Microbes coordinate homeostasis in host-associated and environmental ecosystems alike, but the connectivity of these biomes is seldom considered. Hosts exert controls on the composition and function of their internally associated symbionts, but an underappreciated modality of microbiome curation is external to the host through changes to the environmental species pool from which they recruit microbial symbionts. Niche construction theory describes how organisms alter their environment and the selective landscape of their offspring and conspecifics. We hypothesize that host-driven manipulation of environmental microbial communities is an underexplored form of this concept. Using the pitcher plant mosquito (Wyeomyia smithii) as a model, we tested how hosts shape microbial communities across developmental stages and gradients of pre-existing community complexity. We report three lines of evidence supporting host-mediated niche construction, leveraging amplicon sequencing and microbiota manipulation experiments with germ-free (axenic) and selectively recolonized (gnotobiotic) mosquitoes. First, single female egg-laying assays showed repeatable adult inoculation of sterile water with beneficial bacteria capable of sustaining robust larval development. Second, increasing larval density in assays inoculated with complex, field-derived microbial communities selected for environmental and host-associated bacteria that correlated with increased larval fitness. Finally, exposing axenic larvae to mixtures of parentally and environmentally derived microbiota demonstrated that prior conditioning by conspecifics enhanced offspring fitness. Although the bacterial taxa associated with mosquito structuring varied, members of the Actinobacteriota and Acetobacteraceae were consistently associated with increased fitness. Overall, our results provide an example of host-mediated niche construction to favor environmental microbial communities that positively impact host fitness.
{"title":"Host-mediated niche construction of bacterial communities in an aquatic microecosystem.","authors":"Aldo A Arellano,Journey L Prack,Kerri L Coon","doi":"10.1093/ismejo/wraf233","DOIUrl":"https://doi.org/10.1093/ismejo/wraf233","url":null,"abstract":"Microbes coordinate homeostasis in host-associated and environmental ecosystems alike, but the connectivity of these biomes is seldom considered. Hosts exert controls on the composition and function of their internally associated symbionts, but an underappreciated modality of microbiome curation is external to the host through changes to the environmental species pool from which they recruit microbial symbionts. Niche construction theory describes how organisms alter their environment and the selective landscape of their offspring and conspecifics. We hypothesize that host-driven manipulation of environmental microbial communities is an underexplored form of this concept. Using the pitcher plant mosquito (Wyeomyia smithii) as a model, we tested how hosts shape microbial communities across developmental stages and gradients of pre-existing community complexity. We report three lines of evidence supporting host-mediated niche construction, leveraging amplicon sequencing and microbiota manipulation experiments with germ-free (axenic) and selectively recolonized (gnotobiotic) mosquitoes. First, single female egg-laying assays showed repeatable adult inoculation of sterile water with beneficial bacteria capable of sustaining robust larval development. Second, increasing larval density in assays inoculated with complex, field-derived microbial communities selected for environmental and host-associated bacteria that correlated with increased larval fitness. Finally, exposing axenic larvae to mixtures of parentally and environmentally derived microbiota demonstrated that prior conditioning by conspecifics enhanced offspring fitness. Although the bacterial taxa associated with mosquito structuring varied, members of the Actinobacteriota and Acetobacteraceae were consistently associated with increased fitness. Overall, our results provide an example of host-mediated niche construction to favor environmental microbial communities that positively impact host fitness.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"57 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145305716","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}
Farah Boubsi, Adrien Anckaert, Anthony Argüelles-Arias, Marc Ongena
Certain beneficial bacteria of the root-associated microbiome such as B. velezensis protect plants against diseases and are promising biocontrol agents exploited in sustainable agriculture. Unveiling the molecular dialogue governing mutualistic interactions between these beneficials and their host is essential to better understand their ecological behavior and to optimize their use as bioprotectants. However, the chemical diversity and functionality of mediators involved in this interkingdom crosstalk remain largely unexplored. In this study, we uncover a strategy by which B. velezensis exploits the root cell wall polymer pectin to prime its host for enhanced resistance against phytopathogens and to ensure a safe environment enabling its efficient root establishment. Thanks to the activity of its two conserved pectinolytic enzymes, the bacterium generates a specific pattern of short oligogalacturonides that act as efficient triggers of plant systemic defense against leaf pathogens. Moreover, these oligomers induce only weak immune responses in root cells and dampen local defense reaction in response to the perception of the bacterium itself. Our data emphasize the key role of short oligogalacturonides as mediators in the intricate interplay between plants and their bacterial associates, providing new insights into the mechanisms that enable beneficial bacteria to coexist with their host plant.
{"title":"Pectin-derived oligogalacturonides shape mutualistic interactions between Bacillus and its host plant","authors":"Farah Boubsi, Adrien Anckaert, Anthony Argüelles-Arias, Marc Ongena","doi":"10.1093/ismejo/wraf232","DOIUrl":"https://doi.org/10.1093/ismejo/wraf232","url":null,"abstract":"Certain beneficial bacteria of the root-associated microbiome such as B. velezensis protect plants against diseases and are promising biocontrol agents exploited in sustainable agriculture. Unveiling the molecular dialogue governing mutualistic interactions between these beneficials and their host is essential to better understand their ecological behavior and to optimize their use as bioprotectants. However, the chemical diversity and functionality of mediators involved in this interkingdom crosstalk remain largely unexplored. In this study, we uncover a strategy by which B. velezensis exploits the root cell wall polymer pectin to prime its host for enhanced resistance against phytopathogens and to ensure a safe environment enabling its efficient root establishment. Thanks to the activity of its two conserved pectinolytic enzymes, the bacterium generates a specific pattern of short oligogalacturonides that act as efficient triggers of plant systemic defense against leaf pathogens. Moreover, these oligomers induce only weak immune responses in root cells and dampen local defense reaction in response to the perception of the bacterium itself. Our data emphasize the key role of short oligogalacturonides as mediators in the intricate interplay between plants and their bacterial associates, providing new insights into the mechanisms that enable beneficial bacteria to coexist with their host plant.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"19 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145310803","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}
Ravikumar R Patel,Lindsay R Triplett,Stephen J Taerum,Sara L Nason,Cole O Wilson,Blaire Steven
Predatory protists are single-cell eukaryotic organisms capable of hunting and ingesting bacteria and other microorganisms, which are thought to enrich populations of beneficial bacteria in the rhizosphere, potentially influencing plant health. However, the mechanisms underpinning protist interactions with plant growth promoting bacteria are not well understood. We examined the conservation of plant beneficial traits in bacteria associated with ten protists of diverse lineages that were isolated from the maize rhizosphere. Metagenomics, whole-genome sequence analysis, and functional assays of 61 groups of protist-associated bacteria identified tryptophan-dependent biosynthesis of the auxin hormone indole-3-acetic acid (IAA) as the most prevalent predicted trait. Mass spectrometry confirmed that all the protist cultures accumulated IAA after tryptophan supplementation, and that IAA production was bacterial-dependent. Hypothesizing that IAA affects protist function, we observed that exogenous IAA significantly increased the culture density and cell size of all ten protists. Examination of four partial protist genome assemblies identified 13 candidate auxin metabolic gene homologs conserved across plants and protists, and transcriptomic analysis of a Colpoda sp. protist revealed differential expression of thousands of genes in the presence of IAA, further supporting auxin regulation of protist function. These findings demonstrate that soil microeukaryotes can widely host auxin-producing bacteria and that much broader range of eukaryotic lineages perceive and respond to auxin signals than previously recognized. This significantly expands the known breadth of auxin perception as an interkingdom signal, with important implications for soil nutrient cycling and rhizosphere ecology.
{"title":"Diverse soil protists show auxin regulated growth in partnership with auxin-producing bacteria.","authors":"Ravikumar R Patel,Lindsay R Triplett,Stephen J Taerum,Sara L Nason,Cole O Wilson,Blaire Steven","doi":"10.1093/ismejo/wraf234","DOIUrl":"https://doi.org/10.1093/ismejo/wraf234","url":null,"abstract":"Predatory protists are single-cell eukaryotic organisms capable of hunting and ingesting bacteria and other microorganisms, which are thought to enrich populations of beneficial bacteria in the rhizosphere, potentially influencing plant health. However, the mechanisms underpinning protist interactions with plant growth promoting bacteria are not well understood. We examined the conservation of plant beneficial traits in bacteria associated with ten protists of diverse lineages that were isolated from the maize rhizosphere. Metagenomics, whole-genome sequence analysis, and functional assays of 61 groups of protist-associated bacteria identified tryptophan-dependent biosynthesis of the auxin hormone indole-3-acetic acid (IAA) as the most prevalent predicted trait. Mass spectrometry confirmed that all the protist cultures accumulated IAA after tryptophan supplementation, and that IAA production was bacterial-dependent. Hypothesizing that IAA affects protist function, we observed that exogenous IAA significantly increased the culture density and cell size of all ten protists. Examination of four partial protist genome assemblies identified 13 candidate auxin metabolic gene homologs conserved across plants and protists, and transcriptomic analysis of a Colpoda sp. protist revealed differential expression of thousands of genes in the presence of IAA, further supporting auxin regulation of protist function. These findings demonstrate that soil microeukaryotes can widely host auxin-producing bacteria and that much broader range of eukaryotic lineages perceive and respond to auxin signals than previously recognized. This significantly expands the known breadth of auxin perception as an interkingdom signal, with important implications for soil nutrient cycling and rhizosphere ecology.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"2 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145296175","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}
Vaishnavi G Padaki, Xavier Mayali, Peter K Weber, Stephen J Giovannoni, Kaylene Abraham, Kerry Jacobs, Lindsay Collart, Kimberly H Halsey
Labile dissolved organic carbon in the surface oceans accounts for ~¼ of carbon produced through photosynthesis and turns over on average every three days, fueling one of the largest engines of microbial heterotrophic production on the planet. Volatile organic compounds are poorly constrained components of dissolved organic carbon. Here, we detected 72 m/z signals, corresponding to unique volatile organic compounds, including petroleum hydrocarbons, totaling approximately 18.5 nM in the culture medium of a model diatom. In five cocultures with bacteria adapted to grow with this diatom, 1 to 59 m/z signals were depleted. Two of the most active volatile organic compound consumers, Marinobacter and Roseibium, contained more genes encoding volatile organic compound oxidation proteins, and attached to the diatom, suggesting volatile organic compound specialism. With nanoscale secondary ion mass spectrometry and stable isotope labeling, we confirmed that Marinobacter incorporated carbon from benzene, one of the depleted m/z signals detected in the co-culture. Diatom gross carbon production increased by up to 29% in the presence of volatile organic compound consumers, indicating that volatile organic compound consumption by heterotrophic bacteria in the phycosphere – a region of rapid organic carbon oxidation that surrounds phytoplankton cells – could impact global rates of gross primary production.
{"title":"Bacterial Volatile Organic Compound Specialists in the Phycosphere","authors":"Vaishnavi G Padaki, Xavier Mayali, Peter K Weber, Stephen J Giovannoni, Kaylene Abraham, Kerry Jacobs, Lindsay Collart, Kimberly H Halsey","doi":"10.1093/ismejo/wraf229","DOIUrl":"https://doi.org/10.1093/ismejo/wraf229","url":null,"abstract":"Labile dissolved organic carbon in the surface oceans accounts for ~¼ of carbon produced through photosynthesis and turns over on average every three days, fueling one of the largest engines of microbial heterotrophic production on the planet. Volatile organic compounds are poorly constrained components of dissolved organic carbon. Here, we detected 72 m/z signals, corresponding to unique volatile organic compounds, including petroleum hydrocarbons, totaling approximately 18.5 nM in the culture medium of a model diatom. In five cocultures with bacteria adapted to grow with this diatom, 1 to 59 m/z signals were depleted. Two of the most active volatile organic compound consumers, Marinobacter and Roseibium, contained more genes encoding volatile organic compound oxidation proteins, and attached to the diatom, suggesting volatile organic compound specialism. With nanoscale secondary ion mass spectrometry and stable isotope labeling, we confirmed that Marinobacter incorporated carbon from benzene, one of the depleted m/z signals detected in the co-culture. Diatom gross carbon production increased by up to 29% in the presence of volatile organic compound consumers, indicating that volatile organic compound consumption by heterotrophic bacteria in the phycosphere – a region of rapid organic carbon oxidation that surrounds phytoplankton cells – could impact global rates of gross primary production.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"11 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145295598","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}
Jason L Baer,Kacie T Kajihara,Leena L Vilonen,Allie J Hall,Cadie M Young,Danyel K Yogi,Matthew C I Medeiros,Anthony S Amend,Nicole A Hynson
The species area relationship is a classic ecological law describing the relationship between habitat increase and the number of species. Species area relationships are resoundingly positive across macrobes such as plants and animals, and emerge through non-exclusive stochastic and deterministic processes including changes in immigration and extinction, drift, and environmental heterogeneity. Due to unique attributes of the microbial lifestyle, they may not abide by similar rules as macrobes, especially when it comes to spatial scaling. We predict that host-associated microbiomes will exhibit shallower species area relationships than free-living microbiomes due to strong host filtering, and that the species area relationships of bacteria will be shallower than fungi due primarily to differences in dispersal ability. We test these predictions in a relatively simple field system where bromeliad phytotelmata comprise aquatic ecosystems that support invertebrates and environmental substrates such as detritus. Larger phytotelmata generate larger habitat islands for microbiomes allowing us to explicitly examine their species area relationships. We find that the species area relationships of free-living and host-associated microbiomes differ, as do those of microbiome members. By assessing the relationship between environmental conditions and richness, and measuring diversity across scales, we posit that these observed differences in species area relationships are owed to differences in realized niches and dispersal abilities among microbes. These findings highlight that the classic laws of biological spatial scaling do not necessarily accurately represent microbiomes, and that the influence of area on diversity appears to be more important for some microbiomes and microbes than others.
{"title":"Microbiome spatial scaling varies among members, hosts, and environments across model island ecosystems.","authors":"Jason L Baer,Kacie T Kajihara,Leena L Vilonen,Allie J Hall,Cadie M Young,Danyel K Yogi,Matthew C I Medeiros,Anthony S Amend,Nicole A Hynson","doi":"10.1093/ismejo/wraf228","DOIUrl":"https://doi.org/10.1093/ismejo/wraf228","url":null,"abstract":"The species area relationship is a classic ecological law describing the relationship between habitat increase and the number of species. Species area relationships are resoundingly positive across macrobes such as plants and animals, and emerge through non-exclusive stochastic and deterministic processes including changes in immigration and extinction, drift, and environmental heterogeneity. Due to unique attributes of the microbial lifestyle, they may not abide by similar rules as macrobes, especially when it comes to spatial scaling. We predict that host-associated microbiomes will exhibit shallower species area relationships than free-living microbiomes due to strong host filtering, and that the species area relationships of bacteria will be shallower than fungi due primarily to differences in dispersal ability. We test these predictions in a relatively simple field system where bromeliad phytotelmata comprise aquatic ecosystems that support invertebrates and environmental substrates such as detritus. Larger phytotelmata generate larger habitat islands for microbiomes allowing us to explicitly examine their species area relationships. We find that the species area relationships of free-living and host-associated microbiomes differ, as do those of microbiome members. By assessing the relationship between environmental conditions and richness, and measuring diversity across scales, we posit that these observed differences in species area relationships are owed to differences in realized niches and dispersal abilities among microbes. These findings highlight that the classic laws of biological spatial scaling do not necessarily accurately represent microbiomes, and that the influence of area on diversity appears to be more important for some microbiomes and microbes than others.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"136 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145277134","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 overwintering recovery of Microcystis aeruginosa represents a critical but underexplored phase in the seasonal development of cyanobacterial blooms. Although the role of temperature in driving bloom onset is recognized, its effects on microbial assembly and the molecular transformation of dissolved organic matter during reactivation remain insufficiently characterized. In this study, 16S rRNA gene sequencing, excitation-emission matrix fluorescence spectroscopy coupled with parallel factor analysis, Fourier transform ion cyclotron resonance mass spectrometry, and metabolomics were applied to examine how three thermal recovery regimes-constant temperature, gradual warming, and cold-dark preconditioning-shape microbial succession and dissolved organic matter dynamics. Constant temperature accelerated the dispersal limitation of bacterial communities and promoted rapid DOM turnover, whereas gradual warming and cold-dark preconditioning induced more undominated community structures, and the accumulation of nitrogen- and sulfur-rich DOM compounds. Cold-dark pretreatment notably enhanced the formation of structurally complex, recalcitrant DOM, and delayed microbial reactivation. The network of relationships between microorganisms and dissolved organic matter revealed distinct coupling patterns across treatments, with enhanced microbial processing of aromatic and humic-like molecules occurring under thermal fluctuation or stress. Metabolomic profiling further indicated different physiological adaptation strategies, with stress-linked metabolites enriched under variable-temperature conditions. These findings highlight the mechanistic links between temperature-driven microbial recovery and dissolved organic matter transformation, providing new insights into how winter conditions influence cyanobacterial bloom trajectories in freshwater ecosystems.
{"title":"Thermal regimes during overwintering recovery shape microbial network and dissolved organic matter complexity in Microcystis-dominated systems.","authors":"Yang Liu,Zongjie Xie,Jia Feng,Shulian Xie,Chao Ma","doi":"10.1093/ismejo/wraf227","DOIUrl":"https://doi.org/10.1093/ismejo/wraf227","url":null,"abstract":"The overwintering recovery of Microcystis aeruginosa represents a critical but underexplored phase in the seasonal development of cyanobacterial blooms. Although the role of temperature in driving bloom onset is recognized, its effects on microbial assembly and the molecular transformation of dissolved organic matter during reactivation remain insufficiently characterized. In this study, 16S rRNA gene sequencing, excitation-emission matrix fluorescence spectroscopy coupled with parallel factor analysis, Fourier transform ion cyclotron resonance mass spectrometry, and metabolomics were applied to examine how three thermal recovery regimes-constant temperature, gradual warming, and cold-dark preconditioning-shape microbial succession and dissolved organic matter dynamics. Constant temperature accelerated the dispersal limitation of bacterial communities and promoted rapid DOM turnover, whereas gradual warming and cold-dark preconditioning induced more undominated community structures, and the accumulation of nitrogen- and sulfur-rich DOM compounds. Cold-dark pretreatment notably enhanced the formation of structurally complex, recalcitrant DOM, and delayed microbial reactivation. The network of relationships between microorganisms and dissolved organic matter revealed distinct coupling patterns across treatments, with enhanced microbial processing of aromatic and humic-like molecules occurring under thermal fluctuation or stress. Metabolomic profiling further indicated different physiological adaptation strategies, with stress-linked metabolites enriched under variable-temperature conditions. These findings highlight the mechanistic links between temperature-driven microbial recovery and dissolved organic matter transformation, providing new insights into how winter conditions influence cyanobacterial bloom trajectories in freshwater ecosystems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"37 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145277133","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}
Sarah J Tucker, Kelle C Freel, A Murat Eren, Michael S Rappé
The order Pelagibacterales (SAR11) is the most abundant group of heterotrophic bacteria in the global surface ocean, where individual sublineages likely play distinct roles in oceanic biogeochemical cycles. Yet, understanding the determinants of niche partitioning within SAR11 has been a formidable challenge due to the high genetic diversity within individual SAR11 sublineages and the limited availability of high-quality genomes from both cultivation and metagenomic reconstruction. Through an integrated metapangenomic analysis of 71 new SAR11 isolate genomes and a time-series of metagenomes from the prominent source of isolation, we reveal an ecological and phylogenetic partitioning of metabolic traits across SAR11 genera. We resolve distinct habitat preferences among genera for coastal or offshore environments of the tropical Pacific and identify a handful of genes involved in carbon and nitrogen metabolisms that appear to contribute to these contrasting lifestyles. Furthermore, we find that some habitat-specific genes experience high selective pressures, indicating that they are critical determinants of SAR11 fitness and niche differentiation. Together, these insights reveal the underlying evolutionary processes shaping niche-partitioning within sympatric and parapatric populations of SAR11 and demonstrate that the immense genomic diversity of SAR11 bacteria naturally segregates into ecologically and genetically cohesive units, or ecotypes, that vary in spatial distributions in the tropical Pacific.
{"title":"Habitat-specificity in SAR11 is associated with a few genes under high selection","authors":"Sarah J Tucker, Kelle C Freel, A Murat Eren, Michael S Rappé","doi":"10.1093/ismejo/wraf216","DOIUrl":"https://doi.org/10.1093/ismejo/wraf216","url":null,"abstract":"The order Pelagibacterales (SAR11) is the most abundant group of heterotrophic bacteria in the global surface ocean, where individual sublineages likely play distinct roles in oceanic biogeochemical cycles. Yet, understanding the determinants of niche partitioning within SAR11 has been a formidable challenge due to the high genetic diversity within individual SAR11 sublineages and the limited availability of high-quality genomes from both cultivation and metagenomic reconstruction. Through an integrated metapangenomic analysis of 71 new SAR11 isolate genomes and a time-series of metagenomes from the prominent source of isolation, we reveal an ecological and phylogenetic partitioning of metabolic traits across SAR11 genera. We resolve distinct habitat preferences among genera for coastal or offshore environments of the tropical Pacific and identify a handful of genes involved in carbon and nitrogen metabolisms that appear to contribute to these contrasting lifestyles. Furthermore, we find that some habitat-specific genes experience high selective pressures, indicating that they are critical determinants of SAR11 fitness and niche differentiation. Together, these insights reveal the underlying evolutionary processes shaping niche-partitioning within sympatric and parapatric populations of SAR11 and demonstrate that the immense genomic diversity of SAR11 bacteria naturally segregates into ecologically and genetically cohesive units, or ecotypes, that vary in spatial distributions in the tropical Pacific.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"10 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145261600","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}
Bacterial locomotion is integral to acquiring resources and getting access to new niches. Swarming, a type of motility where flagellated bacteria cooperatively move together across a semi solid surface, is one example of how bacteria can colonize new territories. This collective behavior is temporally and spatially orchestrated, requiring task specialization of community members. In this study, we paired a swarming bacterium, Paenibacillus amylolyticus, with a non-swarmer, Stenotrophomonas maltophilia, to investigate the impact on fitness of each strain. In dual-species conditions, the community swarm became significantly thicker and improved the ability of S. maltophilia to range into new territories. Swarming enabled P. amylolyticus to cross barriers of antimicrobials, whereas the thicker, dual-species swarm did not empower S. maltophilia to cross. Comparative studies of population dynamics revealed that over time, monospecies swarms of P. amylolyticus entered a state unable to grow despite still showing reductase activity. However, in a dual-species swarm, S. maltophilia rescued P. amylolyticus from this state. This rescue is attributed to the pH stabilization that occurs in this two-species combination, where S. maltophilia alkalizes the environment, thereby providing a more favorable environment for P. amylolyticus.
{"title":"Co-cultivation rescues suicidal Paenibacillus amylolyticus swarms.","authors":"Dana Ronin,Mads Frederik Hansen,Mette Burmølle","doi":"10.1093/ismejo/wraf225","DOIUrl":"https://doi.org/10.1093/ismejo/wraf225","url":null,"abstract":"Bacterial locomotion is integral to acquiring resources and getting access to new niches. Swarming, a type of motility where flagellated bacteria cooperatively move together across a semi solid surface, is one example of how bacteria can colonize new territories. This collective behavior is temporally and spatially orchestrated, requiring task specialization of community members. In this study, we paired a swarming bacterium, Paenibacillus amylolyticus, with a non-swarmer, Stenotrophomonas maltophilia, to investigate the impact on fitness of each strain. In dual-species conditions, the community swarm became significantly thicker and improved the ability of S. maltophilia to range into new territories. Swarming enabled P. amylolyticus to cross barriers of antimicrobials, whereas the thicker, dual-species swarm did not empower S. maltophilia to cross. Comparative studies of population dynamics revealed that over time, monospecies swarms of P. amylolyticus entered a state unable to grow despite still showing reductase activity. However, in a dual-species swarm, S. maltophilia rescued P. amylolyticus from this state. This rescue is attributed to the pH stabilization that occurs in this two-species combination, where S. maltophilia alkalizes the environment, thereby providing a more favorable environment for P. amylolyticus.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"64 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145247114","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}
Yihua Liu,Alyse K Kiesser,Agasteswar Vadlamani,Angela Kouris,Marc Strous
Alkaline soda lakes, characterized by high pH and high concentrations of sodium and dissolved carbonates, support diverse alkaliphilic microbial communities. Using stable isotope probing with 13C-bicarbonate, 15N-ammonium, 15N-nitrate, and 15N-urea, we measured assimilation rates for carbon and nitrogen by microbial mats of alkaline Goodenough Lake, Canada. Our results showed extremely high carbon fixation rates averaging 24 g C/m2/day, equalling or exceeding rates measured fifty years ago in African alkaline soda lakes. Urea consumption occurred both during the day and during the night, but assimilation mainly occurred during the day. Ammonium assimilation was stable between day and night. Apparently, cyanobacteria preferred urea as a nitrogen source, whereas heterotrophs preferred ammonium. Two different cyanobacteria dominated the microbial mats, Nodosilinea and Sodalinema. Using Orbitrap mass spectrometry, we only observed assimilation of 13C bicarbonate by Sodalinema, but not by Nodosilinea. The latter might focus on different carbon sources, such as urea. Strong negative correlation between their abundances in proteomes also supported niche partitioning between these two cyanobacteria.
碱性苏打湖的特点是pH值高，钠和溶解的碳酸盐浓度高，支持多种亲碱微生物群落。采用13c -碳酸氢盐、15n -铵、15n -硝酸盐和15n -尿素等稳定同位素探测，测定了加拿大古迪纳夫湖碱性微生物垫对碳和氮的同化速率。我们的研究结果显示了极高的碳固定率，平均为24 g C/m2/天，等于或超过了50年前在非洲碱性苏打湖中测量到的碳固定率。尿素消耗在白天和夜间都有发生，但同化主要发生在白天。铵态氮同化在白天和夜间都是稳定的。显然，蓝藻偏爱尿素作为氮源，而异养菌偏爱铵。两种不同的蓝藻占据了微生物席，Nodosilinea和Sodalinema。利用Orbitrap质谱法，我们只观察到Sodalinema对碳酸盐13C的同化作用，而Nodosilinea则没有。后者可能侧重于不同的碳源，如尿素。它们在蛋白质组中丰度之间的强负相关也支持这两种蓝藻之间的生态位分配。
{"title":"Exceptionally high carbon fixation and nitrogen assimilation rates in microbial mats of an alkaline soda lake.","authors":"Yihua Liu,Alyse K Kiesser,Agasteswar Vadlamani,Angela Kouris,Marc Strous","doi":"10.1093/ismejo/wraf226","DOIUrl":"https://doi.org/10.1093/ismejo/wraf226","url":null,"abstract":"Alkaline soda lakes, characterized by high pH and high concentrations of sodium and dissolved carbonates, support diverse alkaliphilic microbial communities. Using stable isotope probing with 13C-bicarbonate, 15N-ammonium, 15N-nitrate, and 15N-urea, we measured assimilation rates for carbon and nitrogen by microbial mats of alkaline Goodenough Lake, Canada. Our results showed extremely high carbon fixation rates averaging 24 g C/m2/day, equalling or exceeding rates measured fifty years ago in African alkaline soda lakes. Urea consumption occurred both during the day and during the night, but assimilation mainly occurred during the day. Ammonium assimilation was stable between day and night. Apparently, cyanobacteria preferred urea as a nitrogen source, whereas heterotrophs preferred ammonium. Two different cyanobacteria dominated the microbial mats, Nodosilinea and Sodalinema. Using Orbitrap mass spectrometry, we only observed assimilation of 13C bicarbonate by Sodalinema, but not by Nodosilinea. The latter might focus on different carbon sources, such as urea. Strong negative correlation between their abundances in proteomes also supported niche partitioning between these two cyanobacteria.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"111 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145247026","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}
Clifton P Bueno de Mesquita,Matthew R Olm,Andrew Bissett,Noah Fierer
Global surveys of soil bacteria have identified several taxa that are nearly ubiquitous and often the most abundant members of soil bacterial communities. However, it remains unclear why these taxa are so abundant and prevalent across a wide range of soil types and environmental conditions. Here we use genome-resolved metagenomics to test the hypothesis that strain-level differences exist in these taxa that are not adequately captured with standard marker gene sequencing, and that distinct strains harbor unique traits that reflect adaptations to different soil environments. We analyzed data from 331 natural soils spanning Australia to assess strain differentiation in Bradyrhizobium, a dominant soil bacterial genus of ecological importance. We developed a workflow for strain-level bacterial analyses of complex soil metagenomes, combining genomes from pre-existing databases with new genomes generated via targeted assembly from metagenomes to detect 181 Bradyrhizobium strains across the soil collection. In addition to a high degree of phylogenetic variation, we observed substantial variation in pangenome content and inferred traits, highlighting the breadth of diversity within this widespread genus. Although members of the genus Bradyrhizobium were detected in >80% of samples, most individual strains were restricted in their distributions. The overall strain-level community composition of Bradyrhizobium varied significantly across geographic space and environmental gradients, and was particularly associated with differences in temperature, soil pH, and soil nitrate and metal concentrations. Our work provides a general framework for studying the strain-level ecology of soil bacteria and highlights the ecological and pangenomic diversity within this dominant soil bacterial genus.
{"title":"High strain-level diversity of Bradyrhizobium across Australian soils.","authors":"Clifton P Bueno de Mesquita,Matthew R Olm,Andrew Bissett,Noah Fierer","doi":"10.1093/ismejo/wraf222","DOIUrl":"https://doi.org/10.1093/ismejo/wraf222","url":null,"abstract":"Global surveys of soil bacteria have identified several taxa that are nearly ubiquitous and often the most abundant members of soil bacterial communities. However, it remains unclear why these taxa are so abundant and prevalent across a wide range of soil types and environmental conditions. Here we use genome-resolved metagenomics to test the hypothesis that strain-level differences exist in these taxa that are not adequately captured with standard marker gene sequencing, and that distinct strains harbor unique traits that reflect adaptations to different soil environments. We analyzed data from 331 natural soils spanning Australia to assess strain differentiation in Bradyrhizobium, a dominant soil bacterial genus of ecological importance. We developed a workflow for strain-level bacterial analyses of complex soil metagenomes, combining genomes from pre-existing databases with new genomes generated via targeted assembly from metagenomes to detect 181 Bradyrhizobium strains across the soil collection. In addition to a high degree of phylogenetic variation, we observed substantial variation in pangenome content and inferred traits, highlighting the breadth of diversity within this widespread genus. Although members of the genus Bradyrhizobium were detected in >80% of samples, most individual strains were restricted in their distributions. The overall strain-level community composition of Bradyrhizobium varied significantly across geographic space and environmental gradients, and was particularly associated with differences in temperature, soil pH, and soil nitrate and metal concentrations. Our work provides a general framework for studying the strain-level ecology of soil bacteria and highlights the ecological and pangenomic diversity within this dominant soil bacterial genus.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"11 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145246610","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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