,707 candidate proteins. Six representative MLEs were functionally validated, conferring resistance to 16-membered macrolides and increasing minimum inhibitory concentrations up to 16-fold in Escherichia coli and 128-fold in Bacillus subtilis. Moreover, two exhibited broad-spectrum activity against all clinically and veterinary relevant 16-membered macrolides. Temporal analysis revealed that Gram-positive MLEs originated at least 2.7 million years ago, contrasting with their emergence in Gram-negative bacteria after the introduction of antibiotics. Genomic surveys further demonstrated the global distribution of MLE-carrying Gram-positive bacteria across 97 countries and diverse ecosystems, including clinical, food, agricultural, and natural environments. These findings highlight Gram-positive MLEs as an underrecognized risk and underscore the need for a One Health–oriented strategy to monitor, assess, and mitigate the spread of macrolide resistance across interconnected ecosystems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145599050","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}
Jibing Li, Xixi Cai, Menghui Li, Dayi Zhang, Bei Li, Ling N Jin, Chunling Luo, Gan Zhang
Fungi play critical but underappreciated roles comparing to bacteria in the bioremediation of organic pollutants, particularly emerging contaminants. Numerous fungal species, along with their functional genes and metabolic pathways, remain largely unexplored. Here, we integrate single-cell Raman-activated cell sorting with stable isotope probing to identify and characterize in situ active fungi involved in emerging contaminant degradation. This approach enabled the isolation of a Penicillium sp. strain LJD-20, previously unreported, which acts as an active degrader of 2-methylnaphthalene, a model emerging pollutant. Genomic analyses revealed that LJD-20 harbors a diverse repertoire of degradation-related genes, including those encoding dioxygenases, methylhydroxylases, and cytochrome P450 monooxygenases, highlighting its versatile metabolic potential. Single-cell genome sequencing also uncovered a potential close fungal–bacterial co-occurrence, suggesting possible ecological or metabolic interactions. In bioaugmentation trials, strain LJD-20 independently degraded 2-methylnaphthalene and simultaneously promoted the enrichment of other microorganisms involved in its removal. These findings highlight the metabolic versatility and ecological importance of fungi in pollutant degradation and demonstrate the utility of combining single-cell and isotopic approaches to explore microbial function and interaction in complex environments.
{"title":"In situ Degradation of 2-Methylnaphthalene by a Soil Penicillium Strain Associated with Fungal-Bacterial Interactions","authors":"Jibing Li, Xixi Cai, Menghui Li, Dayi Zhang, Bei Li, Ling N Jin, Chunling Luo, Gan Zhang","doi":"10.1093/ismejo/wraf260","DOIUrl":"https://doi.org/10.1093/ismejo/wraf260","url":null,"abstract":"Fungi play critical but underappreciated roles comparing to bacteria in the bioremediation of organic pollutants, particularly emerging contaminants. Numerous fungal species, along with their functional genes and metabolic pathways, remain largely unexplored. Here, we integrate single-cell Raman-activated cell sorting with stable isotope probing to identify and characterize in situ active fungi involved in emerging contaminant degradation. This approach enabled the isolation of a Penicillium sp. strain LJD-20, previously unreported, which acts as an active degrader of 2-methylnaphthalene, a model emerging pollutant. Genomic analyses revealed that LJD-20 harbors a diverse repertoire of degradation-related genes, including those encoding dioxygenases, methylhydroxylases, and cytochrome P450 monooxygenases, highlighting its versatile metabolic potential. Single-cell genome sequencing also uncovered a potential close fungal–bacterial co-occurrence, suggesting possible ecological or metabolic interactions. In bioaugmentation trials, strain LJD-20 independently degraded 2-methylnaphthalene and simultaneously promoted the enrichment of other microorganisms involved in its removal. These findings highlight the metabolic versatility and ecological importance of fungi in pollutant degradation and demonstrate the utility of combining single-cell and isotopic approaches to explore microbial function and interaction in complex environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145594092","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}
Bathyarchaeia, among the most ancient and abundant microbial lineages on Earth, dominate diverse anoxic subsurface ecosystems and play a pivotal role in global carbon cycling. This review synthesizes current understanding of their physiological, metabolic, and evolutionary foundations underlying their ecological significance and environmental effects over geological timescales. Despite their global distribution in the deep biosphere, the phylogenetic diversity and total cellular abundance of Bathyarchaeia remain substantially underestimated. As uncultivated metabolic generalists, Bathyarchaeia exhibit remarkable metabolic versatility, including anaerobic organic degradation, dark carbon fixation, and putative methane and alkane metabolism. Specifically, genus Baizosediminiarchaeum has been demonstrated to adopt organomixotrophy by coupling anaerobic lignin degradation with inorganic carbon assimilation. These metabolic strategies likely enable them to thrive in energy-limited subsurface environments with dynamic geochemical fluctuation. The early evolutionary history of Bathyarchaeia appears closely linked to major geological events, including tectonic activity and plant evolution, whereas more recent lineage expansions reflect physiological adaptations to host-associated and anthropogenically influenced environments, highlighting their on-going co-evolution with Earth's modern environments. Overall, we propose carbon metabolic innovation as the central driver behind the ecological and evolutionary significance of Bathyarchaeia, putatively linking microbial ecological functions to planetary biogeochemical processes. Future efforts in isolation and cultivation remains essential for elucidating their unknown physiological and metabolic mechanisms. In parallel, advances in ecological modeling and the development of lineage-specific lipid biomarkers hold great promise for quantifying their contributions to global carbon budgets and reconstructing paleoenvironmental and paleoclimate conditions.
{"title":"Carbon metabolic versatility underpins Bathyarchaeia ecological significance across the global deep subsurface.","authors":"Jialin Hou 侯佳林,Chen Yang 杨琛,Fengping Wang 王风平","doi":"10.1093/ismejo/wraf259","DOIUrl":"https://doi.org/10.1093/ismejo/wraf259","url":null,"abstract":"Bathyarchaeia, among the most ancient and abundant microbial lineages on Earth, dominate diverse anoxic subsurface ecosystems and play a pivotal role in global carbon cycling. This review synthesizes current understanding of their physiological, metabolic, and evolutionary foundations underlying their ecological significance and environmental effects over geological timescales. Despite their global distribution in the deep biosphere, the phylogenetic diversity and total cellular abundance of Bathyarchaeia remain substantially underestimated. As uncultivated metabolic generalists, Bathyarchaeia exhibit remarkable metabolic versatility, including anaerobic organic degradation, dark carbon fixation, and putative methane and alkane metabolism. Specifically, genus Baizosediminiarchaeum has been demonstrated to adopt organomixotrophy by coupling anaerobic lignin degradation with inorganic carbon assimilation. These metabolic strategies likely enable them to thrive in energy-limited subsurface environments with dynamic geochemical fluctuation. The early evolutionary history of Bathyarchaeia appears closely linked to major geological events, including tectonic activity and plant evolution, whereas more recent lineage expansions reflect physiological adaptations to host-associated and anthropogenically influenced environments, highlighting their on-going co-evolution with Earth's modern environments. Overall, we propose carbon metabolic innovation as the central driver behind the ecological and evolutionary significance of Bathyarchaeia, putatively linking microbial ecological functions to planetary biogeochemical processes. Future efforts in isolation and cultivation remains essential for elucidating their unknown physiological and metabolic mechanisms. In parallel, advances in ecological modeling and the development of lineage-specific lipid biomarkers hold great promise for quantifying their contributions to global carbon budgets and reconstructing paleoenvironmental and paleoclimate conditions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"9 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145559199","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}
Qing-Lian Wu, Tian Lan, Lin Deng, Jing-Wen Jia, Wei-Tong Ren, Hua-Zhe Wang, Juan-Shan Du, Nan-Qi Ren, Wan-Qian Guo
Widespread aromatic pollutants such as benzene, toluene, ethylbenzene, and xylene are traditionally considered to drive soil carbon loss through mineralisation and ecotoxicity. Contrary to this view, our study reveals that low concentrations of these pollutants stimulate microbial carbon chain elongation—a previously overlooked carbon conversion pathway producing medium-chain fatty acids, thereby reshaping soil carbon dynamics. Using phased amplicon sequencing, metagenomics, and metaproteomics of soil microcosms amended with these compounds, we demonstrate that aromatic pollutants bidirectionally regulate carbon chain elongation at both taxonomic and molecular levels. These pollutants selectively enrich Clostridium_sensu_stricto_12 and Rummelibacillus while suppressing Acinetobacter, a key elongation taxon in natural soils. Simultaneously, they inhibit Petrimonas, a syntrophic fatty acid degrader, promoting the accumulation of medium-chain fatty acids. Carbon chain-elongating bacteria cooperate with aromatic degraders, redirecting pollutant-derived carbon towards chain elongation rather than complete mineralisation to CO₂. Among them, Bacillus occupies a pivotal niche bridging aromatic degradation and carbon elongation. At the molecular level, aromatic pollutants enhance chain elongation by accelerating substrate uptake and channelling the key intermediate acetyl-CoA into the reverse β-oxidation pathway. Additionally, aromatic pollutants restrain fatty acid biosynthesis pathway by upregulating fabR, whereas inhibiting acrR and fadR. They also maintain NADH availability to alleviate Rex-mediated repression of bcd, a critical gene in the β-oxidation pathway. However, high concentrations of aromatic pollutants disrupt metabolic homeostasis and suppress chain elongation activity. Our findings redefine the ecological impact of aromatic hydrocarbon contamination in soil, demonstrating their role in modulating anaerobic carbon fixation and retention within soil microbial communities.
{"title":"Aromatic Pollutants Rewire Soil Microbial Carbon Fixation via Chain Elongation","authors":"Qing-Lian Wu, Tian Lan, Lin Deng, Jing-Wen Jia, Wei-Tong Ren, Hua-Zhe Wang, Juan-Shan Du, Nan-Qi Ren, Wan-Qian Guo","doi":"10.1093/ismejo/wraf254","DOIUrl":"https://doi.org/10.1093/ismejo/wraf254","url":null,"abstract":"Widespread aromatic pollutants such as benzene, toluene, ethylbenzene, and xylene are traditionally considered to drive soil carbon loss through mineralisation and ecotoxicity. Contrary to this view, our study reveals that low concentrations of these pollutants stimulate microbial carbon chain elongation—a previously overlooked carbon conversion pathway producing medium-chain fatty acids, thereby reshaping soil carbon dynamics. Using phased amplicon sequencing, metagenomics, and metaproteomics of soil microcosms amended with these compounds, we demonstrate that aromatic pollutants bidirectionally regulate carbon chain elongation at both taxonomic and molecular levels. These pollutants selectively enrich Clostridium_sensu_stricto_12 and Rummelibacillus while suppressing Acinetobacter, a key elongation taxon in natural soils. Simultaneously, they inhibit Petrimonas, a syntrophic fatty acid degrader, promoting the accumulation of medium-chain fatty acids. Carbon chain-elongating bacteria cooperate with aromatic degraders, redirecting pollutant-derived carbon towards chain elongation rather than complete mineralisation to CO₂. Among them, Bacillus occupies a pivotal niche bridging aromatic degradation and carbon elongation. At the molecular level, aromatic pollutants enhance chain elongation by accelerating substrate uptake and channelling the key intermediate acetyl-CoA into the reverse β-oxidation pathway. Additionally, aromatic pollutants restrain fatty acid biosynthesis pathway by upregulating fabR, whereas inhibiting acrR and fadR. They also maintain NADH availability to alleviate Rex-mediated repression of bcd, a critical gene in the β-oxidation pathway. However, high concentrations of aromatic pollutants disrupt metabolic homeostasis and suppress chain elongation activity. Our findings redefine the ecological impact of aromatic hydrocarbon contamination in soil, demonstrating their role in modulating anaerobic carbon fixation and retention within soil microbial communities.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"109 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145594093","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 Lehenberger, Yu Pan, Stefanie Ungerer, Michael Reichelt, Daniela Pemp, Christian Paetz, Josef Lehenberger, Niklas Gentsch, Felix Feistel, Peter Gros, Leane Lehmann, Jonathan Gershenzon
Wood-colonizing beetles are associated with a diversity of microbes many of which are thought to act as mutualists with their beetle hosts, but the evidence is usually anecdotal. The ship-timber beetle Elateroides dermestoides, one of the few fungus-farming but non-social ambrosia beetles, is described to have a mutualistic relationship with the yeast-like fungus Alloascoidea hylecoeti. Here, we tested the hypothesis that A. hylecoeti has a high nutrient content thus allowing it to function as a valuable food source for the solitary larvae of E. dermestoides, which bore into the wood of dead trees, an extremely nutrient-poor substrate. Our analyses revealed that A. hylecoeti is rich in soluble sugars, free amino acids, ergosterol, phosphorus, and potassium compared to the other fungi measured, and also accumulates high amounts of fatty acids, B vitamins and nitrogen. We also tested whether A. hylecoeti possesses chemical mechanisms to suppress antagonistic microbes. Extracts from A. hylecoeti and chemical compounds produced or accumulated by this fungus were found to significantly inhibit the growth of potentially competing fungi. The active substances include fungal-produced monoterpenes and acetic acid, as well as phenolic compounds accumulated from host tree tissues. Moreover, sufficient acetic acid was released by A. hylecoeti to drop the medium pH to as low as 3.6, which inhibited all tested competitors, whereas the growth of A. hylecoeti was promoted. Taken together, the nutritional properties and competitive ability of A. hylecoeti may make a major contribution to the success of its insect partner, the ship-timber beetle under natural conditions.
{"title":"Fungal symbiont of an ambrosia beetle possesses high nutrient content and suppresses competing fungi with antimicrobial compounds","authors":"Maximilian Lehenberger, Yu Pan, Stefanie Ungerer, Michael Reichelt, Daniela Pemp, Christian Paetz, Josef Lehenberger, Niklas Gentsch, Felix Feistel, Peter Gros, Leane Lehmann, Jonathan Gershenzon","doi":"10.1093/ismejo/wraf258","DOIUrl":"https://doi.org/10.1093/ismejo/wraf258","url":null,"abstract":"Wood-colonizing beetles are associated with a diversity of microbes many of which are thought to act as mutualists with their beetle hosts, but the evidence is usually anecdotal. The ship-timber beetle Elateroides dermestoides, one of the few fungus-farming but non-social ambrosia beetles, is described to have a mutualistic relationship with the yeast-like fungus Alloascoidea hylecoeti. Here, we tested the hypothesis that A. hylecoeti has a high nutrient content thus allowing it to function as a valuable food source for the solitary larvae of E. dermestoides, which bore into the wood of dead trees, an extremely nutrient-poor substrate. Our analyses revealed that A. hylecoeti is rich in soluble sugars, free amino acids, ergosterol, phosphorus, and potassium compared to the other fungi measured, and also accumulates high amounts of fatty acids, B vitamins and nitrogen. We also tested whether A. hylecoeti possesses chemical mechanisms to suppress antagonistic microbes. Extracts from A. hylecoeti and chemical compounds produced or accumulated by this fungus were found to significantly inhibit the growth of potentially competing fungi. The active substances include fungal-produced monoterpenes and acetic acid, as well as phenolic compounds accumulated from host tree tissues. Moreover, sufficient acetic acid was released by A. hylecoeti to drop the medium pH to as low as 3.6, which inhibited all tested competitors, whereas the growth of A. hylecoeti was promoted. Taken together, the nutritional properties and competitive ability of A. hylecoeti may make a major contribution to the success of its insect partner, the ship-timber beetle under natural conditions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"172 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145553961","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：