Shan Li, Jiajia Liu, Lei Su, Jingwen Qiu, Lianbing Lin, Ákos T Kovács, Yicen Lin
Polyethylene, one of the most widely used synthetic polymers, presents significant environmental challenges due to its resistance to biodegradation. Its surface offers a unique ecological niche for microbial colonization and serves as a primary habitat for degrading microorganisms. Despite the pivotal role microbial communities play in plastic degradation, there has been limited research on constructing stable, interacting microbial consortia. In this study, we explored the potential of evolving bacterial biofilm communities to enhance polyethylene degradation. Through long-term experimental evolution, six microbial populations underwent 40 selection cycles using polyethylene as their sole carbon source. The resulting evolved communities formed robust, multi-species biofilms with enhanced degradation capabilities, outperforming their ancestral populations in biofilm production. Stutzerimonas stutzeri emerged as the dominant species, orchestrating a synergistic interaction with two other isolates through metabolic division of labor. (Meta)-transcriptomics analysis revealed that Stutzerimonas primarily contributed to the expression of enzymes involved in microbe-mediated degradation of polyethylene, whereas the other community members were responsible for secreting extracellular polysaccharides, improving biofilm formation. This study highlights the potential of experimentally evolved microbial consortia to synergistically accelerate plastic biodegradation, offering promising strategies for environmental bioremediation.
{"title":"Synergistic biodegradation of polyethylene by experimentally evolved bacterial biofilms","authors":"Shan Li, Jiajia Liu, Lei Su, Jingwen Qiu, Lianbing Lin, Ákos T Kovács, Yicen Lin","doi":"10.1093/ismejo/wraf223","DOIUrl":"https://doi.org/10.1093/ismejo/wraf223","url":null,"abstract":"Polyethylene, one of the most widely used synthetic polymers, presents significant environmental challenges due to its resistance to biodegradation. Its surface offers a unique ecological niche for microbial colonization and serves as a primary habitat for degrading microorganisms. Despite the pivotal role microbial communities play in plastic degradation, there has been limited research on constructing stable, interacting microbial consortia. In this study, we explored the potential of evolving bacterial biofilm communities to enhance polyethylene degradation. Through long-term experimental evolution, six microbial populations underwent 40 selection cycles using polyethylene as their sole carbon source. The resulting evolved communities formed robust, multi-species biofilms with enhanced degradation capabilities, outperforming their ancestral populations in biofilm production. Stutzerimonas stutzeri emerged as the dominant species, orchestrating a synergistic interaction with two other isolates through metabolic division of labor. (Meta)-transcriptomics analysis revealed that Stutzerimonas primarily contributed to the expression of enzymes involved in microbe-mediated degradation of polyethylene, whereas the other community members were responsible for secreting extracellular polysaccharides, improving biofilm formation. This study highlights the potential of experimentally evolved microbial consortia to synergistically accelerate plastic biodegradation, offering promising strategies for environmental bioremediation.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"82 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145247046","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}
Joanna A Lepper,H B Beryl Rappaport,Angela M Oliverio
Although microbial eukaryotes comprise the majority of eukaryotic phylogenetic diversity and inhabit nearly all ecosystems globally, most research focuses on only a few species of human parasites. Here, we quantify the extent of research on known microbial eukaryotic species. Nearly half of the mentions of protist species on publications in PubMed referenced only 10 species included in the Protist Ribosomal Reference (PR2) Database. Likewise, although most samples in the PR2 database are free-living protists from aquatic environments, 12 species of human parasites comprise 47% of the literature. Research efforts that focus on only a handful of eukaryotic lineages severely limit our understanding of the fundamental biology of eukaryotic cells. We highlight recent efforts to characterize novel eukaryotic lineages that have resulted in a new understanding of the rules of life and identify key lineages that are notably absent or limited in the literature, despite their abundance and significance across global ecosystems.
{"title":"Half of microbial eukaryote literature focuses on only twelve human parasites.","authors":"Joanna A Lepper,H B Beryl Rappaport,Angela M Oliverio","doi":"10.1093/ismejo/wraf219","DOIUrl":"https://doi.org/10.1093/ismejo/wraf219","url":null,"abstract":"Although microbial eukaryotes comprise the majority of eukaryotic phylogenetic diversity and inhabit nearly all ecosystems globally, most research focuses on only a few species of human parasites. Here, we quantify the extent of research on known microbial eukaryotic species. Nearly half of the mentions of protist species on publications in PubMed referenced only 10 species included in the Protist Ribosomal Reference (PR2) Database. Likewise, although most samples in the PR2 database are free-living protists from aquatic environments, 12 species of human parasites comprise 47% of the literature. Research efforts that focus on only a handful of eukaryotic lineages severely limit our understanding of the fundamental biology of eukaryotic cells. We highlight recent efforts to characterize novel eukaryotic lineages that have resulted in a new understanding of the rules of life and identify key lineages that are notably absent or limited in the literature, despite their abundance and significance across global ecosystems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"348 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145235980","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}
Quorum sensing (QS) is a chemical communication process that connects microbial members in various microbial systems. Bacterial communication networks mediated by QS play important roles in the regulation of intestinal microecological balance as well as nutrition and metabolism of the host. However, how human gut microbes utilize QS signals to communicate with one another remains largely unknown. In this study, we first examined the prevalence and abundance of genes encoding QS signal synthases in 3329 species representatives clustered from 289232 prokaryotic genomes in the Unified Human Gastrointestinal Genome collection. Our results show autoinducer-2 (AI-2) is the most prevalent QS signal within the human gut microbiota, with the synthase gene luxS being found in 2039 species mainly distributed within Firmicutes, Actinobacteriota, Bacteroidota, and Proteobacteria. Furthermore, 299 species carry genes encoding one or more types of AI-2 receptors (LuxP-, LsrB-, dCache_1-, and GAPES1-type). The dCache_1- and GAPES1-type receptors can function as methyl-accepting chemotaxis proteins, histidine kinases, c-di-GMP synthases and/or c-di-GMP-specific phosphodiesterases, serine phosphatases, and serine/threonine kinases, suggesting the diversity of AI-2-mediated interspecies communication modes among human gut microbiota. Metatranscriptomic analysis showed that a number of AI-2 synthase- and receptor-encoding genes can be expressed in the human gut in healthy and/or unhealthy states. The communication network analysis suggests that AI-2-mediated interactions widely occur among members of Firmicutes, Proteobacteria, Actinobacteriota, Campylobacterota, and Spirochaetota. Overall, this study deepens understanding of QS-mediated communication network among human gut microbiota, and provides guidance for engineering gut microbiota and constructing new synthetic microbial consortia based on complex microbial interactions.
{"title":"Autoinducer-2-mediated communication network within human gut microbiota","authors":"Qingying Fan, Hengxi Sun, Xueyuan Lin, Wenguang Yang, Xihui Shen, Lei Zhang","doi":"10.1093/ismejo/wraf204","DOIUrl":"https://doi.org/10.1093/ismejo/wraf204","url":null,"abstract":"Quorum sensing (QS) is a chemical communication process that connects microbial members in various microbial systems. Bacterial communication networks mediated by QS play important roles in the regulation of intestinal microecological balance as well as nutrition and metabolism of the host. However, how human gut microbes utilize QS signals to communicate with one another remains largely unknown. In this study, we first examined the prevalence and abundance of genes encoding QS signal synthases in 3329 species representatives clustered from 289232 prokaryotic genomes in the Unified Human Gastrointestinal Genome collection. Our results show autoinducer-2 (AI-2) is the most prevalent QS signal within the human gut microbiota, with the synthase gene luxS being found in 2039 species mainly distributed within Firmicutes, Actinobacteriota, Bacteroidota, and Proteobacteria. Furthermore, 299 species carry genes encoding one or more types of AI-2 receptors (LuxP-, LsrB-, dCache_1-, and GAPES1-type). The dCache_1- and GAPES1-type receptors can function as methyl-accepting chemotaxis proteins, histidine kinases, c-di-GMP synthases and/or c-di-GMP-specific phosphodiesterases, serine phosphatases, and serine/threonine kinases, suggesting the diversity of AI-2-mediated interspecies communication modes among human gut microbiota. Metatranscriptomic analysis showed that a number of AI-2 synthase- and receptor-encoding genes can be expressed in the human gut in healthy and/or unhealthy states. The communication network analysis suggests that AI-2-mediated interactions widely occur among members of Firmicutes, Proteobacteria, Actinobacteriota, Campylobacterota, and Spirochaetota. Overall, this study deepens understanding of QS-mediated communication network among human gut microbiota, and provides guidance for engineering gut microbiota and constructing new synthetic microbial consortia based on complex microbial interactions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"9 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145241900","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}
Coastal bacteria play an important role in the conversion of terrestrial organic carbon (TerrOC). However, their ecological patterns and drivers remains elusive. Here, 180 bacterial communities from 10 regions along the Chinese coastline, covering an 18,000 km transect between 18.27 °N and 39.82 °N, were cultured under three typical lignocellulosic substrates, hardwood (aspen), softwood (pine), and herbaceous (rice straw), respectively. All the consortia showed a broad spectrum of TerrOC utilization, and displayed degradation capacities comparable with those previously established though preliminary in situ lignocellulose enrichment. Moreover, following the metabolic theory of ecology, annual average temperature of the sites stimulated community metabolism, even though all were cultured at 30°C. Consortia enriched on aspen exhibited the highest temperature sensitivity. 16S rRNA gene amplicon and metatranscriptomic sequencing analyses revealed temperature-dependent latitudinal diversity gradients, displaying a trend that was opposite of the temperature-diversity positive relationship observed in terrestrial lignin-degrading microbes. The community composition shifted to adapt to rising environmental temperature. To enhance lignin degradation, aspen consortia from high annual average temperature employed metabolic generalists, which induced expression of dypB centered gene families for lignin depolymerization and versatile pathways for degradation of lignin derivates. This study reveals the intrinsic drivers for coastal cultured lignocellulose degrading bacterial communities from an ecological perspective and deepens our understanding of the metabolic mechanisms in coastal TerrOC conversion.
{"title":"Temperature mediates biodiversity and metabolism of culturable lignocellulose-degrading consortia from intertidal wetlands.","authors":"Jiyu Chen,Min Yang,Qichao Tu,Lu Lin","doi":"10.1093/ismejo/wraf218","DOIUrl":"https://doi.org/10.1093/ismejo/wraf218","url":null,"abstract":"Coastal bacteria play an important role in the conversion of terrestrial organic carbon (TerrOC). However, their ecological patterns and drivers remains elusive. Here, 180 bacterial communities from 10 regions along the Chinese coastline, covering an 18,000 km transect between 18.27 °N and 39.82 °N, were cultured under three typical lignocellulosic substrates, hardwood (aspen), softwood (pine), and herbaceous (rice straw), respectively. All the consortia showed a broad spectrum of TerrOC utilization, and displayed degradation capacities comparable with those previously established though preliminary in situ lignocellulose enrichment. Moreover, following the metabolic theory of ecology, annual average temperature of the sites stimulated community metabolism, even though all were cultured at 30°C. Consortia enriched on aspen exhibited the highest temperature sensitivity. 16S rRNA gene amplicon and metatranscriptomic sequencing analyses revealed temperature-dependent latitudinal diversity gradients, displaying a trend that was opposite of the temperature-diversity positive relationship observed in terrestrial lignin-degrading microbes. The community composition shifted to adapt to rising environmental temperature. To enhance lignin degradation, aspen consortia from high annual average temperature employed metabolic generalists, which induced expression of dypB centered gene families for lignin depolymerization and versatile pathways for degradation of lignin derivates. This study reveals the intrinsic drivers for coastal cultured lignocellulose degrading bacterial communities from an ecological perspective and deepens our understanding of the metabolic mechanisms in coastal TerrOC conversion.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"97 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145215840","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}
Shamik Roy, Marc G Dumont, James A Bradley, Marcela Hernández
Anthropogenic activities are impacting the environment in ways that may intersect and have compounding effects. In soil, the spread of antibiotics and resistant microbes, and thereby antimicrobial resistance (AMR), can accelerate because of climate change and anthropogenic activities. Here we propose that the dual production and release of antimicrobial compounds to the environment, and the increase in global temperatures as a consequence of climate change, will have synergistic effects leading to both enhanced climate change and disease risk. We predict that an increase in AMR will reduce microbial carbon use efficiency (CUE) because interactions among microbes will lead to the allocation of available resources towards AMR and metabolism instead of growth. This reduction in CUE may lead to increased greenhouse gas release; however, the extent to which AMR can affect the stability of soil carbon by altering microbial CUE remains unknown. This concern is especially pertinent in the Arctic, which is warming faster than anywhere else on Earth and contains substantial soil carbon reservoirs.
{"title":"Microbial interactions between climate warming and antimicrobial resistance threaten soil carbon storage and global health","authors":"Shamik Roy, Marc G Dumont, James A Bradley, Marcela Hernández","doi":"10.1093/ismejo/wraf220","DOIUrl":"https://doi.org/10.1093/ismejo/wraf220","url":null,"abstract":"Anthropogenic activities are impacting the environment in ways that may intersect and have compounding effects. In soil, the spread of antibiotics and resistant microbes, and thereby antimicrobial resistance (AMR), can accelerate because of climate change and anthropogenic activities. Here we propose that the dual production and release of antimicrobial compounds to the environment, and the increase in global temperatures as a consequence of climate change, will have synergistic effects leading to both enhanced climate change and disease risk. We predict that an increase in AMR will reduce microbial carbon use efficiency (CUE) because interactions among microbes will lead to the allocation of available resources towards AMR and metabolism instead of growth. This reduction in CUE may lead to increased greenhouse gas release; however, the extent to which AMR can affect the stability of soil carbon by altering microbial CUE remains unknown. This concern is especially pertinent in the Arctic, which is warming faster than anywhere else on Earth and contains substantial soil carbon reservoirs.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"157 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145215657","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 gut microbiota represents a critical yet underexplored "second genome" in the host that functions as a key driver of pollutant transformation across Earth's ecosystems. This review synthesizes current understanding of over 490 pollutants across a wide range of species, highlighting the universal role of gut microbial communities in modifying pollutant exposure. We demonstrated that gut microbial communities transform a broad spectrum of environmental pollutants through evolutionarily conserved pathways, fundamentally altering their bioavailability, fate and toxicity potential within the host. Transformation reactions are elucidated with connections among the metabolic enzymes that are developed by specific gut microbes, emphasizing the markedly specific and complementary signatures of microbial biotransformation compared with the host process. By integrating multidisciplinary studies, the complex and dynamic interplay between the gut microbiota, host physiology, and environmental pollutants have been elucidated, and the drivers involved in the biotransformation processes have been proposed. Furthermore, current methodologies are critically evaluated and next-generation approaches to reveal the underlying mechanisms of gut microbiota-driven pollutant transformation are outlined. This review underscores the urgent need to systematize research on "pollutant-gut microbiota-host" interactions and advocates the integration of gut microbial perspectives into interdisciplinary research paradigms of toxicology, microbiology, and ecology.
{"title":"Deciphering the Universal Role of Gut Microbiota in Pollutant Transformation.","authors":"Rui Hou,Xiaowei Jin,Jingchun Feng,Jingchuan Xue,Chengzhi Chen,Yuanqiang Zou,Xiangrong Xu,Kefu Yu,Pei-Yuan Qian,Wei Zhang,Jizhong Zhou,Si Zhang,Zhifeng Yang","doi":"10.1093/ismejo/wraf215","DOIUrl":"https://doi.org/10.1093/ismejo/wraf215","url":null,"abstract":"The gut microbiota represents a critical yet underexplored \"second genome\" in the host that functions as a key driver of pollutant transformation across Earth's ecosystems. This review synthesizes current understanding of over 490 pollutants across a wide range of species, highlighting the universal role of gut microbial communities in modifying pollutant exposure. We demonstrated that gut microbial communities transform a broad spectrum of environmental pollutants through evolutionarily conserved pathways, fundamentally altering their bioavailability, fate and toxicity potential within the host. Transformation reactions are elucidated with connections among the metabolic enzymes that are developed by specific gut microbes, emphasizing the markedly specific and complementary signatures of microbial biotransformation compared with the host process. By integrating multidisciplinary studies, the complex and dynamic interplay between the gut microbiota, host physiology, and environmental pollutants have been elucidated, and the drivers involved in the biotransformation processes have been proposed. Furthermore, current methodologies are critically evaluated and next-generation approaches to reveal the underlying mechanisms of gut microbiota-driven pollutant transformation are outlined. This review underscores the urgent need to systematize research on \"pollutant-gut microbiota-host\" interactions and advocates the integration of gut microbial perspectives into interdisciplinary research paradigms of toxicology, microbiology, and ecology.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"68 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145188961","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}
Learning about the metabolic activities and adaptations of deep-sea microbes is challenging, as sample collection and retrieval often cause RNA degradation and microbial community shifts. Here, we employed an in situ DNA/RNA co-extraction device to collect 18 time-series nucleic acid samples during winter and summer in the South China Sea, minimizing sampling perturbation for metatranscriptome and metagenome analyses. Between the two seasons, the prokaryotic microbiota showed seasonal variations in species composition. Burkholderiales dominated in summer, whereas Pseudomonadales, Bacillales, and Rhodobacterales were enriched in winter. However, the dominant transcriptionally active taxa affiliated with Nitrososphaerales, MGIII, SAR324, UBA11654, Marinisomatales and Poseidoniales remained largely stable across seasons. Among eukaryotes, Ciliophora were the most active, whereas Retaria were abundant but inactive. Despite the stable active prokaryotic community, metabolic profiles differed significantly between seasons. In the winter, autotrophic microorganisms, particularly Nitrososphaerales, exhibited higher CO2 fixation activity via the 3HP/4HB cycle, accompanied by enhanced ammonia oxidation for energy generation. In addition, CO oxidation activity was also elevated. In the summer, the primary source of energy originated from heterotrophic microorganisms capable of utilizing fatty acids, benzoate, and H2, likely relying on anaerobic respiration within organic particles. This may relate with nutrient source variations as reflected by the different levels of microbial network complexity between two seasons. Altogether, our in situ metatranscriptomes revealed the metabolic activities and adaptations of active microbial groups across seasons, providing a basis for identifying the microbial contributors to elemental cycles in the deep ocean.
{"title":"Seasonal variability in community structure and metabolism of active deep-sea microorganisms.","authors":"Yinghui He,Federico Baltar,Yong Wang","doi":"10.1093/ismejo/wraf214","DOIUrl":"https://doi.org/10.1093/ismejo/wraf214","url":null,"abstract":"Learning about the metabolic activities and adaptations of deep-sea microbes is challenging, as sample collection and retrieval often cause RNA degradation and microbial community shifts. Here, we employed an in situ DNA/RNA co-extraction device to collect 18 time-series nucleic acid samples during winter and summer in the South China Sea, minimizing sampling perturbation for metatranscriptome and metagenome analyses. Between the two seasons, the prokaryotic microbiota showed seasonal variations in species composition. Burkholderiales dominated in summer, whereas Pseudomonadales, Bacillales, and Rhodobacterales were enriched in winter. However, the dominant transcriptionally active taxa affiliated with Nitrososphaerales, MGIII, SAR324, UBA11654, Marinisomatales and Poseidoniales remained largely stable across seasons. Among eukaryotes, Ciliophora were the most active, whereas Retaria were abundant but inactive. Despite the stable active prokaryotic community, metabolic profiles differed significantly between seasons. In the winter, autotrophic microorganisms, particularly Nitrososphaerales, exhibited higher CO2 fixation activity via the 3HP/4HB cycle, accompanied by enhanced ammonia oxidation for energy generation. In addition, CO oxidation activity was also elevated. In the summer, the primary source of energy originated from heterotrophic microorganisms capable of utilizing fatty acids, benzoate, and H2, likely relying on anaerobic respiration within organic particles. This may relate with nutrient source variations as reflected by the different levels of microbial network complexity between two seasons. Altogether, our in situ metatranscriptomes revealed the metabolic activities and adaptations of active microbial groups across seasons, providing a basis for identifying the microbial contributors to elemental cycles in the deep ocean.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"41 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145117072","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}
Junwei Peng,Dmitri V Mavrodi,Jiasui Li,Suhelen Egan,Huanhuan Zhang,Xiuli Fan,Yang Liu,Keke Dang,Olga V Mavrodi,Qin Liu,Yuanhua Dong,Jiangang Li
Harnessing antibiotic-producing microorganisms that antagonize pathogens represents a sustainable approach for plant disease management. However, biocontrol agents that are effective in the laboratory often have diminished or variable performance in the field. It is often assumed that microbial interactions within the plant rhizosphere can influence the performance of biocontrol agents. To validate this hypothesis, we established a tripartite bacterial model system based on field investigations, involving antibiotic producers (Bacillus amyloliquefaciens P224, Bacillus subtilis P165, and Bacillus velezensis P63), an antibiotic degrader (Stenotrophomonas maltophilia P373), and a bacterial plant pathogen (Ralstonia solanacearum PA1). The selected Bacillus species antagonize R. solanacearum and act as biocontrol agents of the bacterial wilt of tomatoes caused by this pathogen. We demonstrated that S. maltophilia diminished this biocontrol effect by degrading the lipopeptide antibiotics iturin, fengycin, and surfactin secreted by Bacillus spp., thereby serving as a "pathogen helper" that indirectly facilitated pathogen invasion. Further transcriptomic and proteomic analyses revealed that the lipopeptide inactivation mechanism in S. maltophilia involved multi-drug efflux systems, ribosomal adaptation, and enzymatic hydrolysis. Additionally, the interspecies interactions in our model system are modulated by nutrient availability, with elevated carbon sources enhancing the interference competitive ability of Bacillus spp. against S. maltophilia, thereby mitigating its negative impact on the biocontrol of R. solanacearum. Our study sheds light on the complex interactions among plant pathogens, biocontrol agents, and the indigenous microbial community, underscoring the necessity to account for native antibiotic-degrading organisms when applying biocontrol strategies for effective disease management.
{"title":"Stenotrophomonas maltophilia impedes Bacillus biocontrol of tomato wilt disease by degrading its lipopeptide antibiotics.","authors":"Junwei Peng,Dmitri V Mavrodi,Jiasui Li,Suhelen Egan,Huanhuan Zhang,Xiuli Fan,Yang Liu,Keke Dang,Olga V Mavrodi,Qin Liu,Yuanhua Dong,Jiangang Li","doi":"10.1093/ismejo/wraf210","DOIUrl":"https://doi.org/10.1093/ismejo/wraf210","url":null,"abstract":"Harnessing antibiotic-producing microorganisms that antagonize pathogens represents a sustainable approach for plant disease management. However, biocontrol agents that are effective in the laboratory often have diminished or variable performance in the field. It is often assumed that microbial interactions within the plant rhizosphere can influence the performance of biocontrol agents. To validate this hypothesis, we established a tripartite bacterial model system based on field investigations, involving antibiotic producers (Bacillus amyloliquefaciens P224, Bacillus subtilis P165, and Bacillus velezensis P63), an antibiotic degrader (Stenotrophomonas maltophilia P373), and a bacterial plant pathogen (Ralstonia solanacearum PA1). The selected Bacillus species antagonize R. solanacearum and act as biocontrol agents of the bacterial wilt of tomatoes caused by this pathogen. We demonstrated that S. maltophilia diminished this biocontrol effect by degrading the lipopeptide antibiotics iturin, fengycin, and surfactin secreted by Bacillus spp., thereby serving as a \"pathogen helper\" that indirectly facilitated pathogen invasion. Further transcriptomic and proteomic analyses revealed that the lipopeptide inactivation mechanism in S. maltophilia involved multi-drug efflux systems, ribosomal adaptation, and enzymatic hydrolysis. Additionally, the interspecies interactions in our model system are modulated by nutrient availability, with elevated carbon sources enhancing the interference competitive ability of Bacillus spp. against S. maltophilia, thereby mitigating its negative impact on the biocontrol of R. solanacearum. Our study sheds light on the complex interactions among plant pathogens, biocontrol agents, and the indigenous microbial community, underscoring the necessity to account for native antibiotic-degrading organisms when applying biocontrol strategies for effective disease management.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"2 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-09-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145117073","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}
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}
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：