Microbial communities are crucial in host adaptation to stressors, particularly in dynamic ecosystems. In aquatic environments, Daphnia magna is ideal for studying host-microbiome interactions due to its ecological importance and sensitivity. Adaptation to toxins, such as those produced by cyanobacteria, may involve both host and microbial gene repertoires. Yet, the influence of microbiota composition and function on host performance remains poorly understood. Because epigenetic mechanisms such as DNA methylation regulate gene expression and mediate adaptive responses, we also investigated whether these associations are reflected in DNA methylation levels. To address this, we conducted a fully factorial transplant experiment using microbiota-depleted Daphnia colonised with microbiota from the same or different genotype, previously exposed to toxic or non-toxic diets, or left uncolonised. We assessed life-history traits, microbial composition (16S rRNA genes), functional profiles (whole-genome-resequencing), and DNA methylation (colorimetric quantification). Daphnia fed non-toxic diets grew larger and reproduced more. Increased methylation occurred when microbiota donors differed from the host genotype and was strongest under toxic diet. Dysbiosis and reduced performance were noted in individuals colonised with toxic-diet microbiota from another genotype, where Limnohabitans spp. was reduced or absent. Signs of hormesis emerged when Daphnia received microbiota from their own genotype reared on non-toxic diets. DNA methylation of both host and microbiota was associated with functional pathways, including increased mitochondrial fatty acid biosynthesis. These findings highlight the importance of host-microbiota matching and microbial environmental history in shaping host performance and epigenetic responses, emphasizing the need to consider host-microbe-environment interactions in evolutionary and ecological studies.
{"title":"Host-microbiota matching and epigenetic modulation drive Daphnia magna responses to cyanobacterial stress.","authors":"Karen Bisschop,Naina Goel,Manon Coone,Isabel Vanoverberghe,Anna Greffe,Jana Asselman,Ellen Decaestecker","doi":"10.1093/ismejo/wraf247","DOIUrl":"https://doi.org/10.1093/ismejo/wraf247","url":null,"abstract":"Microbial communities are crucial in host adaptation to stressors, particularly in dynamic ecosystems. In aquatic environments, Daphnia magna is ideal for studying host-microbiome interactions due to its ecological importance and sensitivity. Adaptation to toxins, such as those produced by cyanobacteria, may involve both host and microbial gene repertoires. Yet, the influence of microbiota composition and function on host performance remains poorly understood. Because epigenetic mechanisms such as DNA methylation regulate gene expression and mediate adaptive responses, we also investigated whether these associations are reflected in DNA methylation levels. To address this, we conducted a fully factorial transplant experiment using microbiota-depleted Daphnia colonised with microbiota from the same or different genotype, previously exposed to toxic or non-toxic diets, or left uncolonised. We assessed life-history traits, microbial composition (16S rRNA genes), functional profiles (whole-genome-resequencing), and DNA methylation (colorimetric quantification). Daphnia fed non-toxic diets grew larger and reproduced more. Increased methylation occurred when microbiota donors differed from the host genotype and was strongest under toxic diet. Dysbiosis and reduced performance were noted in individuals colonised with toxic-diet microbiota from another genotype, where Limnohabitans spp. was reduced or absent. Signs of hormesis emerged when Daphnia received microbiota from their own genotype reared on non-toxic diets. DNA methylation of both host and microbiota was associated with functional pathways, including increased mitochondrial fatty acid biosynthesis. These findings highlight the importance of host-microbiota matching and microbial environmental history in shaping host performance and epigenetic responses, emphasizing the need to consider host-microbe-environment interactions in evolutionary and ecological studies.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"112 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145433853","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}
Xuhui Huang,Emily E Chase,Brittany N Zepernick,Robbie M Martin,Lauren E Krausfeldt,Helena L Pound,Hanqi Wu,Zheng Zheng,Steven W Wilhelm
Cyanobacterial blooms dominated by Microcystis spp. pose significant ecological challenges, including the release of toxins and disruption of aquatic food webs. Although Microcystis can exist as free-living single cells or within dense mucilaginous colonies, the drivers and consequences of colony formation remain unclear. Here, we integrated metatranscriptomic datasets from two Microcystis bloom events in Lake Taihu, China, to analyze and to support findings on the functional differences between colonial and single-cell Microcystis. Our results confirmed colony expression profiles were disproportionately enriched in Microcystis transcripts compared to other prokaryotic taxa. This pattern exhibits Black Queen-like dynamics, where Microcystis assumes greater metabolic and defensive roles while associated bacteria reduce their transcriptional activity. Concomitantly, viral infection strategies diverged by Microcystis community morphology: colony-associated cells expressed lysogeny-associated genes, whereas single cells exhibited increased signatures of lytic infection. These data are consistent with the hypothesis that Microcystis colonies foster conditions favorable to lysogen formation-likely due to local high cell densities and the resulting advantage of superinfection immunity-whereas solitary cells experience stronger lytic pressure. On a broader scale, our findings refine the understanding of bloom dynamics by identifying how community morphological states coincide with distinct host-virus interactions. Cumulatively, this work underscores the importance of colony formation in shaping Microcystis ecology and highlights the need for further mechanistic studies to disentangle the complex interplay between phage infection modes, colony formation, and microbial community structure.
{"title":"Contrasting viral infection strategies for single cell and colonial Microcystis populations consistent with Black Queen dynamics.","authors":"Xuhui Huang,Emily E Chase,Brittany N Zepernick,Robbie M Martin,Lauren E Krausfeldt,Helena L Pound,Hanqi Wu,Zheng Zheng,Steven W Wilhelm","doi":"10.1093/ismejo/wraf244","DOIUrl":"https://doi.org/10.1093/ismejo/wraf244","url":null,"abstract":"Cyanobacterial blooms dominated by Microcystis spp. pose significant ecological challenges, including the release of toxins and disruption of aquatic food webs. Although Microcystis can exist as free-living single cells or within dense mucilaginous colonies, the drivers and consequences of colony formation remain unclear. Here, we integrated metatranscriptomic datasets from two Microcystis bloom events in Lake Taihu, China, to analyze and to support findings on the functional differences between colonial and single-cell Microcystis. Our results confirmed colony expression profiles were disproportionately enriched in Microcystis transcripts compared to other prokaryotic taxa. This pattern exhibits Black Queen-like dynamics, where Microcystis assumes greater metabolic and defensive roles while associated bacteria reduce their transcriptional activity. Concomitantly, viral infection strategies diverged by Microcystis community morphology: colony-associated cells expressed lysogeny-associated genes, whereas single cells exhibited increased signatures of lytic infection. These data are consistent with the hypothesis that Microcystis colonies foster conditions favorable to lysogen formation-likely due to local high cell densities and the resulting advantage of superinfection immunity-whereas solitary cells experience stronger lytic pressure. On a broader scale, our findings refine the understanding of bloom dynamics by identifying how community morphological states coincide with distinct host-virus interactions. Cumulatively, this work underscores the importance of colony formation in shaping Microcystis ecology and highlights the need for further mechanistic studies to disentangle the complex interplay between phage infection modes, colony formation, and microbial community structure.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145433856","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}
Fangze Gui,Yusufjon Gafforov,Juan Ignacio Vílchez,Jiangtao Zhao,Zhonghua Ma,Tianxing Lv,Mengcen Wang
Chemical communication, a universal mode among the interactive members within dynamic plant-microbiome systems, fundamentally drives coevolutionary trajectories. Emerging evidence suggests the critical role of epigenetic regulation in chemical communication, though its mechanistic insights are yet not well understood, a gap that has limited the precise mining of microbiomes function in modern agriculture. Here, we synthesize recent findings from chemistry to epigenetics to illuminate the overlooked epigenetic landscape in plant-microbiome chemical communication. Revisiting the traditional plant-pathogen interaction model and a more complex ternary model involving the plant resident microbiota, we not only present knowledge gaps but also critically dissect the paradoxical roles of resident microbiota by proposing four chemo-epigenetic patterns that fine-tune the interactions among plants, resident microbiota and pathogens. Further, Intelligent Click Chemistry (ICC), an innovative interdisciplinary strategy integrating click chemistry and artificial intelligence, is proposed and discussed, with the aim of unraveling the complex chemo-epigenetic events underlying plant-microbiome chemical communication. Untangling the epigenetic landscape underpinning plant-microbiome chemical communication would enable the strategic and precise exploitation of beneficial microbial traits and suppression of detrimental interactions for sustainable agriculture.
{"title":"Epigenetic landscape underlying plant-microbiome chemical communication.","authors":"Fangze Gui,Yusufjon Gafforov,Juan Ignacio Vílchez,Jiangtao Zhao,Zhonghua Ma,Tianxing Lv,Mengcen Wang","doi":"10.1093/ismejo/wraf249","DOIUrl":"https://doi.org/10.1093/ismejo/wraf249","url":null,"abstract":"Chemical communication, a universal mode among the interactive members within dynamic plant-microbiome systems, fundamentally drives coevolutionary trajectories. Emerging evidence suggests the critical role of epigenetic regulation in chemical communication, though its mechanistic insights are yet not well understood, a gap that has limited the precise mining of microbiomes function in modern agriculture. Here, we synthesize recent findings from chemistry to epigenetics to illuminate the overlooked epigenetic landscape in plant-microbiome chemical communication. Revisiting the traditional plant-pathogen interaction model and a more complex ternary model involving the plant resident microbiota, we not only present knowledge gaps but also critically dissect the paradoxical roles of resident microbiota by proposing four chemo-epigenetic patterns that fine-tune the interactions among plants, resident microbiota and pathogens. Further, Intelligent Click Chemistry (ICC), an innovative interdisciplinary strategy integrating click chemistry and artificial intelligence, is proposed and discussed, with the aim of unraveling the complex chemo-epigenetic events underlying plant-microbiome chemical communication. Untangling the epigenetic landscape underpinning plant-microbiome chemical communication would enable the strategic and precise exploitation of beneficial microbial traits and suppression of detrimental interactions for sustainable agriculture.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"35 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145433854","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}
This study reports the isolation and characterization of Bacteriovorax sp. As-1, a predatory bacterium recovered from the gut of oxytetracycline-treated juvenile rainbow trout (Oncorhynchus mykiss). Phylogenetic and genomic analysis indicate it is closely related to Bacteriovorax stolpii DSM 12778T, although genomic metrics suggest it represents a new species. Like other Bdellovibrio-and-like organisms, Bacteriovorax sp. As-1 exhibits predatory activity against Aeromonas salmonicida, significantly reducing its prey viability by nearly six orders of magnitude. However, whole genome sequencing revealed the presence of multiple antibiotic resistance genes, including those previously associated with decreased susceptibility to tetracyclines, aminoglycosides, sulfonamides, and fluoroquinolones, located within genomic islands, and flanked by insertion sequences, suggesting acquisition via horizontal gene transfer. In addition to these, mutations were also detected in gyrA gene that confer resistance to ciprofloxacin. Phenotypic assays confirmed Bacteriovorax sp. As-1 has increased antibiotic resistance as compared to Bx. stolpii DSM 12778T. This study presents a natural predatory strain carrying IS-linked ARG clusters consistent with horizontal gene transfer, highlighting their potential role as reservoirs of resistance determinants in antibiotic-enriched environments.
{"title":"Acquisition of Novel Antibiotic Resistance Genes by the Bacterial Predator Bacteriovorax sp. As-1.","authors":"Fathrinah Binti Kohadie,Young-Ung Heo,Wonsik Mun,Sumin Choi,Sinseong Park,Yoonhang Lee,Do-Hyung Kim,Robert J Mitchell","doi":"10.1093/ismejo/wraf245","DOIUrl":"https://doi.org/10.1093/ismejo/wraf245","url":null,"abstract":"This study reports the isolation and characterization of Bacteriovorax sp. As-1, a predatory bacterium recovered from the gut of oxytetracycline-treated juvenile rainbow trout (Oncorhynchus mykiss). Phylogenetic and genomic analysis indicate it is closely related to Bacteriovorax stolpii DSM 12778T, although genomic metrics suggest it represents a new species. Like other Bdellovibrio-and-like organisms, Bacteriovorax sp. As-1 exhibits predatory activity against Aeromonas salmonicida, significantly reducing its prey viability by nearly six orders of magnitude. However, whole genome sequencing revealed the presence of multiple antibiotic resistance genes, including those previously associated with decreased susceptibility to tetracyclines, aminoglycosides, sulfonamides, and fluoroquinolones, located within genomic islands, and flanked by insertion sequences, suggesting acquisition via horizontal gene transfer. In addition to these, mutations were also detected in gyrA gene that confer resistance to ciprofloxacin. Phenotypic assays confirmed Bacteriovorax sp. As-1 has increased antibiotic resistance as compared to Bx. stolpii DSM 12778T. This study presents a natural predatory strain carrying IS-linked ARG clusters consistent with horizontal gene transfer, highlighting their potential role as reservoirs of resistance determinants in antibiotic-enriched environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"22 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145433822","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}
Silvia Abbà,Liam D Adair,Francesca Barbero,Luca P Casacci,Iljia Dukovski,Francisca Font,Tom Hawtrey,Elizabeth J New,Jukkrit Nootem,Pramsak Patawanich,Lukas Patten,Marco Polin,Daniel Segrè,Nian Kee Tan,Irene Stefanini
Saccharomyces cerevisiae relies on social wasps (e.g., Vespa crabro, Polistes spp.) for dispersal and genetic mixing. Unlike most natural environments, wasp intestines provide conditions that support yeast survival, sporulation, spore germination, and mating. This study explores the mechanisms at the basis of this process by examining the wasp gut environment and yeast responses. Molecular analyses based on yeast deletion collection and transcriptomics showed that yeast sporulates in the crop, spores germinate in the gut, and cells ferment in the gut. The crop and gut differ chemically: the gut has more sugars, a higher pH, and (in workers) greater viscosity. In vitro tests confirmed yeast survival in both environments, with faster germination in gut-like conditions. Computational models based on these physicochemical traits matched the experimental results. The data obtained provide fundamental insights into yeast progression towards mating within wasps' intestines and suggest a possible relation between yeast alcoholic fermentation and wasps' alcohol tolerance, thereby enhancing our understanding of the S. cerevisiae-social wasp association.
{"title":"Wasp intestinal cues drive yeast toward outbreeding strategies.","authors":"Silvia Abbà,Liam D Adair,Francesca Barbero,Luca P Casacci,Iljia Dukovski,Francisca Font,Tom Hawtrey,Elizabeth J New,Jukkrit Nootem,Pramsak Patawanich,Lukas Patten,Marco Polin,Daniel Segrè,Nian Kee Tan,Irene Stefanini","doi":"10.1093/ismejo/wraf243","DOIUrl":"https://doi.org/10.1093/ismejo/wraf243","url":null,"abstract":"Saccharomyces cerevisiae relies on social wasps (e.g., Vespa crabro, Polistes spp.) for dispersal and genetic mixing. Unlike most natural environments, wasp intestines provide conditions that support yeast survival, sporulation, spore germination, and mating. This study explores the mechanisms at the basis of this process by examining the wasp gut environment and yeast responses. Molecular analyses based on yeast deletion collection and transcriptomics showed that yeast sporulates in the crop, spores germinate in the gut, and cells ferment in the gut. The crop and gut differ chemically: the gut has more sugars, a higher pH, and (in workers) greater viscosity. In vitro tests confirmed yeast survival in both environments, with faster germination in gut-like conditions. Computational models based on these physicochemical traits matched the experimental results. The data obtained provide fundamental insights into yeast progression towards mating within wasps' intestines and suggest a possible relation between yeast alcoholic fermentation and wasps' alcohol tolerance, thereby enhancing our understanding of the S. cerevisiae-social wasp association.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145411535","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}
Sai Yang,Jiawei Zhang,Yafei Ou,Wenxiao Liu,Xinru Tian,Li-Jun Hou,Hong-Po Dong
Aerobic methanotrophs encode a hydroxylamine oxidoreductase, which facilitates the oxidation of ammonia to nitrite or nitric oxide, potentially leading to nitrous oxide production. Aerobic methane oxidation has been documented in shallow marine waters or the water column of the open ocean. However, little is known about the distribution pattern of marine aerobic methanotrophs containing hydroxylamine oxidoreductase and their contribution to marine nitrous oxide emissions. Here, by analyzing global marine metagenomes, we show that hydroxylamine oxidoreductase-containing aerobic methanotrophs were widely distributed across diverse marine habitats, with higher abundances in methane seep systems and estuary regions than in other environments. Among these, aerobic methanotrophs belonging to Gammaproteobacteria were the most widely distributed and abundant functional group. We also identified a second order within Gammaproteobacteria (Ga0077536) potentially capable of aerobic methanotrophy, and a complete repertoire of denitrification genes in a gammaproteobacterial methanotroph, expanding the phylogenetic and functional diversity of marine aerobic methanotrophs. By using enrichments of estuarine methanotrophs in combination with 15N stable isotope tracing and metatranscriptomic analysis, we indicate that marine aerobic methanotrophs take part in ammonia oxidation and nitrous oxide production. The ammonia oxidation can persist for approximately 6 days, and the nitrous oxide produced is at least partially derived from the hydroxylamine oxidation. Given the prevalence of denitrification genes in aerobic methanotrophs, methane oxidation may also be coupled to NOx- reduction under anoxic marine conditions, potentially contributing to nitrous oxide production. The intrinsic nature of aerobic methanotrophs could partially offset the mitigation of global warming achieved through the methane consumption.
{"title":"Ammonia oxidation by aerobic methanotrophs as a source of marine nitrous oxide.","authors":"Sai Yang,Jiawei Zhang,Yafei Ou,Wenxiao Liu,Xinru Tian,Li-Jun Hou,Hong-Po Dong","doi":"10.1093/ismejo/wraf242","DOIUrl":"https://doi.org/10.1093/ismejo/wraf242","url":null,"abstract":"Aerobic methanotrophs encode a hydroxylamine oxidoreductase, which facilitates the oxidation of ammonia to nitrite or nitric oxide, potentially leading to nitrous oxide production. Aerobic methane oxidation has been documented in shallow marine waters or the water column of the open ocean. However, little is known about the distribution pattern of marine aerobic methanotrophs containing hydroxylamine oxidoreductase and their contribution to marine nitrous oxide emissions. Here, by analyzing global marine metagenomes, we show that hydroxylamine oxidoreductase-containing aerobic methanotrophs were widely distributed across diverse marine habitats, with higher abundances in methane seep systems and estuary regions than in other environments. Among these, aerobic methanotrophs belonging to Gammaproteobacteria were the most widely distributed and abundant functional group. We also identified a second order within Gammaproteobacteria (Ga0077536) potentially capable of aerobic methanotrophy, and a complete repertoire of denitrification genes in a gammaproteobacterial methanotroph, expanding the phylogenetic and functional diversity of marine aerobic methanotrophs. By using enrichments of estuarine methanotrophs in combination with 15N stable isotope tracing and metatranscriptomic analysis, we indicate that marine aerobic methanotrophs take part in ammonia oxidation and nitrous oxide production. The ammonia oxidation can persist for approximately 6 days, and the nitrous oxide produced is at least partially derived from the hydroxylamine oxidation. Given the prevalence of denitrification genes in aerobic methanotrophs, methane oxidation may also be coupled to NOx- reduction under anoxic marine conditions, potentially contributing to nitrous oxide production. The intrinsic nature of aerobic methanotrophs could partially offset the mitigation of global warming achieved through the methane consumption.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"82 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145411462","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}
Yunhua Zhang,Wujia Mo,Keyi Chen,Yichen Ding,Kaikai Mao,Hu Wan,Jizhong Zhou,Feng Ju
The fall armyworm, Spodoptera frugiperda, is a major global agricultural pest, known for its rapid evolution of insecticide resistance. Although host genetic adaptation contributes to this trait, the role of gut symbiont-mediated metabolic pathways in promoting resistance remains poorly understood. Here, we show that besides direct biodegradation, a generalist symbiont Enterococcus casseliflavus EMBL-3 indirectly promotes chlorantraniliprole resistance by compensating for tryptophan deficiency in a maize-based diet. Metabolomics and isotope tracing identify EMBL-3 as the primary producer of tryptophan, which is subsequently converted by co-resident microbes to indoleacetic acid. Indoleacetic acid activates the aryl hydrocarbon receptor, leading to upregulation of UDP-glucuronosyltransferase, a detoxification enzyme essential for chlorantraniliprole resistance, as confirmed by CRISPR/Cas9 knockout. This tripartite EMBL-3-indoleacetic acid-UDP-glucuronosyltransferase axis defines a hierarchical symbiont-host metabolic network driving chlorantraniliprole resistance. Our findings provide a framework and targets for disrupting pest adaptability by targeting critical symbiont metabolic nodes, positioning microbiome-mediated detoxification as a universal vulnerability in resistant pests.
{"title":"Cooperative Microbial Metabolism Enhances Tryptophan-Mediated Insecticide Detoxification in the Fall Armyworm.","authors":"Yunhua Zhang,Wujia Mo,Keyi Chen,Yichen Ding,Kaikai Mao,Hu Wan,Jizhong Zhou,Feng Ju","doi":"10.1093/ismejo/wraf237","DOIUrl":"https://doi.org/10.1093/ismejo/wraf237","url":null,"abstract":"The fall armyworm, Spodoptera frugiperda, is a major global agricultural pest, known for its rapid evolution of insecticide resistance. Although host genetic adaptation contributes to this trait, the role of gut symbiont-mediated metabolic pathways in promoting resistance remains poorly understood. Here, we show that besides direct biodegradation, a generalist symbiont Enterococcus casseliflavus EMBL-3 indirectly promotes chlorantraniliprole resistance by compensating for tryptophan deficiency in a maize-based diet. Metabolomics and isotope tracing identify EMBL-3 as the primary producer of tryptophan, which is subsequently converted by co-resident microbes to indoleacetic acid. Indoleacetic acid activates the aryl hydrocarbon receptor, leading to upregulation of UDP-glucuronosyltransferase, a detoxification enzyme essential for chlorantraniliprole resistance, as confirmed by CRISPR/Cas9 knockout. This tripartite EMBL-3-indoleacetic acid-UDP-glucuronosyltransferase axis defines a hierarchical symbiont-host metabolic network driving chlorantraniliprole resistance. Our findings provide a framework and targets for disrupting pest adaptability by targeting critical symbiont metabolic nodes, positioning microbiome-mediated detoxification as a universal vulnerability in resistant pests.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"33 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145351794","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 functions of microbial communities, including substrate conversion and pathogen suppression, arise not as a simple sum of individual species' capabilities but through complex interspecies interactions. Understanding how such functions arise from individual species and their interactions remains a major challenge, limiting efforts to rationally understand microbial roles in both natural and engineered ecosystems. Because current holistic (meta-omics) and reductionist (isolation- or single-cell-based) approaches struggle to capture these emergent microbial community functions, this study explores an intermediate strategy: analyzing simple sub-community combinations to enable a bottom-up understanding of community-level functions. To examine the validity of this approach, we used a nine-member synthetic microbial community capable of degrading the environmental pollutant aniline, and systematically generated a dataset of 256 sub-community combinations and their associated functions. Analyses using random forest models revealed that the sub-community combinations of just three to four species enabled the quantitative prediction of functions in larger communities (5-9-member; Pearson's r = 0.78-0.80). Prediction performance remained robust even with limited sub-community data, suggesting applicability to more diverse microbial communities where exhaustive sub-community observation is infeasible. Moreover, interpreting models trained on these simple sub-community combinations enabled the identification of key species and interspecies interactions that strongly influence the overall community function. These findings provide a methodological framework for mechanistically dissecting complex microbial community functions through sub-community-based analysis.
微生物群落的功能，包括底物转化和病原体抑制，不是单个物种能力的简单总和，而是通过复杂的物种间相互作用产生的。了解这些功能是如何从单个物种及其相互作用中产生的仍然是一个重大挑战，限制了合理理解微生物在自然和工程生态系统中的作用。由于目前的整体（元组学）和还原论（基于分离或单细胞的）方法难以捕捉这些新兴的微生物群落功能，本研究探索了一种中间策略：分析简单的亚群落组合，从而能够自下而上地理解群落水平的功能。为了验证该方法的有效性，我们使用了一个能够降解环境污染物苯胺的9个合成微生物群落，并系统地生成了包含256个亚群落组合及其相关功能的数据集。随机森林模型分析表明，仅3 - 4个物种的亚群落组合就可以定量预测更大群落（5-9个成员；Pearson’s r = 0.78-0.80）的功能。即使在有限的亚群落数据下，预测效果仍然很好，这表明在无法进行详尽的亚群落观察的情况下，预测结果适用于更多样化的微生物群落。此外，根据这些简单的亚群落组合训练的解释模型能够识别出对整个群落功能产生强烈影响的关键物种和种间相互作用。这些发现为通过亚社区分析机制剖析复杂微生物群落功能提供了一个方法学框架。
{"title":"Decoding emergent properties of microbial community functions through sub-community observations and interpretable machine learning.","authors":"Hidehiro Ishizawa,Sunao Noguchi,Miku Kito,Yui Nomura,Kodai Kimura,Masahiro Takeo","doi":"10.1093/ismejo/wraf236","DOIUrl":"https://doi.org/10.1093/ismejo/wraf236","url":null,"abstract":"The functions of microbial communities, including substrate conversion and pathogen suppression, arise not as a simple sum of individual species' capabilities but through complex interspecies interactions. Understanding how such functions arise from individual species and their interactions remains a major challenge, limiting efforts to rationally understand microbial roles in both natural and engineered ecosystems. Because current holistic (meta-omics) and reductionist (isolation- or single-cell-based) approaches struggle to capture these emergent microbial community functions, this study explores an intermediate strategy: analyzing simple sub-community combinations to enable a bottom-up understanding of community-level functions. To examine the validity of this approach, we used a nine-member synthetic microbial community capable of degrading the environmental pollutant aniline, and systematically generated a dataset of 256 sub-community combinations and their associated functions. Analyses using random forest models revealed that the sub-community combinations of just three to four species enabled the quantitative prediction of functions in larger communities (5-9-member; Pearson's r = 0.78-0.80). Prediction performance remained robust even with limited sub-community data, suggesting applicability to more diverse microbial communities where exhaustive sub-community observation is infeasible. Moreover, interpreting models trained on these simple sub-community combinations enabled the identification of key species and interspecies interactions that strongly influence the overall community function. These findings provide a methodological framework for mechanistically dissecting complex microbial community functions through sub-community-based analysis.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"52 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145339098","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}
Coronary artery disease remains the leading cause of mortality and morbidity globally. The gut microbiota has been implicated in the development of coronary artery disease through unclear mechanisms. Here, we demonstrate that the abundance and inter-species interactions of Olsenella scatoligenes are 4.7-fold and 1.6-fold higher in patients with coronary artery disease, respectively, and positively associated with disease severity. Furthermore, integrative metagenomic and metabolomic analyses identify skatole as the key microbial effector mediating the pro-atherogenic effect of Olsenella scatoligenes. Consistently, supplementation with Olsenella scatoligenes or skatole results in 1.26- and 1.23-fold increases in aortic plaque area, respectively, by promoting vascular smooth muscle cell proliferation and migration to the intima. Mechanistically, Olsenella scatoligenes -derived skatole facilitates nuclear translocation of the aryl hydrocarbon receptor, and enhances its binding to the promoter region of calponin 1. Silencing either aryl hydrocarbon receptor or calponin 1 attenuates approximately 40% of the vascular smooth muscle cell proliferation and migration induced by skatole. Collectively, our study identifies increased skatole production as the principal microbial effector linking Olsenella scatoligenes to aggravated atherosclerosis through activation of aryl hydrocarbon receptor -calponin 1 axis and underscores the therapeutic potential of targeting skatole production for the management of coronary artery disease.
{"title":"Olsenella scatoligenes-derived Skatole Promotes Smooth Muscle Cell Proliferation and Migration to Aggravate Atherosclerosis.","authors":"Yawen Zhao,Jiarui Chen,Shanshan Zhu,Yingxi Xu,Jiangyuan Zhu,Jialu Yang,Weibin Zhou,Ying Yang,Maohuan Lin,Qian Chen,Min Xia,Yangxin Chen,Yan Liu","doi":"10.1093/ismejo/wraf238","DOIUrl":"https://doi.org/10.1093/ismejo/wraf238","url":null,"abstract":"Coronary artery disease remains the leading cause of mortality and morbidity globally. The gut microbiota has been implicated in the development of coronary artery disease through unclear mechanisms. Here, we demonstrate that the abundance and inter-species interactions of Olsenella scatoligenes are 4.7-fold and 1.6-fold higher in patients with coronary artery disease, respectively, and positively associated with disease severity. Furthermore, integrative metagenomic and metabolomic analyses identify skatole as the key microbial effector mediating the pro-atherogenic effect of Olsenella scatoligenes. Consistently, supplementation with Olsenella scatoligenes or skatole results in 1.26- and 1.23-fold increases in aortic plaque area, respectively, by promoting vascular smooth muscle cell proliferation and migration to the intima. Mechanistically, Olsenella scatoligenes -derived skatole facilitates nuclear translocation of the aryl hydrocarbon receptor, and enhances its binding to the promoter region of calponin 1. Silencing either aryl hydrocarbon receptor or calponin 1 attenuates approximately 40% of the vascular smooth muscle cell proliferation and migration induced by skatole. Collectively, our study identifies increased skatole production as the principal microbial effector linking Olsenella scatoligenes to aggravated atherosclerosis through activation of aryl hydrocarbon receptor -calponin 1 axis and underscores the therapeutic potential of targeting skatole production for the management of coronary artery disease.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"2 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145339094","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}
Yu Lei,Yangqing Wang,Xiaojuan Tan,Chuanwu Xi,Hong Liu
Bioconversion of ammonium to dinitrogen (N2) is an essential process in the nitrogen cycle, primarily driven by O2-dependent nitrification and followed by O2-limited denitrification, involving multiple redox states of nitrogen (NH4+ → NH2OH → NO2- → NO3- → NO2- → NO→N2O → N2). Here we discovered a new process termed acetone-mediated ammonium oxidation (AMAO) in Zobellella taiwanensis bacteria under both oxic and anoxic conditions, directly oxidizing ammonium to N2 (NH4+ + acetone → acetoxime → N2 + acetone). Acetone, produced from organic sources, couples with ammonium to form acetoxime in the presence of O2, NO2-, NO3-, or Fe(III). Subsequently, acetoxime is oxidized to N2, thereby releasing recyclable acetone. We purified two new enzymes (acetoxime synthase, AOS; acetoxime dehydrogenase, AOH) catalyzing this process and identified their corresponding genes. The widespread distribution of homologous amino acid sequences across thousands of prokaryotic and eukaryotic microorganisms suggests the potential ubiquity of this process in nature and its possible substantial contributions to the nitrogen cycle.
{"title":"Acetone-mediated ammonium oxidation to dinitrogen by Zobellella taiwanensis bacteria.","authors":"Yu Lei,Yangqing Wang,Xiaojuan Tan,Chuanwu Xi,Hong Liu","doi":"10.1093/ismejo/wraf230","DOIUrl":"https://doi.org/10.1093/ismejo/wraf230","url":null,"abstract":"Bioconversion of ammonium to dinitrogen (N2) is an essential process in the nitrogen cycle, primarily driven by O2-dependent nitrification and followed by O2-limited denitrification, involving multiple redox states of nitrogen (NH4+ → NH2OH → NO2- → NO3- → NO2- → NO→N2O → N2). Here we discovered a new process termed acetone-mediated ammonium oxidation (AMAO) in Zobellella taiwanensis bacteria under both oxic and anoxic conditions, directly oxidizing ammonium to N2 (NH4+ + acetone → acetoxime → N2 + acetone). Acetone, produced from organic sources, couples with ammonium to form acetoxime in the presence of O2, NO2-, NO3-, or Fe(III). Subsequently, acetoxime is oxidized to N2, thereby releasing recyclable acetone. We purified two new enzymes (acetoxime synthase, AOS; acetoxime dehydrogenase, AOH) catalyzing this process and identified their corresponding genes. The widespread distribution of homologous amino acid sequences across thousands of prokaryotic and eukaryotic microorganisms suggests the potential ubiquity of this process in nature and its possible substantial contributions to the nitrogen cycle.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"17 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145338703","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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