Athanasia Ioannou, Maryse D Berkhout, William T Scott, Bernadet Blijenberg, Sjef Boeren, Marko Mank, Jan Knol, Clara Belzer
Quickly after birth, the gut microbiota is shaped via species acquisition and resource pressure. Breastmilk, and more specifically, human milk oligosaccharides are a determining factor in the formation of microbial communities and the interactions between bacteria. Prominent human milk oligosaccharide degraders have been rigorously characterized, but it is not known how the gut microbiota is shaped as a complex community. Here, we designed BIG-Syc, a synthetic community of 13 strains from the gut of vaginally born, breastfed infants. BIG-Syc replicated key compositional, metabolic, and proteomic characteristics of the gut microbiota of infants. Upon fermentation of a 4 and 5 human milk oligosaccharide mix, BIG-Syc demonstrated different compositional and proteomic profiles, with Bifidobacterium infantis and Bifidobacterium bifidum suppressing one another. The mix of 5 human milk oligosaccharides resulted in a more diverse composition with dominance of B. bifidum, whereas that with 4 human milk oligosaccharides supported the dominance of B. infantis, in 4 of 6 replicates. Reintroduction of bifidobacteria to BIG-Syc led to their engraftment and establishment of their niche. Based on proteomics and genome-scale metabolic models, we reconstructed the carbon source utilization and metabolite and gas production per strain. BIG-Syc demonstrated teamwork as cross-feeders utilized simpler carbohydrates, organic acids, and gases released from human milk oligosaccharide degraders. Collectively, our results showed that human milk oligosaccharides prompt resource-sharing for their complete degradation while leading to a different compositional and functional profile in the community. At the same time, BIG-Syc proved to be an accurate model for the representation of intra-microbe interactions.
{"title":"Resource sharing of an infant gut microbiota synthetic community in combinations of human milk oligosaccharides","authors":"Athanasia Ioannou, Maryse D Berkhout, William T Scott, Bernadet Blijenberg, Sjef Boeren, Marko Mank, Jan Knol, Clara Belzer","doi":"10.1093/ismejo/wrae209","DOIUrl":"https://doi.org/10.1093/ismejo/wrae209","url":null,"abstract":"Quickly after birth, the gut microbiota is shaped via species acquisition and resource pressure. Breastmilk, and more specifically, human milk oligosaccharides are a determining factor in the formation of microbial communities and the interactions between bacteria. Prominent human milk oligosaccharide degraders have been rigorously characterized, but it is not known how the gut microbiota is shaped as a complex community. Here, we designed BIG-Syc, a synthetic community of 13 strains from the gut of vaginally born, breastfed infants. BIG-Syc replicated key compositional, metabolic, and proteomic characteristics of the gut microbiota of infants. Upon fermentation of a 4 and 5 human milk oligosaccharide mix, BIG-Syc demonstrated different compositional and proteomic profiles, with Bifidobacterium infantis and Bifidobacterium bifidum suppressing one another. The mix of 5 human milk oligosaccharides resulted in a more diverse composition with dominance of B. bifidum, whereas that with 4 human milk oligosaccharides supported the dominance of B. infantis, in 4 of 6 replicates. Reintroduction of bifidobacteria to BIG-Syc led to their engraftment and establishment of their niche. Based on proteomics and genome-scale metabolic models, we reconstructed the carbon source utilization and metabolite and gas production per strain. BIG-Syc demonstrated teamwork as cross-feeders utilized simpler carbohydrates, organic acids, and gases released from human milk oligosaccharide degraders. Collectively, our results showed that human milk oligosaccharides prompt resource-sharing for their complete degradation while leading to a different compositional and functional profile in the community. At the same time, BIG-Syc proved to be an accurate model for the representation of intra-microbe interactions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"29 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142449619","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}
Jule Freudenthal, Kenneth Dumack, Stefan Schaffer, Martin Schlegel, Michael Bonkowski
With over 3 trillion trees, forest ecosystems comprise nearly one-third of the terrestrial surface of the Earth. Very little attention has been given to the exploration of the above-ground plant microbiome of trees, its complex trophic interactions, and variations among tree species. To address this knowledge gap, we applied a primer-independent shotgun metatranscriptomic approach to assess the entire living canopy bark microbiome comprising prokaryotic and eukaryotic primary producers, decomposers, and various groups of consumers. With almost 1500 genera, we found a high microbial diversity on three tree species with distinct bark textures: oak (Quercus robur), linden (Tilia cordata), both with rough bark, and maple (Acer pseudoplatanus) with smooth bark. Core co-occurrence network analysis revealed a rich food web dominated by algal primary producers, and bacterial and fungal decomposers, sustaining a diverse community of consumers, including protists, microscopic metazoans and predatory bacteria. Whereas maple accommodated a depauperate microbiome, oak and linden accommodated a richer microbiome mainly differing in their relative community composition: Bacteria exhibited an increased dominance on linden, whereas co-occurring algae and fungi dominated on oak, highlighting the importance of algal-fungal lichen symbioses even at the microscopic scale. Further, due to bacteria-fungi co-exclusion, bacteria on bark are not the main beneficiaries of algae-derived carbon compounds as it is known from aquatic systems.
{"title":"Algae-fungi symbioses and bacteria-fungi co-exclusion drive tree species-specific differences in canopy bark microbiomes","authors":"Jule Freudenthal, Kenneth Dumack, Stefan Schaffer, Martin Schlegel, Michael Bonkowski","doi":"10.1093/ismejo/wrae206","DOIUrl":"https://doi.org/10.1093/ismejo/wrae206","url":null,"abstract":"With over 3 trillion trees, forest ecosystems comprise nearly one-third of the terrestrial surface of the Earth. Very little attention has been given to the exploration of the above-ground plant microbiome of trees, its complex trophic interactions, and variations among tree species. To address this knowledge gap, we applied a primer-independent shotgun metatranscriptomic approach to assess the entire living canopy bark microbiome comprising prokaryotic and eukaryotic primary producers, decomposers, and various groups of consumers. With almost 1500 genera, we found a high microbial diversity on three tree species with distinct bark textures: oak (Quercus robur), linden (Tilia cordata), both with rough bark, and maple (Acer pseudoplatanus) with smooth bark. Core co-occurrence network analysis revealed a rich food web dominated by algal primary producers, and bacterial and fungal decomposers, sustaining a diverse community of consumers, including protists, microscopic metazoans and predatory bacteria. Whereas maple accommodated a depauperate microbiome, oak and linden accommodated a richer microbiome mainly differing in their relative community composition: Bacteria exhibited an increased dominance on linden, whereas co-occurring algae and fungi dominated on oak, highlighting the importance of algal-fungal lichen symbioses even at the microscopic scale. Further, due to bacteria-fungi co-exclusion, bacteria on bark are not the main beneficiaries of algae-derived carbon compounds as it is known from aquatic systems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"124 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142448353","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}
Autotrophic antimony (Sb) oxidation coupled to nitrate reduction plays an important role in the transformation and detoxification of Sb. However, the specific oxidase involved in this process has yet to be identified. Herein, we enriched the microbiota capable of nitrate-dependent Sb(III) oxidation and identified a new Sb(III) oxidase in an uncultured member of Symbiobacteriaceae. Incubation experiments demonstrated that nitrate-dependent Sb(III) oxidation occurred in the microcosm supplemented with Sb(III) and nitrate. Both the 16S rRNA gene and metagenomic analyses indicated that a species within Symbiobacteriaceae played a crucial role in this process. Furthermore, carbon-13 isotope labelling with carbon dioxide-fixing Rhodopseudomonas palustris in combination with nanoscale secondary ion mass spectrometry revealed that a newly characterized oxidase from the dimethylsulfoxide reductase family, designated as NaoABC, was responsible for autotrophic Sb(III) oxidation coupled with nitrate reduction. The NaoABC complex functions in conjunction with the nitrate reductase NarGHI, forming a redox loop that transfers electrons from Sb(III) to nitrate, thereby generating the energy necessary for autotrophic growth. This research offers new insights into the understanding of how microbes link Sb and nitrogen biogeochemical cycles in the environment.
{"title":"Nitrate-dependent antimony oxidase in an uncultured Symbiobacteriaceae member","authors":"Liying Wang, Zhipeng Yin, Wei Yan, Jialong Hao, Fei Tian, Jianbo Shi","doi":"10.1093/ismejo/wrae204","DOIUrl":"https://doi.org/10.1093/ismejo/wrae204","url":null,"abstract":"Autotrophic antimony (Sb) oxidation coupled to nitrate reduction plays an important role in the transformation and detoxification of Sb. However, the specific oxidase involved in this process has yet to be identified. Herein, we enriched the microbiota capable of nitrate-dependent Sb(III) oxidation and identified a new Sb(III) oxidase in an uncultured member of Symbiobacteriaceae. Incubation experiments demonstrated that nitrate-dependent Sb(III) oxidation occurred in the microcosm supplemented with Sb(III) and nitrate. Both the 16S rRNA gene and metagenomic analyses indicated that a species within Symbiobacteriaceae played a crucial role in this process. Furthermore, carbon-13 isotope labelling with carbon dioxide-fixing Rhodopseudomonas palustris in combination with nanoscale secondary ion mass spectrometry revealed that a newly characterized oxidase from the dimethylsulfoxide reductase family, designated as NaoABC, was responsible for autotrophic Sb(III) oxidation coupled with nitrate reduction. The NaoABC complex functions in conjunction with the nitrate reductase NarGHI, forming a redox loop that transfers electrons from Sb(III) to nitrate, thereby generating the energy necessary for autotrophic growth. This research offers new insights into the understanding of how microbes link Sb and nitrogen biogeochemical cycles in the environment.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"29 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142444255","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}
Chemolithoautotrophic nitrifiers are model groups for linking phylogeny, evolution, and ecophysiology. Ammonia-oxidising bacteria (AOB) typically dominate the first step of ammonia oxidation at high ammonium supply rates, ammonia-oxidising archaea (AOA) and complete ammonia-oxidising Nitrospira (comammox) are often active at lower supply rates or during AOB inactivity, and nitrite-oxidising bacteria (NOB) complete canonical nitrification. Soil virus communities are dynamic but contributions to functional processes are largely undetermined. In addition, characterising viruses infecting hosts with low relative abundance, such as nitrifiers, may be constrained by vast viral diversity, partial genome recovery, and difficulties in host linkage. Here, we describe a targeted incubation study that aimed to determine whether growth of different nitrifier groups in soil is associated with active virus populations and if process-focussed analyses facilitate characterisation of high-quality virus genomes. dsDNA viruses infecting different nitrifier groups were enriched in situ via differential host inhibition. Growth of each nitrifier group was consistent with predicted inhibition profiles and concomitant with the abundance of their viruses. These included 61 high-quality/complete virus genomes 35-173 kb in length with minimal similarity to validated families. AOA viruses lacked ammonia monooxygenase sub-unit C (amoC) genes found in marine AOA viruses but some encoded AOA-specific multicopper oxidase type 1 (MCO1), previously implicated in copper acquisition, and suggesting a role in supporting energy metabolism of soil AOA. Findings demonstrate focussed incubation studies facilitate characterisation of active host-virus interactions associated with specific processes and viruses of soil AOA, AOB and NOB are dynamic and potentially influence nitrogen cycling processes.
{"title":"Activity of novel virus families infecting soil nitrifiers is concomitant with host niche differentiation","authors":"Sungeun Lee, Christina Hazard, Graeme W Nicol","doi":"10.1093/ismejo/wrae205","DOIUrl":"https://doi.org/10.1093/ismejo/wrae205","url":null,"abstract":"Chemolithoautotrophic nitrifiers are model groups for linking phylogeny, evolution, and ecophysiology. Ammonia-oxidising bacteria (AOB) typically dominate the first step of ammonia oxidation at high ammonium supply rates, ammonia-oxidising archaea (AOA) and complete ammonia-oxidising Nitrospira (comammox) are often active at lower supply rates or during AOB inactivity, and nitrite-oxidising bacteria (NOB) complete canonical nitrification. Soil virus communities are dynamic but contributions to functional processes are largely undetermined. In addition, characterising viruses infecting hosts with low relative abundance, such as nitrifiers, may be constrained by vast viral diversity, partial genome recovery, and difficulties in host linkage. Here, we describe a targeted incubation study that aimed to determine whether growth of different nitrifier groups in soil is associated with active virus populations and if process-focussed analyses facilitate characterisation of high-quality virus genomes. dsDNA viruses infecting different nitrifier groups were enriched in situ via differential host inhibition. Growth of each nitrifier group was consistent with predicted inhibition profiles and concomitant with the abundance of their viruses. These included 61 high-quality/complete virus genomes 35-173 kb in length with minimal similarity to validated families. AOA viruses lacked ammonia monooxygenase sub-unit C (amoC) genes found in marine AOA viruses but some encoded AOA-specific multicopper oxidase type 1 (MCO1), previously implicated in copper acquisition, and suggesting a role in supporting energy metabolism of soil AOA. Findings demonstrate focussed incubation studies facilitate characterisation of active host-virus interactions associated with specific processes and viruses of soil AOA, AOB and NOB are dynamic and potentially influence nitrogen cycling processes.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"2 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142444257","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}
Ikaia Leleiwi,Katherine Kokkinias,Yongseok Kim,Maryam Baniasad,Michael Shaffer,Anice Sabag-Daigle,Rebecca A Daly,Rory M Flynn,Vicki H Wysocki,Brian M M Ahmer,Mikayla A Borton,Kelly C Wrighton
Salmonella enterica serovar Typhimurium is a pervasive enteric pathogen and ongoing global threat to public health. Ecological studies in the Salmonella impacted gut remain underrepresented in the literature, discounting microbiome mediated interactions that may inform Salmonella physiology during colonization and infection. To understand the microbial ecology of Salmonella remodeling of the gut microbiome, we performed multi-omics on fecal microbial communities from untreated and Salmonella-infected mice. Reconstructed genomes recruited metatranscriptomic and metabolomic data providing a strain-resolved view of the expressed metabolisms of the microbiome during Salmonella infection. These data informed possible Salmonella interactions with members of the gut microbiome that were previously uncharacterized. Salmonella-induced inflammation significantly reduced the diversity of genomes that recruited transcripts in the gut microbiome, yet increased transcript mapping was observed for 7 members, among which Luxibacter and Ligilactobacillus transcript read recruitment was most prevalent. Metatranscriptomic insights from Salmonella and other persistent taxa in the inflamed microbiome further expounded the necessity for oxidative tolerance mechanisms to endure the host inflammatory responses to infection. In the inflamed gut lactate was a key metabolite, with microbiota production and consumption reported amongst members with detected transcript recruitment. We also showed that organic sulfur sources could be converted by gut microbiota to yield inorganic sulfur pools that become oxidized in the inflamed gut, resulting in thiosulfate and tetrathionate that supports Salmonella respiration. This research advances physiological microbiome insights beyond prior amplicon-based approaches, with the transcriptionally active organismal and metabolic pathways outlined here offering intriguing intervention targets in the Salmonella-infected intestine.
{"title":"Gut microbiota carbon and sulfur metabolisms support Salmonella infections.","authors":"Ikaia Leleiwi,Katherine Kokkinias,Yongseok Kim,Maryam Baniasad,Michael Shaffer,Anice Sabag-Daigle,Rebecca A Daly,Rory M Flynn,Vicki H Wysocki,Brian M M Ahmer,Mikayla A Borton,Kelly C Wrighton","doi":"10.1093/ismejo/wrae187","DOIUrl":"https://doi.org/10.1093/ismejo/wrae187","url":null,"abstract":"Salmonella enterica serovar Typhimurium is a pervasive enteric pathogen and ongoing global threat to public health. Ecological studies in the Salmonella impacted gut remain underrepresented in the literature, discounting microbiome mediated interactions that may inform Salmonella physiology during colonization and infection. To understand the microbial ecology of Salmonella remodeling of the gut microbiome, we performed multi-omics on fecal microbial communities from untreated and Salmonella-infected mice. Reconstructed genomes recruited metatranscriptomic and metabolomic data providing a strain-resolved view of the expressed metabolisms of the microbiome during Salmonella infection. These data informed possible Salmonella interactions with members of the gut microbiome that were previously uncharacterized. Salmonella-induced inflammation significantly reduced the diversity of genomes that recruited transcripts in the gut microbiome, yet increased transcript mapping was observed for 7 members, among which Luxibacter and Ligilactobacillus transcript read recruitment was most prevalent. Metatranscriptomic insights from Salmonella and other persistent taxa in the inflamed microbiome further expounded the necessity for oxidative tolerance mechanisms to endure the host inflammatory responses to infection. In the inflamed gut lactate was a key metabolite, with microbiota production and consumption reported amongst members with detected transcript recruitment. We also showed that organic sulfur sources could be converted by gut microbiota to yield inorganic sulfur pools that become oxidized in the inflamed gut, resulting in thiosulfate and tetrathionate that supports Salmonella respiration. This research advances physiological microbiome insights beyond prior amplicon-based approaches, with the transcriptionally active organismal and metabolic pathways outlined here offering intriguing intervention targets in the Salmonella-infected intestine.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"193 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142439457","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}
Adam J Ellington,Kendra Walters,Brent C Christner,Sam Fox,Krista Bonfantine,Cassie Walker,Phinehas Lampman,David C Vuono,Michael Strickland,Katie Lambert,Leda N Kobziar
Wildland fire is increasingly recognized as a driver of bioaerosol emissions, but the effects that smoke-emitted microbes have on the diversity and community assembly patterns of the habitats where they are deposited remain unknown. In this study, we examined whether microbes aerosolized by biomass burning smoke detectably impact the composition and function of soil sinks using lab-based mesocosm experiments. Soils either containing the native microbial community or presterilized by γ-irradiation were inundated with various doses of smoke from native tallgrass prairie grasses. Smoke-inundated, γ-irradiated soils exhibited significantly higher respiration rates than both smoke-inundated, native soils and γ-irradiated soils exposed to ambient air only. Microbial communities in γ-irradiated soils were significantly different between smoke-treated and control soils, which supports the hypothesis that wildland fire smoke can act as a dispersal agent. Community compositions differed based on smoke dose, incubation time, and soil type. Concentrations of phosphate and microbial biomass carbon and nitrogen together with pH were significant predictors of community composition. Source tracking analysis attributed smoke as contributing nearly 30% of the taxa found in smoke-inundated, γ-irradiated soils, suggesting smoke may play a role in the recovery of microbial communities in similar damaged soils. Our findings demonstrate that short-distance microbial dispersal by biomass burning smoke can influence the assembly processes of microbial communities in soils and has implications for a broad range of fields including agriculture, restoration, plant disease, and biodiversity.
{"title":"Dispersal of microbes from grassland fire smoke to soils.","authors":"Adam J Ellington,Kendra Walters,Brent C Christner,Sam Fox,Krista Bonfantine,Cassie Walker,Phinehas Lampman,David C Vuono,Michael Strickland,Katie Lambert,Leda N Kobziar","doi":"10.1093/ismejo/wrae203","DOIUrl":"https://doi.org/10.1093/ismejo/wrae203","url":null,"abstract":"Wildland fire is increasingly recognized as a driver of bioaerosol emissions, but the effects that smoke-emitted microbes have on the diversity and community assembly patterns of the habitats where they are deposited remain unknown. In this study, we examined whether microbes aerosolized by biomass burning smoke detectably impact the composition and function of soil sinks using lab-based mesocosm experiments. Soils either containing the native microbial community or presterilized by γ-irradiation were inundated with various doses of smoke from native tallgrass prairie grasses. Smoke-inundated, γ-irradiated soils exhibited significantly higher respiration rates than both smoke-inundated, native soils and γ-irradiated soils exposed to ambient air only. Microbial communities in γ-irradiated soils were significantly different between smoke-treated and control soils, which supports the hypothesis that wildland fire smoke can act as a dispersal agent. Community compositions differed based on smoke dose, incubation time, and soil type. Concentrations of phosphate and microbial biomass carbon and nitrogen together with pH were significant predictors of community composition. Source tracking analysis attributed smoke as contributing nearly 30% of the taxa found in smoke-inundated, γ-irradiated soils, suggesting smoke may play a role in the recovery of microbial communities in similar damaged soils. Our findings demonstrate that short-distance microbial dispersal by biomass burning smoke can influence the assembly processes of microbial communities in soils and has implications for a broad range of fields including agriculture, restoration, plant disease, and biodiversity.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"105 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142439553","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}
Tobyn Branck, Zhiji Hu, William A Nickols, Aaron M Walsh, Amrisha Bhosle, Meghan I Short, Jacob T Nearing, Francesco Asnicar, Lauren J McIver, Sagun Maharjan, Ali Rahnavard, Artemis Louyakis, Dayakar V Badri, Christoph Brockel, Kelsey N Thompson, Curtis Huttenhower
The gut microbiome of companion animals is relatively underexplored, despite its relevance to animal health, pet owner health, and basic microbial community biology. Here, we provide the most comprehensive analysis of the canine and feline gut microbiomes to date, incorporating 2639 stool shotgun metagenomes (2272 dog and 367 cat) spanning 14 publicly available datasets (n = 730) and 8 new study populations (n = 1909). These are compared with 238 and 112 baseline human gut metagenomes from the Human Microbiome Project 1-II and a traditionally living Malagasy cohort, respectively, processed in a manner identical to the animal metagenomes. All microbiomes were characterized using reference-based taxonomic and functional profiling, as well as de novo assembly yielding metagenomic assembled genomes clustered into species-level genome bins. Companion animals shared 184 species-level genome bins not found in humans, whereas 198 were found in all three hosts. We applied novel methodology to distinguish strains of these shared organisms either transferred or unique to host species, with phylogenetic patterns suggesting host-specific adaptation of microbial lineages. This corresponded with functional divergence of these lineages by host (e.g., differences in metabolic and antibiotic resistance genes) likely important to companion animal health. This study provides the largest resource to date of companion animal gut metagenomes and greatly contributes to our understanding of the “One Health” concept of a shared microbial environment among humans and companion animals, affecting infectious diseases, immune response, and specific genetic elements.
{"title":"Comprehensive profile of the companion animal gut microbiome integrating reference-based and reference-free methods","authors":"Tobyn Branck, Zhiji Hu, William A Nickols, Aaron M Walsh, Amrisha Bhosle, Meghan I Short, Jacob T Nearing, Francesco Asnicar, Lauren J McIver, Sagun Maharjan, Ali Rahnavard, Artemis Louyakis, Dayakar V Badri, Christoph Brockel, Kelsey N Thompson, Curtis Huttenhower","doi":"10.1093/ismejo/wrae201","DOIUrl":"https://doi.org/10.1093/ismejo/wrae201","url":null,"abstract":"The gut microbiome of companion animals is relatively underexplored, despite its relevance to animal health, pet owner health, and basic microbial community biology. Here, we provide the most comprehensive analysis of the canine and feline gut microbiomes to date, incorporating 2639 stool shotgun metagenomes (2272 dog and 367 cat) spanning 14 publicly available datasets (n = 730) and 8 new study populations (n = 1909). These are compared with 238 and 112 baseline human gut metagenomes from the Human Microbiome Project 1-II and a traditionally living Malagasy cohort, respectively, processed in a manner identical to the animal metagenomes. All microbiomes were characterized using reference-based taxonomic and functional profiling, as well as de novo assembly yielding metagenomic assembled genomes clustered into species-level genome bins. Companion animals shared 184 species-level genome bins not found in humans, whereas 198 were found in all three hosts. We applied novel methodology to distinguish strains of these shared organisms either transferred or unique to host species, with phylogenetic patterns suggesting host-specific adaptation of microbial lineages. This corresponded with functional divergence of these lineages by host (e.g., differences in metabolic and antibiotic resistance genes) likely important to companion animal health. This study provides the largest resource to date of companion animal gut metagenomes and greatly contributes to our understanding of the “One Health” concept of a shared microbial environment among humans and companion animals, affecting infectious diseases, immune response, and specific genetic elements.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"229 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142430429","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}
Cristina M Alcaraz, Joana Séneca, Martin Kunert, Christopher Pree, Marta Sudo, Jillian M Petersen
Like many marine invertebrates, marine lucinid clams have an intimate relationship with beneficial sulfur-oxidizing bacteria located within specialized gill cells known as bacteriocytes. Most previous research has focused on the symbionts in the gills of these (and other) symbiotic bivalves, often assuming that the symbionts only persistently colonize the gills, at least in the adult stage. We used 16S rRNA gene sequencing and digital polymerase chain reaction with symbiont-specific primers targeting the soxB gene on the foot, mantle, visceral mass, and gills of the lucinid clam Loripes orbiculatus. We also used fluorescence in situ hybridization with symbiont-specific probes to examine symbiont distribution at the level of the whole holobiont. Despite 40 years of research on these symbioses, we detected previously unknown populations of symbiont cells in several organs, including the digestive tract. As in the well-studied gills, symbionts in the digestive tract may be housed within host cells. A 14-month starvation experiment without hydrogen sulfide to power symbiont metabolism caused a larger reduction in symbiont numbers in the gills compared to the visceral mass, raising the possibility that symbionts in the digestive tract are persistent and may have a distinct physiology and role in the symbiosis compared with the gill symbionts. Our results highlight the unexpectedly complex relationships between marine lucinid clams and their symbionts and challenge the view that chemosynthetic symbionts are restricted to the gills of these hosts.
{"title":"Sulfur-oxidizing symbionts colonize the digestive tract of their Lucinid hosts","authors":"Cristina M Alcaraz, Joana Séneca, Martin Kunert, Christopher Pree, Marta Sudo, Jillian M Petersen","doi":"10.1093/ismejo/wrae200","DOIUrl":"https://doi.org/10.1093/ismejo/wrae200","url":null,"abstract":"Like many marine invertebrates, marine lucinid clams have an intimate relationship with beneficial sulfur-oxidizing bacteria located within specialized gill cells known as bacteriocytes. Most previous research has focused on the symbionts in the gills of these (and other) symbiotic bivalves, often assuming that the symbionts only persistently colonize the gills, at least in the adult stage. We used 16S rRNA gene sequencing and digital polymerase chain reaction with symbiont-specific primers targeting the soxB gene on the foot, mantle, visceral mass, and gills of the lucinid clam Loripes orbiculatus. We also used fluorescence in situ hybridization with symbiont-specific probes to examine symbiont distribution at the level of the whole holobiont. Despite 40 years of research on these symbioses, we detected previously unknown populations of symbiont cells in several organs, including the digestive tract. As in the well-studied gills, symbionts in the digestive tract may be housed within host cells. A 14-month starvation experiment without hydrogen sulfide to power symbiont metabolism caused a larger reduction in symbiont numbers in the gills compared to the visceral mass, raising the possibility that symbionts in the digestive tract are persistent and may have a distinct physiology and role in the symbiosis compared with the gill symbionts. Our results highlight the unexpectedly complex relationships between marine lucinid clams and their symbionts and challenge the view that chemosynthetic symbionts are restricted to the gills of these hosts.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"26 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142405075","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}
Katarina Belcijan Pandur, Barbara Kraigher, Ana Tomac, Polonca Stefanic, Ines Mandic Mulec
Cooperative behaviors in human, animal, and even microbial societies are vulnerable to exploitation. Kin discrimination has been hypothesized to help stabilize cooperation. However, the mechanisms that sustain cooperative behavior remain poorly understood. Here, we investigate the role of kin discrimination in limiting the spread of cheats in adjoining populations during surfactant dependent cooperative swarming over surfaces using the bacterium Bacillus subtilis as a model organism. We show that mixing surfactant secreting cooperators and cheats that do not produce surfactants at 1:1 initial ratio quickly leads to cooperation collapse. However, when such common swarms encounter non-kin B. subtilis swarms, the proportion of the surfactant non-producers decreases, suggesting that kinship dependent interactions may limit cheats’ advantage in an adjoining population. To further validate this finding, we subjected wild-type cooperators to multiple transient encounters with kin and non-kin swarms over 20 cycles of experimental evolution. The evolved populations exposed to non-kin swarms less frequently contained defective swarming phenotypes compared to those encountering kin swarms. Altogether, our results support the prediction that the spread of cheats in an adjoining bacterial population is impeded by kin discrimination interactions which might have a role in stabilizing cooperative behavior in evolving populations.
{"title":"Non-kin interactions between Bacillus subtilis soil isolates limit the spread of swarming deficient cheats","authors":"Katarina Belcijan Pandur, Barbara Kraigher, Ana Tomac, Polonca Stefanic, Ines Mandic Mulec","doi":"10.1093/ismejo/wrae199","DOIUrl":"https://doi.org/10.1093/ismejo/wrae199","url":null,"abstract":"Cooperative behaviors in human, animal, and even microbial societies are vulnerable to exploitation. Kin discrimination has been hypothesized to help stabilize cooperation. However, the mechanisms that sustain cooperative behavior remain poorly understood. Here, we investigate the role of kin discrimination in limiting the spread of cheats in adjoining populations during surfactant dependent cooperative swarming over surfaces using the bacterium Bacillus subtilis as a model organism. We show that mixing surfactant secreting cooperators and cheats that do not produce surfactants at 1:1 initial ratio quickly leads to cooperation collapse. However, when such common swarms encounter non-kin B. subtilis swarms, the proportion of the surfactant non-producers decreases, suggesting that kinship dependent interactions may limit cheats’ advantage in an adjoining population. To further validate this finding, we subjected wild-type cooperators to multiple transient encounters with kin and non-kin swarms over 20 cycles of experimental evolution. The evolved populations exposed to non-kin swarms less frequently contained defective swarming phenotypes compared to those encountering kin swarms. Altogether, our results support the prediction that the spread of cheats in an adjoining bacterial population is impeded by kin discrimination interactions which might have a role in stabilizing cooperative behavior in evolving populations.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"225 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142384469","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}
Cao Zheng, Dingqi Liu, Xinyu Lu, Huijun Wu, Jingyi Hua, Chuang Zhang, Kang Liu, Changchun Li, Jin He, Cuiying Du
The ability of bacteria to use natural carbon sources greatly affects their growth and survival in the environment. Bacteria have evolved versatile abilities to use environmental carbon sources, but their diversity and assimilation pathways remain largely unexplored. Trans-aconitic acid, a geometric isomer of cis-aconitic acid involved in the tricarboxylic acid cycle, has long been considered a natural carbon source metabolizable by bacteria. However, its catabolism and ecological role in linking bacterial interactions with the environments remain unclear. Here, we identify a regulatory system in Bacillus velezensis FZB42 that is capable of sensing and catabolizing trans-aconitic acid. The system consists of a tar operon, an adjacent positive regulatory gene tarR, and a shared promoter. After receiving the trans-aconitic acid signal, the TarR protein interacts directly with the promoter, initiating the expression of the membrane transporter TarB and aconitate isomerase TarA encoded by the operon, which function in importing the trans-aconitic acid and isomerizing it into the central intermediate cis-aconitic acid. Subsequent soil colonization experiments reveal that trans-aconitic acid assimilating ability can give its coding bacteria a growth and competitive advantage. Bioinformatics analyses coupled with bacterial isolation experiments further show that the assimilation system of trans-aconitic acid is widely distributed in the bacterial domain, and its assimilating bacteria also extensively distributed in nature, indicating an important role of trans-aconitic acid metabolism in bacterial carbon acquisition. This work emphasizes the importance of metabolic adaptation to environmental carbon sources for bacterial survival and may provide inspiration for engineering microbes with enhanced environmental competitiveness.
{"title":"Trans-aconitic acid assimilation system as a widespread bacterial mechanism for environmental adaptation","authors":"Cao Zheng, Dingqi Liu, Xinyu Lu, Huijun Wu, Jingyi Hua, Chuang Zhang, Kang Liu, Changchun Li, Jin He, Cuiying Du","doi":"10.1093/ismejo/wrae198","DOIUrl":"https://doi.org/10.1093/ismejo/wrae198","url":null,"abstract":"The ability of bacteria to use natural carbon sources greatly affects their growth and survival in the environment. Bacteria have evolved versatile abilities to use environmental carbon sources, but their diversity and assimilation pathways remain largely unexplored. Trans-aconitic acid, a geometric isomer of cis-aconitic acid involved in the tricarboxylic acid cycle, has long been considered a natural carbon source metabolizable by bacteria. However, its catabolism and ecological role in linking bacterial interactions with the environments remain unclear. Here, we identify a regulatory system in Bacillus velezensis FZB42 that is capable of sensing and catabolizing trans-aconitic acid. The system consists of a tar operon, an adjacent positive regulatory gene tarR, and a shared promoter. After receiving the trans-aconitic acid signal, the TarR protein interacts directly with the promoter, initiating the expression of the membrane transporter TarB and aconitate isomerase TarA encoded by the operon, which function in importing the trans-aconitic acid and isomerizing it into the central intermediate cis-aconitic acid. Subsequent soil colonization experiments reveal that trans-aconitic acid assimilating ability can give its coding bacteria a growth and competitive advantage. Bioinformatics analyses coupled with bacterial isolation experiments further show that the assimilation system of trans-aconitic acid is widely distributed in the bacterial domain, and its assimilating bacteria also extensively distributed in nature, indicating an important role of trans-aconitic acid metabolism in bacterial carbon acquisition. This work emphasizes the importance of metabolic adaptation to environmental carbon sources for bacterial survival and may provide inspiration for engineering microbes with enhanced environmental competitiveness.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"70 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142384687","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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