James S Weagley, Luis Alberto Chica Cárdenas, Ana Romani, Meagan E Sullender, Somya Aggarwal, Heyde Makimaa, Michael P Hogarty, Rachel Rodgers, Elizabeth A Kennedy, Lynne Foster, Lawrence A Schriefer, Megan T Baldridge
Mouse models are vital tools for discerning the relative contributions of host and microbial genetics to disease, often requiring the transfer of microbiota between different mouse strains. Transfer methods include antibiotic treatment of recipients and colonization using either co-housing with donors or the transplantation of faecal or caecal donor material. However, the efficiency and dynamics of these methods in reconstituting recipients with donor microbes is not well understood. We thus directly compared co-housing, faecal transplantation, and caecal transplantation methods. Donor mice from Taconic Biosciences, possessing distinct microbial communities, served as the microbial source for recipient mice from Jackson Laboratories, which were treated with antibiotics to disrupt their native microbiota. We monitored bacterial and viral populations longitudinally over the course of antibiotics treatment and reconstitution using 16S rRNA gene sequencing, quantitative PCR, and shotgun sequencing of viral-like particles. As expected, antibiotic treatment rapidly depleted microbial biomass and diversity, with slow and incomplete natural recovery of the microbiota in non-transfer-recipient control mice. Although all transfer methods reconstituted recipient mice with donor microbiota, co-housing achieved this more rapidly for both bacterial and viral communities. Overall, faecal and caecal transplant resulted in highly similar colonization processes with some minor variation in enrichment for two specific bacterial families. This study provides valuable insights into microbial ecology, as well as the dynamics underlying experimental microbial transfer methods, enhancing reproducibility and informing best practices for microbiota transfer in mouse models.
{"title":"Differential Microbial Community Assembly Following Co-housing versus Microbiota Transplant","authors":"James S Weagley, Luis Alberto Chica Cárdenas, Ana Romani, Meagan E Sullender, Somya Aggarwal, Heyde Makimaa, Michael P Hogarty, Rachel Rodgers, Elizabeth A Kennedy, Lynne Foster, Lawrence A Schriefer, Megan T Baldridge","doi":"10.1093/ismejo/wraf256","DOIUrl":"https://doi.org/10.1093/ismejo/wraf256","url":null,"abstract":"Mouse models are vital tools for discerning the relative contributions of host and microbial genetics to disease, often requiring the transfer of microbiota between different mouse strains. Transfer methods include antibiotic treatment of recipients and colonization using either co-housing with donors or the transplantation of faecal or caecal donor material. However, the efficiency and dynamics of these methods in reconstituting recipients with donor microbes is not well understood. We thus directly compared co-housing, faecal transplantation, and caecal transplantation methods. Donor mice from Taconic Biosciences, possessing distinct microbial communities, served as the microbial source for recipient mice from Jackson Laboratories, which were treated with antibiotics to disrupt their native microbiota. We monitored bacterial and viral populations longitudinally over the course of antibiotics treatment and reconstitution using 16S rRNA gene sequencing, quantitative PCR, and shotgun sequencing of viral-like particles. As expected, antibiotic treatment rapidly depleted microbial biomass and diversity, with slow and incomplete natural recovery of the microbiota in non-transfer-recipient control mice. Although all transfer methods reconstituted recipient mice with donor microbiota, co-housing achieved this more rapidly for both bacterial and viral communities. Overall, faecal and caecal transplant resulted in highly similar colonization processes with some minor variation in enrichment for two specific bacterial families. This study provides valuable insights into microbial ecology, as well as the dynamics underlying experimental microbial transfer methods, enhancing reproducibility and informing best practices for microbiota transfer in mouse models.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"217 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145531733","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}
François Maillard, Fredrik Klinghammer, Briana H Beatty, Hanbang Zou, Enrique Lara, Edith C Hammer, Anders Tunlid, Peter G Kennedy
The keystone species concept holds that certain members of an ecological community, despite their low abundance, exert disproportionately large effects on species diversity and composition. In microbial ecology, experimental validation of this concept has been limited because targeted removal of individual species remains technically challenging. Here, we developed a procedure to test the keystone species concept within a soil microbial food web by selectively suppressing a protist predator at the microscale via UV-induced phototoxicity in a microfluidic soil chip system. We targeted a hypotrich ciliate (subclass Hypotrichia), and combined microscopy with high-throughput amplicon sequencing of microbial taxonomic markers to assess, across multiple trophic levels, how its suppression affected microbial community abundance, diversity, and composition. Over the 20-day incubation, the chip system supported complex communities of bacteria, fungi, and protists. Following Hypotrichia suppression, two distinct ecological responses were observed: first, an increase in the relative abundance of flagellates, consistent with mesopredator release, accompanied by a significant rise in overall protist diversity; second, a convergence in protist community composition, indicative of biotic homogenization. Bacterial community abundance, richness, and composition remained unchanged, likely due to compensatory predation from a relative increase in bacterivorous flagellates. In contrast, fungal diversity decreased, presumably because the altered protist community favored facultative fungal consumers. Collectively, these findings provide direct experimental evidence that low abundance microbial predators can function as keystone species, modulating predator community composition and diversity, and exerting cascading effects on lower trophic levels within microbial brown food webs.
{"title":"Keystone protist suppression triggers mesopredator release and biotic homogenization in complex soil microbial communities","authors":"François Maillard, Fredrik Klinghammer, Briana H Beatty, Hanbang Zou, Enrique Lara, Edith C Hammer, Anders Tunlid, Peter G Kennedy","doi":"10.1093/ismejo/wraf253","DOIUrl":"https://doi.org/10.1093/ismejo/wraf253","url":null,"abstract":"The keystone species concept holds that certain members of an ecological community, despite their low abundance, exert disproportionately large effects on species diversity and composition. In microbial ecology, experimental validation of this concept has been limited because targeted removal of individual species remains technically challenging. Here, we developed a procedure to test the keystone species concept within a soil microbial food web by selectively suppressing a protist predator at the microscale via UV-induced phototoxicity in a microfluidic soil chip system. We targeted a hypotrich ciliate (subclass Hypotrichia), and combined microscopy with high-throughput amplicon sequencing of microbial taxonomic markers to assess, across multiple trophic levels, how its suppression affected microbial community abundance, diversity, and composition. Over the 20-day incubation, the chip system supported complex communities of bacteria, fungi, and protists. Following Hypotrichia suppression, two distinct ecological responses were observed: first, an increase in the relative abundance of flagellates, consistent with mesopredator release, accompanied by a significant rise in overall protist diversity; second, a convergence in protist community composition, indicative of biotic homogenization. Bacterial community abundance, richness, and composition remained unchanged, likely due to compensatory predation from a relative increase in bacterivorous flagellates. In contrast, fungal diversity decreased, presumably because the altered protist community favored facultative fungal consumers. Collectively, these findings provide direct experimental evidence that low abundance microbial predators can function as keystone species, modulating predator community composition and diversity, and exerting cascading effects on lower trophic levels within microbial brown food webs.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"46 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145509318","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}
Andrew Wilson, Elise Van Fossen, Ritu Shrestha, Andrew Frank, Valentine Trotter, Henri Baldino, Brenton Poirier, Young-Mo Kim, William Nelson, Tuesday Simmons, Devin Coleman-Derr, Adam Deutschbauer, Robert Egbert, Joshua Elmore
Microbial nitrification of fertilizers represents is a significant global source of greenhouse gas emissions. This process increases emissions, fosters toxic algal blooms, and raises crop production costs. Some plants naturally release biological nitrification inhibitors to suppress ammonium-oxidizing microbes and reduce nitrification. Engineering nitrification inhibitor production into food and bioenergy crops via synthetic biology offers a promising mitigation strategy, but its success depends on addressing gaps in our understanding of inhibitor degradation in soil. This study begins to fill this gap by identifying a previously unknown microbial pathway for degrading phenylpropanoid methyl esters, a key class of aromatic nitrification inhibitors. Using transcriptomics and high-throughput functional genomics, we discovered genes essential for phenylpropanoid methyl ester degradation. Genetic and biochemical analyses revealed two novel enzymes, including a newly identified phenylpropanoid methyl esterase, that direct phenylpropanoid methyl esters into known metabolic pathways. Importantly, transferring these genes into bacteria capable of metabolizing other phenylpropanoids enabled them to use the methyl esters as a carbon source. This work provides critical insights into microbial nitrification inhibitor degradation, a poorly understood element of the nitrification cycle.
{"title":"Phenylpropanoid methyl esterase unlocks catabolism of aromatic biological nitrification inhibitors","authors":"Andrew Wilson, Elise Van Fossen, Ritu Shrestha, Andrew Frank, Valentine Trotter, Henri Baldino, Brenton Poirier, Young-Mo Kim, William Nelson, Tuesday Simmons, Devin Coleman-Derr, Adam Deutschbauer, Robert Egbert, Joshua Elmore","doi":"10.1093/ismejo/wraf251","DOIUrl":"https://doi.org/10.1093/ismejo/wraf251","url":null,"abstract":"Microbial nitrification of fertilizers represents is a significant global source of greenhouse gas emissions. This process increases emissions, fosters toxic algal blooms, and raises crop production costs. Some plants naturally release biological nitrification inhibitors to suppress ammonium-oxidizing microbes and reduce nitrification. Engineering nitrification inhibitor production into food and bioenergy crops via synthetic biology offers a promising mitigation strategy, but its success depends on addressing gaps in our understanding of inhibitor degradation in soil. This study begins to fill this gap by identifying a previously unknown microbial pathway for degrading phenylpropanoid methyl esters, a key class of aromatic nitrification inhibitors. Using transcriptomics and high-throughput functional genomics, we discovered genes essential for phenylpropanoid methyl ester degradation. Genetic and biochemical analyses revealed two novel enzymes, including a newly identified phenylpropanoid methyl esterase, that direct phenylpropanoid methyl esters into known metabolic pathways. Importantly, transferring these genes into bacteria capable of metabolizing other phenylpropanoids enabled them to use the methyl esters as a carbon source. This work provides critical insights into microbial nitrification inhibitor degradation, a poorly understood element of the nitrification cycle.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"52 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145498445","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}
Host-bacteria symbioses are often specific and transgenerationaly stable. In hosts that acquire their symbionts from the environment across successive generations, selective mechanisms are required to identify and maintain beneficial partners from diverse environmental microorganisms. In Coreoidea stinkbugs, which house environmentally acquired symbionts in a specialized midgut region, bacterial competition plays a key role in shaping symbiont specificity whereby Caballeronia strains consistently outcompete bacteria of other genera. Here, we show that competition within the gut also occurs among Caballeronia strains themselves, driving specificity at a finer taxonomic scale. Specifically, the stinkbugs Riptortus pedestris and Coreus marginatus, when reared on the same soil sample, preferentially select for α- and β-subclade Caballeronia, respectively. Using a gnotobiotic infection system, we demonstrate that representative strains from the α-, β-, and γ-subclades can independently colonize the midgut of both insect species in monoculture. However, in pairwise co-culture infections, each host exhibits a marked selectivity for either α- or β-subclade strains, consistent with patterns observed in the soil inoculation experiment. In R. pedestris, we further find that interspecies competition outcomes are shaped by both priority effects and displacement mechanisms. At the molecular level, differences among symbionts in metabolic capabilities, resistance to antimicrobial peptides, and chemotactic behavior influence their competitive success in the gut. Finally, we show that in R. pedestris, the reproductive fitness benefits conferred by the symbiosis align with the observed strain specificity in the tested strain panel, suggesting a functional link between symbiont selection and host fitness, despite these processes occurring at distinct stages of the symbiotic relationship. Our findings highlight that the gut in Coreoidea species constitutes a multifactorial, species-specific selective environment that contributes to the colonization of the symbiotic midgut region by the best-adapted Caballeronia strain.
{"title":"Strict gut symbiont specificity in Coreoidea insects governed by interspecies competition within Caballeronia strains","authors":"Gaelle Lextrait, Srotoswini Joardar, Raynald Cossard, Yoshitomo Kikuchi, Tsubasa Ohbayashi, Peter Mergaert","doi":"10.1093/ismejo/wraf240","DOIUrl":"https://doi.org/10.1093/ismejo/wraf240","url":null,"abstract":"Host-bacteria symbioses are often specific and transgenerationaly stable. In hosts that acquire their symbionts from the environment across successive generations, selective mechanisms are required to identify and maintain beneficial partners from diverse environmental microorganisms. In Coreoidea stinkbugs, which house environmentally acquired symbionts in a specialized midgut region, bacterial competition plays a key role in shaping symbiont specificity whereby Caballeronia strains consistently outcompete bacteria of other genera. Here, we show that competition within the gut also occurs among Caballeronia strains themselves, driving specificity at a finer taxonomic scale. Specifically, the stinkbugs Riptortus pedestris and Coreus marginatus, when reared on the same soil sample, preferentially select for α- and β-subclade Caballeronia, respectively. Using a gnotobiotic infection system, we demonstrate that representative strains from the α-, β-, and γ-subclades can independently colonize the midgut of both insect species in monoculture. However, in pairwise co-culture infections, each host exhibits a marked selectivity for either α- or β-subclade strains, consistent with patterns observed in the soil inoculation experiment. In R. pedestris, we further find that interspecies competition outcomes are shaped by both priority effects and displacement mechanisms. At the molecular level, differences among symbionts in metabolic capabilities, resistance to antimicrobial peptides, and chemotactic behavior influence their competitive success in the gut. Finally, we show that in R. pedestris, the reproductive fitness benefits conferred by the symbiosis align with the observed strain specificity in the tested strain panel, suggesting a functional link between symbiont selection and host fitness, despite these processes occurring at distinct stages of the symbiotic relationship. Our findings highlight that the gut in Coreoidea species constitutes a multifactorial, species-specific selective environment that contributes to the colonization of the symbiotic midgut region by the best-adapted Caballeronia strain.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"56 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145498475","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}
Carolyn A Miller, Enrico Pirotta, Sharon Grim, Michael J Moore, John W Durban, Peter L Tyack, Holly Fearnbach, Samantha G M Leander, Amy R Knowlton, Amy M Warren, Monica A Zani, Regina Asmutis-Silvia, Heather M Pettis, Amy Apprill
As important members of the marine ecosystem, baleen whales are frequently managed and protected, but methodology to assess their health remains limited. Recent technological advances, such as the use of drones, support the non-invasive collection of promising health-associated data, including respiratory exhalant microbiota. Here, we considered five health metrics paired with respiratory exhalant samples to examine the utility of characterizing respiratory microorganisms for health diagnostics of North Atlantic right whales (Eubalaena glacialis), one of the most endangered baleen whale species. In 2016–2024, we used drones to collect 103 exhalant samples from 85 individuals to examine the associated microbiome, using amplicon sequencing methods targeting bacteria and archaea. The health status of sampled whales was characterized using an index of body condition derived from full-body vertical drone images, three qualitative assessments obtained from photo-identification imagery, and an existing health and vital rates model. Using an elastic net penalized regression approach, we demonstrate significant relationships between these health metrics and respiratory-associated microorganisms. Bacterial taxa that significantly contributed to the model for the body condition index differed between the thinnest and most robust males in the dataset. The thin whale harbored taxa belonging to the same genus as mammalian pathogens, Clostridium and Peptoniphilus, whereas the robust whale harbored taxa commonly observed in lipid-rich environments, Sediminispirochaeta and Candidatus Gracilibacteria. These differences warrant further investigation into the mechanisms by which bacteria contribute to whale health. Our findings demonstrate the utility of non-invasive multi-metric health models that include respiratory exhalant microbiota for whale health assessment and management.
{"title":"Respiratory microbiomes reflect whale health","authors":"Carolyn A Miller, Enrico Pirotta, Sharon Grim, Michael J Moore, John W Durban, Peter L Tyack, Holly Fearnbach, Samantha G M Leander, Amy R Knowlton, Amy M Warren, Monica A Zani, Regina Asmutis-Silvia, Heather M Pettis, Amy Apprill","doi":"10.1093/ismejo/wraf231","DOIUrl":"https://doi.org/10.1093/ismejo/wraf231","url":null,"abstract":"As important members of the marine ecosystem, baleen whales are frequently managed and protected, but methodology to assess their health remains limited. Recent technological advances, such as the use of drones, support the non-invasive collection of promising health-associated data, including respiratory exhalant microbiota. Here, we considered five health metrics paired with respiratory exhalant samples to examine the utility of characterizing respiratory microorganisms for health diagnostics of North Atlantic right whales (Eubalaena glacialis), one of the most endangered baleen whale species. In 2016–2024, we used drones to collect 103 exhalant samples from 85 individuals to examine the associated microbiome, using amplicon sequencing methods targeting bacteria and archaea. The health status of sampled whales was characterized using an index of body condition derived from full-body vertical drone images, three qualitative assessments obtained from photo-identification imagery, and an existing health and vital rates model. Using an elastic net penalized regression approach, we demonstrate significant relationships between these health metrics and respiratory-associated microorganisms. Bacterial taxa that significantly contributed to the model for the body condition index differed between the thinnest and most robust males in the dataset. The thin whale harbored taxa belonging to the same genus as mammalian pathogens, Clostridium and Peptoniphilus, whereas the robust whale harbored taxa commonly observed in lipid-rich environments, Sediminispirochaeta and Candidatus Gracilibacteria. These differences warrant further investigation into the mechanisms by which bacteria contribute to whale health. Our findings demonstrate the utility of non-invasive multi-metric health models that include respiratory exhalant microbiota for whale health assessment and management.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145478420","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}
Hylke H Kortenbosch, Bo Briggeman, Francisca Reyes Marquez, Ben Auxier, Sytze de Bruin, Bas J Zwaan, Eveline Snelders
Humans are exposed to the mould Aspergillus fumigatus via inhalation, and infections are increasingly resistant to triazole-class antifungals. Ecologically, this fungus is a ubiquitous saprotroph found in terrestrial environments. Although triazole-resistant A. fumigatus is found in large quantities in specific agricultural environments; it is not clear how much these contribute to the overall exposure of individuals to antifungal resistance. Triazoles are also used to protect a wide range of products unrelated to agriculture, and therefore, it could not be excluded that the resistance observed in agricultural settings may be the result of selection beyond agricultural sources. In the case of A. fumigatus genomics cannot reliably link resistant isolates to specific environmental sources. Therefore, we used a spatial sampling approach to measure population trends in triazole resistance. We conducted a large-scale, unbiased air sampling throughout the Netherlands using a citizen science approach. We find that $sim $4$%$ of over 60K screened colonies are resistant to clinical triazoles. Modelling resistance data with spatial land-use data shows that agricultural land use, particularly flower bulbs and greenhouses, can predict peaks in antifungal resistance in airborne A. fumigatus in the Netherlands. Furthermore, genotyping resistant isolates suggests land-use-associated niche differentiation between two dominant resistance haplotypes, with only one of the two showing a significant association with agricultural land use. By linking triazole resistance to land use, this work informs necessary policy-driven changes to reduce human exposure to antifungal-resistant A. fumigatus, and suggests that similar spatial patterns in antifungal resistance may occur in other agriculture-associated fungi as well.
{"title":"Land use drives drug resistance in an airborne human fungal pathogen","authors":"Hylke H Kortenbosch, Bo Briggeman, Francisca Reyes Marquez, Ben Auxier, Sytze de Bruin, Bas J Zwaan, Eveline Snelders","doi":"10.1093/ismejo/wraf246","DOIUrl":"https://doi.org/10.1093/ismejo/wraf246","url":null,"abstract":"Humans are exposed to the mould Aspergillus fumigatus via inhalation, and infections are increasingly resistant to triazole-class antifungals. Ecologically, this fungus is a ubiquitous saprotroph found in terrestrial environments. Although triazole-resistant A. fumigatus is found in large quantities in specific agricultural environments; it is not clear how much these contribute to the overall exposure of individuals to antifungal resistance. Triazoles are also used to protect a wide range of products unrelated to agriculture, and therefore, it could not be excluded that the resistance observed in agricultural settings may be the result of selection beyond agricultural sources. In the case of A. fumigatus genomics cannot reliably link resistant isolates to specific environmental sources. Therefore, we used a spatial sampling approach to measure population trends in triazole resistance. We conducted a large-scale, unbiased air sampling throughout the Netherlands using a citizen science approach. We find that $sim $4$%$ of over 60K screened colonies are resistant to clinical triazoles. Modelling resistance data with spatial land-use data shows that agricultural land use, particularly flower bulbs and greenhouses, can predict peaks in antifungal resistance in airborne A. fumigatus in the Netherlands. Furthermore, genotyping resistant isolates suggests land-use-associated niche differentiation between two dominant resistance haplotypes, with only one of the two showing a significant association with agricultural land use. By linking triazole resistance to land use, this work informs necessary policy-driven changes to reduce human exposure to antifungal-resistant A. fumigatus, and suggests that similar spatial patterns in antifungal resistance may occur in other agriculture-associated fungi as well.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"28 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145472858","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 human nasal microbiome can serve as a reservoir for pathogens. In particular, the opportunistic pathogen Staphylococcus aureus can be a member of the nasal microbiome increasing the risk of subsequent infections. The nasal carriage of S. aureus is known to be positively and negatively impacted by non-pathogenic species, suggesting interactions between the pathogen and commensals, but the underlying molecular mechanism remains largely unclear. Herein we demonstrate that S. aureus competes with nasal commensals for the coenzyme biotin. Biotin is crucial for all living organisms and we show that depletion of biotin impairs S. aureus growth and membrane integrity. We found the nasal cavity to be a biotin-limited environment, suggesting competition for the coenzyme within the microbiome. For some nasal commensals and S. aureus, we observed biotin prototrophy and all strains released biotin into the environment. In contrast, other commensals and especially coagulase-negative staphylococci (CoNS) were found to be biotin auxotrophs and strongly reliant on prototrophic strains under biotin-limited conditions. We show that high-affinity biotin uptake systems are used by prototrophic and auxotrophic strains alike and represent crucial factors to optimize competitive fitness of species in co-culture. Together, our data show that biotin-mediated interactions occur between the species of the human nasal microbiome and provide evidence for interspecies competition and co-dependency.
{"title":"Competitive fitness of Staphylococcus aureus against nasal commensals depends on biotin biosynthesis and acquisition.","authors":"Kevser Bilici,David Gerlach,Laura Camus,Simon Heilbronner","doi":"10.1093/ismejo/wraf248","DOIUrl":"https://doi.org/10.1093/ismejo/wraf248","url":null,"abstract":"The human nasal microbiome can serve as a reservoir for pathogens. In particular, the opportunistic pathogen Staphylococcus aureus can be a member of the nasal microbiome increasing the risk of subsequent infections. The nasal carriage of S. aureus is known to be positively and negatively impacted by non-pathogenic species, suggesting interactions between the pathogen and commensals, but the underlying molecular mechanism remains largely unclear. Herein we demonstrate that S. aureus competes with nasal commensals for the coenzyme biotin. Biotin is crucial for all living organisms and we show that depletion of biotin impairs S. aureus growth and membrane integrity. We found the nasal cavity to be a biotin-limited environment, suggesting competition for the coenzyme within the microbiome. For some nasal commensals and S. aureus, we observed biotin prototrophy and all strains released biotin into the environment. In contrast, other commensals and especially coagulase-negative staphylococci (CoNS) were found to be biotin auxotrophs and strongly reliant on prototrophic strains under biotin-limited conditions. We show that high-affinity biotin uptake systems are used by prototrophic and auxotrophic strains alike and represent crucial factors to optimize competitive fitness of species in co-culture. Together, our data show that biotin-mediated interactions occur between the species of the human nasal microbiome and provide evidence for interspecies competition and co-dependency.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"85 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145440831","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}
Microbial communities are crucial in host adaptation to stressors, particularly in dynamic ecosystems. In aquatic environments, Daphnia magna is ideal for studying host-microbiome interactions due to its ecological importance and sensitivity. Adaptation to toxins, such as those produced by cyanobacteria, may involve both host and microbial gene repertoires. Yet, the influence of microbiota composition and function on host performance remains poorly understood. Because epigenetic mechanisms such as DNA methylation regulate gene expression and mediate adaptive responses, we also investigated whether these associations are reflected in DNA methylation levels. To address this, we conducted a fully factorial transplant experiment using microbiota-depleted Daphnia colonised with microbiota from the same or different genotype, previously exposed to toxic or non-toxic diets, or left uncolonised. We assessed life-history traits, microbial composition (16S rRNA genes), functional profiles (whole-genome-resequencing), and DNA methylation (colorimetric quantification). Daphnia fed non-toxic diets grew larger and reproduced more. Increased methylation occurred when microbiota donors differed from the host genotype and was strongest under toxic diet. Dysbiosis and reduced performance were noted in individuals colonised with toxic-diet microbiota from another genotype, where Limnohabitans spp. was reduced or absent. Signs of hormesis emerged when Daphnia received microbiota from their own genotype reared on non-toxic diets. DNA methylation of both host and microbiota was associated with functional pathways, including increased mitochondrial fatty acid biosynthesis. These findings highlight the importance of host-microbiota matching and microbial environmental history in shaping host performance and epigenetic responses, emphasizing the need to consider host-microbe-environment interactions in evolutionary and ecological studies.
{"title":"Host-microbiota matching and epigenetic modulation drive Daphnia magna responses to cyanobacterial stress.","authors":"Karen Bisschop,Naina Goel,Manon Coone,Isabel Vanoverberghe,Anna Greffe,Jana Asselman,Ellen Decaestecker","doi":"10.1093/ismejo/wraf247","DOIUrl":"https://doi.org/10.1093/ismejo/wraf247","url":null,"abstract":"Microbial communities are crucial in host adaptation to stressors, particularly in dynamic ecosystems. In aquatic environments, Daphnia magna is ideal for studying host-microbiome interactions due to its ecological importance and sensitivity. Adaptation to toxins, such as those produced by cyanobacteria, may involve both host and microbial gene repertoires. Yet, the influence of microbiota composition and function on host performance remains poorly understood. Because epigenetic mechanisms such as DNA methylation regulate gene expression and mediate adaptive responses, we also investigated whether these associations are reflected in DNA methylation levels. To address this, we conducted a fully factorial transplant experiment using microbiota-depleted Daphnia colonised with microbiota from the same or different genotype, previously exposed to toxic or non-toxic diets, or left uncolonised. We assessed life-history traits, microbial composition (16S rRNA genes), functional profiles (whole-genome-resequencing), and DNA methylation (colorimetric quantification). Daphnia fed non-toxic diets grew larger and reproduced more. Increased methylation occurred when microbiota donors differed from the host genotype and was strongest under toxic diet. Dysbiosis and reduced performance were noted in individuals colonised with toxic-diet microbiota from another genotype, where Limnohabitans spp. was reduced or absent. Signs of hormesis emerged when Daphnia received microbiota from their own genotype reared on non-toxic diets. DNA methylation of both host and microbiota was associated with functional pathways, including increased mitochondrial fatty acid biosynthesis. These findings highlight the importance of host-microbiota matching and microbial environmental history in shaping host performance and epigenetic responses, emphasizing the need to consider host-microbe-environment interactions in evolutionary and ecological studies.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"112 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145433853","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Xuhui Huang,Emily E Chase,Brittany N Zepernick,Robbie M Martin,Lauren E Krausfeldt,Helena L Pound,Hanqi Wu,Zheng Zheng,Steven W Wilhelm
Cyanobacterial blooms dominated by Microcystis spp. pose significant ecological challenges, including the release of toxins and disruption of aquatic food webs. Although Microcystis can exist as free-living single cells or within dense mucilaginous colonies, the drivers and consequences of colony formation remain unclear. Here, we integrated metatranscriptomic datasets from two Microcystis bloom events in Lake Taihu, China, to analyze and to support findings on the functional differences between colonial and single-cell Microcystis. Our results confirmed colony expression profiles were disproportionately enriched in Microcystis transcripts compared to other prokaryotic taxa. This pattern exhibits Black Queen-like dynamics, where Microcystis assumes greater metabolic and defensive roles while associated bacteria reduce their transcriptional activity. Concomitantly, viral infection strategies diverged by Microcystis community morphology: colony-associated cells expressed lysogeny-associated genes, whereas single cells exhibited increased signatures of lytic infection. These data are consistent with the hypothesis that Microcystis colonies foster conditions favorable to lysogen formation-likely due to local high cell densities and the resulting advantage of superinfection immunity-whereas solitary cells experience stronger lytic pressure. On a broader scale, our findings refine the understanding of bloom dynamics by identifying how community morphological states coincide with distinct host-virus interactions. Cumulatively, this work underscores the importance of colony formation in shaping Microcystis ecology and highlights the need for further mechanistic studies to disentangle the complex interplay between phage infection modes, colony formation, and microbial community structure.
{"title":"Contrasting viral infection strategies for single cell and colonial Microcystis populations consistent with Black Queen dynamics.","authors":"Xuhui Huang,Emily E Chase,Brittany N Zepernick,Robbie M Martin,Lauren E Krausfeldt,Helena L Pound,Hanqi Wu,Zheng Zheng,Steven W Wilhelm","doi":"10.1093/ismejo/wraf244","DOIUrl":"https://doi.org/10.1093/ismejo/wraf244","url":null,"abstract":"Cyanobacterial blooms dominated by Microcystis spp. pose significant ecological challenges, including the release of toxins and disruption of aquatic food webs. Although Microcystis can exist as free-living single cells or within dense mucilaginous colonies, the drivers and consequences of colony formation remain unclear. Here, we integrated metatranscriptomic datasets from two Microcystis bloom events in Lake Taihu, China, to analyze and to support findings on the functional differences between colonial and single-cell Microcystis. Our results confirmed colony expression profiles were disproportionately enriched in Microcystis transcripts compared to other prokaryotic taxa. This pattern exhibits Black Queen-like dynamics, where Microcystis assumes greater metabolic and defensive roles while associated bacteria reduce their transcriptional activity. Concomitantly, viral infection strategies diverged by Microcystis community morphology: colony-associated cells expressed lysogeny-associated genes, whereas single cells exhibited increased signatures of lytic infection. These data are consistent with the hypothesis that Microcystis colonies foster conditions favorable to lysogen formation-likely due to local high cell densities and the resulting advantage of superinfection immunity-whereas solitary cells experience stronger lytic pressure. On a broader scale, our findings refine the understanding of bloom dynamics by identifying how community morphological states coincide with distinct host-virus interactions. Cumulatively, this work underscores the importance of colony formation in shaping Microcystis ecology and highlights the need for further mechanistic studies to disentangle the complex interplay between phage infection modes, colony formation, and microbial community structure.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145433856","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Fangze Gui,Yusufjon Gafforov,Juan Ignacio Vílchez,Jiangtao Zhao,Zhonghua Ma,Tianxing Lv,Mengcen Wang
Chemical communication, a universal mode among the interactive members within dynamic plant-microbiome systems, fundamentally drives coevolutionary trajectories. Emerging evidence suggests the critical role of epigenetic regulation in chemical communication, though its mechanistic insights are yet not well understood, a gap that has limited the precise mining of microbiomes function in modern agriculture. Here, we synthesize recent findings from chemistry to epigenetics to illuminate the overlooked epigenetic landscape in plant-microbiome chemical communication. Revisiting the traditional plant-pathogen interaction model and a more complex ternary model involving the plant resident microbiota, we not only present knowledge gaps but also critically dissect the paradoxical roles of resident microbiota by proposing four chemo-epigenetic patterns that fine-tune the interactions among plants, resident microbiota and pathogens. Further, Intelligent Click Chemistry (ICC), an innovative interdisciplinary strategy integrating click chemistry and artificial intelligence, is proposed and discussed, with the aim of unraveling the complex chemo-epigenetic events underlying plant-microbiome chemical communication. Untangling the epigenetic landscape underpinning plant-microbiome chemical communication would enable the strategic and precise exploitation of beneficial microbial traits and suppression of detrimental interactions for sustainable agriculture.
{"title":"Epigenetic landscape underlying plant-microbiome chemical communication.","authors":"Fangze Gui,Yusufjon Gafforov,Juan Ignacio Vílchez,Jiangtao Zhao,Zhonghua Ma,Tianxing Lv,Mengcen Wang","doi":"10.1093/ismejo/wraf249","DOIUrl":"https://doi.org/10.1093/ismejo/wraf249","url":null,"abstract":"Chemical communication, a universal mode among the interactive members within dynamic plant-microbiome systems, fundamentally drives coevolutionary trajectories. Emerging evidence suggests the critical role of epigenetic regulation in chemical communication, though its mechanistic insights are yet not well understood, a gap that has limited the precise mining of microbiomes function in modern agriculture. Here, we synthesize recent findings from chemistry to epigenetics to illuminate the overlooked epigenetic landscape in plant-microbiome chemical communication. Revisiting the traditional plant-pathogen interaction model and a more complex ternary model involving the plant resident microbiota, we not only present knowledge gaps but also critically dissect the paradoxical roles of resident microbiota by proposing four chemo-epigenetic patterns that fine-tune the interactions among plants, resident microbiota and pathogens. Further, Intelligent Click Chemistry (ICC), an innovative interdisciplinary strategy integrating click chemistry and artificial intelligence, is proposed and discussed, with the aim of unraveling the complex chemo-epigenetic events underlying plant-microbiome chemical communication. Untangling the epigenetic landscape underpinning plant-microbiome chemical communication would enable the strategic and precise exploitation of beneficial microbial traits and suppression of detrimental interactions for sustainable agriculture.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"35 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-11-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145433854","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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