Pub Date : 2024-11-18DOI: 10.1038/s41564-024-01858-9
Paolo Manghi, Amrisha Bhosle, Kai Wang, Roberta Marconi, Marta Selma-Royo, Liviana Ricci, Francesco Asnicar, Davide Golzato, Wenjie Ma, Dong Hang, Kelsey N. Thompson, Eric A. Franzosa, Amir Nabinejad, Sabrina Tamburini, Eric B. Rimm, Wendy S. Garrett, Qi Sun, Andrew T. Chan, Mireia Valles-Colomer, Manimozhiyan Arumugam, Kate M. Bermingham, Francesca Giordano, Richard Davies, George Hadjigeorgiou, Jonathan Wolf, Till Strowig, Sarah E. Berry, Curtis Huttenhower, Tim D. Spector, Nicola Segata, Mingyang Song
Although diet is a substantial determinant of the human gut microbiome, the interplay between specific foods and microbial community structure remains poorly understood. Coffee is a habitually consumed beverage with established metabolic and health benefits. We previously found that coffee is, among >150 items, the food showing the highest correlation with microbiome components. Here we conducted a multi-cohort, multi-omic analysis of US and UK populations with detailed dietary information from a total of 22,867 participants, which we then integrated with public data from 211 cohorts (N = 54,198). The link between coffee consumption and microbiome was highly reproducible across different populations (area under the curve of 0.89), largely driven by the presence and abundance of the species Lawsonibacter asaccharolyticus. Using in vitro experiments, we show that coffee can stimulate growth of L.asaccharolyticus. Plasma metabolomics on 438 samples identified several metabolites enriched among coffee consumers, with quinic acid and its potential derivatives associated with coffee and L.asaccharolyticus. This study reveals a metabolic link between a specific gut microorganism and a specific food item, providing a framework for the understanding of microbial dietary responses at the biochemical level.
{"title":"Coffee consumption is associated with intestinal Lawsonibacter asaccharolyticus abundance and prevalence across multiple cohorts","authors":"Paolo Manghi, Amrisha Bhosle, Kai Wang, Roberta Marconi, Marta Selma-Royo, Liviana Ricci, Francesco Asnicar, Davide Golzato, Wenjie Ma, Dong Hang, Kelsey N. Thompson, Eric A. Franzosa, Amir Nabinejad, Sabrina Tamburini, Eric B. Rimm, Wendy S. Garrett, Qi Sun, Andrew T. Chan, Mireia Valles-Colomer, Manimozhiyan Arumugam, Kate M. Bermingham, Francesca Giordano, Richard Davies, George Hadjigeorgiou, Jonathan Wolf, Till Strowig, Sarah E. Berry, Curtis Huttenhower, Tim D. Spector, Nicola Segata, Mingyang Song","doi":"10.1038/s41564-024-01858-9","DOIUrl":"https://doi.org/10.1038/s41564-024-01858-9","url":null,"abstract":"<p>Although diet is a substantial determinant of the human gut microbiome, the interplay between specific foods and microbial community structure remains poorly understood. Coffee is a habitually consumed beverage with established metabolic and health benefits. We previously found that coffee is, among >150 items, the food showing the highest correlation with microbiome components. Here we conducted a multi-cohort, multi-omic analysis of US and UK populations with detailed dietary information from a total of 22,867 participants, which we then integrated with public data from 211 cohorts (<i>N</i> = 54,198). The link between coffee consumption and microbiome was highly reproducible across different populations (area under the curve of 0.89), largely driven by the presence and abundance of the species <i>Lawsonibacter asaccharolyticus</i>. Using in vitro experiments, we show that coffee can stimulate growth of <i>L.</i> <i>asaccharolyticus</i>. Plasma metabolomics on 438 samples identified several metabolites enriched among coffee consumers, with quinic acid and its potential derivatives associated with coffee and <i>L.</i> <i>asaccharolyticus</i>. This study reveals a metabolic link between a specific gut microorganism and a specific food item, providing a framework for the understanding of microbial dietary responses at the biochemical level.</p>","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"50 1","pages":""},"PeriodicalIF":28.3,"publicationDate":"2024-11-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142665488","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-15DOI: 10.1038/s41564-024-01849-w
Lauren D. Palmer, Kacie A. Traina, Lillian J. Juttukonda, Zachery R. Lonergan, Dziedzom A. Bansah, Xiaomei Ren, John H. Geary, Christopher Pinelli, Kelli L. Boyd, Tzushan S. Yang, Eric P. Skaar
Dietary zinc deficiency is a major risk factor for pneumonia. Acinetobacter baumannii is a leading cause of ventilator-associated pneumonia and a critical public health threat due to increasing rates of multidrug resistance. Patient populations at increased risk for A. baumannii pneumonia are also at increased risk of zinc deficiency. Here we established a mouse model of dietary zinc deficiency and acute A. baumannii pneumonia to test the hypothesis that host zinc deficiency contributes to A. baumannii pathogenesis. We showed that zinc-deficient mice have significantly increased A. baumannii burdens in the lungs, dissemination to the spleen and higher mortality. During infection, zinc-deficient mice produce more pro-inflammatory cytokines, including IL-13. Administration of IL-13 promotes A. baumannii dissemination in zinc-sufficient mice, while antibody neutralization of IL-13 protects zinc-deficient mice from A. baumannii dissemination and mortality during infection. These data highlight the therapeutic potential of anti-IL-13 antibody treatments, which are well tolerated in humans, for the treatment of pneumonia.
{"title":"Dietary zinc deficiency promotes Acinetobacter baumannii lung infection via IL-13 in mice","authors":"Lauren D. Palmer, Kacie A. Traina, Lillian J. Juttukonda, Zachery R. Lonergan, Dziedzom A. Bansah, Xiaomei Ren, John H. Geary, Christopher Pinelli, Kelli L. Boyd, Tzushan S. Yang, Eric P. Skaar","doi":"10.1038/s41564-024-01849-w","DOIUrl":"https://doi.org/10.1038/s41564-024-01849-w","url":null,"abstract":"<p>Dietary zinc deficiency is a major risk factor for pneumonia. <i>Acinetobacter baumannii</i> is a leading cause of ventilator-associated pneumonia and a critical public health threat due to increasing rates of multidrug resistance. Patient populations at increased risk for <i>A. baumannii</i> pneumonia are also at increased risk of zinc deficiency. Here we established a mouse model of dietary zinc deficiency and acute <i>A. baumannii</i> pneumonia to test the hypothesis that host zinc deficiency contributes to <i>A. baumannii</i> pathogenesis. We showed that zinc-deficient mice have significantly increased <i>A. baumannii</i> burdens in the lungs, dissemination to the spleen and higher mortality. During infection, zinc-deficient mice produce more pro-inflammatory cytokines, including IL-13. Administration of IL-13 promotes <i>A. baumannii</i> dissemination in zinc-sufficient mice, while antibody neutralization of IL-13 protects zinc-deficient mice from <i>A. baumannii</i> dissemination and mortality during infection. These data highlight the therapeutic potential of anti-IL-13 antibody treatments, which are well tolerated in humans, for the treatment of pneumonia.</p>","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"75 1","pages":""},"PeriodicalIF":28.3,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142637062","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-15DOI: 10.1038/s41564-024-01843-2
Richard J. Henshaw, Jonathan Moon, Michael R. Stehnach, Benjamin P. Bowen, Suzanne M. Kosina, Trent R. Northen, Jeffrey S. Guasto, Sheri A. Floge
Chemical cues mediate interactions between marine phytoplankton and bacteria, underpinning ecosystem-scale processes including nutrient cycling and carbon fixation. Phage infection alters host metabolism, stimulating the release of chemical cues from intact plankton, but how these dynamics impact ecology and biogeochemistry is poorly understood. Here we determine the impact of phage infection on dissolved metabolite pools from marine cyanobacteria and the subsequent chemotactic response of heterotrophic bacteria using time-resolved metabolomics and microfluidics. Metabolites released from intact, phage-infected Synechococcus elicited strong chemoattraction from Vibrio alginolyticus and Pseudoalteromonas haloplanktis, especially during early infection stages. Sustained bacterial chemotaxis occurred towards live-infected Synechococcus, contrasted by no discernible chemotaxis towards uninfected cyanobacteria. High-throughput microfluidics identified 5′-deoxyadenosine and 5′-methylthioadenosine as key attractants. Our findings establish that, before lysis, phage-infected picophytoplankton release compounds that attract motile heterotrophic bacteria, suggesting a mechanism for resource transfer that might impact carbon and nutrient fluxes across trophic levels.
{"title":"Metabolites from intact phage-infected Synechococcus chemotactically attract heterotrophic marine bacteria","authors":"Richard J. Henshaw, Jonathan Moon, Michael R. Stehnach, Benjamin P. Bowen, Suzanne M. Kosina, Trent R. Northen, Jeffrey S. Guasto, Sheri A. Floge","doi":"10.1038/s41564-024-01843-2","DOIUrl":"https://doi.org/10.1038/s41564-024-01843-2","url":null,"abstract":"<p>Chemical cues mediate interactions between marine phytoplankton and bacteria, underpinning ecosystem-scale processes including nutrient cycling and carbon fixation. Phage infection alters host metabolism, stimulating the release of chemical cues from intact plankton, but how these dynamics impact ecology and biogeochemistry is poorly understood. Here we determine the impact of phage infection on dissolved metabolite pools from marine cyanobacteria and the subsequent chemotactic response of heterotrophic bacteria using time-resolved metabolomics and microfluidics. Metabolites released from intact, phage-infected <i>Synechococcus</i> elicited strong chemoattraction from <i>Vibrio alginolyticus</i> and <i>Pseudoalteromonas haloplanktis</i>, especially during early infection stages. Sustained bacterial chemotaxis occurred towards live-infected <i>Synechococcus</i>, contrasted by no discernible chemotaxis towards uninfected cyanobacteria. High-throughput microfluidics identified 5′-deoxyadenosine and 5′-methylthioadenosine as key attractants. Our findings establish that, before lysis, phage-infected picophytoplankton release compounds that attract motile heterotrophic bacteria, suggesting a mechanism for resource transfer that might impact carbon and nutrient fluxes across trophic levels.</p>","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"11 1","pages":""},"PeriodicalIF":28.3,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142637054","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Difficulties in antibiotic treatment of Mycobacterium tuberculosis (Mtb) are partly thought to be due to heterogeneity in growth. Although the ability of bacterial pathogens to regulate growth is crucial to control homeostasis, virulence and drug responses, single-cell growth and cell cycle behaviours of Mtb are poorly characterized. Here we use time-lapse, single-cell imaging of Mtb coupled with mathematical modelling to observe asymmetric growth and heterogeneity in cell size, interdivision time and elongation speed. We find that, contrary to Mycobacterium smegmatis, Mtb initiates cell growth not only from the old pole but also from new poles or both poles. Whereas most organisms grow exponentially at the single-cell level, Mtb has a linear growth mode. Our data show that the growth behaviour of Mtb diverges from that of model bacteria, provide details into how Mtb grows and creates heterogeneity and suggest that growth regulation may also diverge from that in other bacteria.
{"title":"Single-cell imaging of the Mycobacterium tuberculosis cell cycle reveals linear and heterogenous growth","authors":"Eun Seon Chung, Prathitha Kar, Maliwan Kamkaew, Ariel Amir, Bree B. Aldridge","doi":"10.1038/s41564-024-01846-z","DOIUrl":"https://doi.org/10.1038/s41564-024-01846-z","url":null,"abstract":"<p>Difficulties in antibiotic treatment of <i>Mycobacterium tuberculosis</i> (Mtb) are partly thought to be due to heterogeneity in growth. Although the ability of bacterial pathogens to regulate growth is crucial to control homeostasis, virulence and drug responses, single-cell growth and cell cycle behaviours of Mtb are poorly characterized. Here we use time-lapse, single-cell imaging of Mtb coupled with mathematical modelling to observe asymmetric growth and heterogeneity in cell size, interdivision time and elongation speed. We find that, contrary to <i>Mycobacterium smegmatis</i>, Mtb initiates cell growth not only from the old pole but also from new poles or both poles. Whereas most organisms grow exponentially at the single-cell level, Mtb has a linear growth mode. Our data show that the growth behaviour of Mtb diverges from that of model bacteria, provide details into how Mtb grows and creates heterogeneity and suggest that growth regulation may also diverge from that in other bacteria.</p>","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"2018 1","pages":""},"PeriodicalIF":28.3,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142637049","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-15DOI: 10.1038/s41564-024-01865-w
Andrew H. Morris, Brendan J. M. Bohannan
Microbiomes contribute to variation in many plant and animal traits, suggesting that microbiome-mediated traits could evolve through selection on the host. However, for such evolution to occur, microbiomes must exhibit sufficient heritability to contribute to host adaptation. Previous work has attempted to estimate the heritability of a variety of microbiome attributes. Here we show that most published estimates are limited to vertebrate and plant hosts, but significant heritability of microbiome attributes has been frequently reported. This indicates that microbiomes could evolve in response to host-level selection, but studies across a wider range of hosts are necessary before general conclusions can be made. We suggest future studies focus on standardizing heritability measurements for the purpose of meta-analyses and investigate the role of the environment in contributing to heritable microbiome variation. This could have important implications for the use of microbiomes in conservation, agriculture and medicine.
{"title":"Estimates of microbiome heritability across hosts","authors":"Andrew H. Morris, Brendan J. M. Bohannan","doi":"10.1038/s41564-024-01865-w","DOIUrl":"https://doi.org/10.1038/s41564-024-01865-w","url":null,"abstract":"<p>Microbiomes contribute to variation in many plant and animal traits, suggesting that microbiome-mediated traits could evolve through selection on the host. However, for such evolution to occur, microbiomes must exhibit sufficient heritability to contribute to host adaptation. Previous work has attempted to estimate the heritability of a variety of microbiome attributes. Here we show that most published estimates are limited to vertebrate and plant hosts, but significant heritability of microbiome attributes has been frequently reported. This indicates that microbiomes could evolve in response to host-level selection, but studies across a wider range of hosts are necessary before general conclusions can be made. We suggest future studies focus on standardizing heritability measurements for the purpose of meta-analyses and investigate the role of the environment in contributing to heritable microbiome variation. This could have important implications for the use of microbiomes in conservation, agriculture and medicine.</p>","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"245 1","pages":""},"PeriodicalIF":28.3,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142637045","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-11-16DOI: 10.1038/s41564-023-01519-3
Paula T. Littlejohn, Avril Metcalfe-Roach, Erick Cardenas Poire, Ravi Holani, Haggai Bar-Yoseph, Yiyun M. Fan, Sarah E. Woodward, B. Brett Finlay
Globally, ~340 million children suffer from multiple micronutrient deficiencies, accompanied by high pathogenic burden and death due to multidrug-resistant bacteria. The microbiome is a reservoir of antimicrobial resistance (AMR), but the implications of undernutrition on the resistome is unclear. Here we used a postnatal mouse model that is deficient in multiple micronutrients (that is, zinc, folate, iron, vitamin A and vitamin B12 deficient) and shotgun metagenomic sequencing of faecal samples to characterize gut microbiome structure and functional potential, and the resistome. Enterobacteriaceae were enriched in micronutrient-deficient mice compared with mice fed an isocaloric experimental control diet. The mycobiome and virome were also altered with multiple micronutrient deficiencies including increased fungal pathogens such as Candida dubliniensis and bacteriophages. Despite being antibiotic naïve, micronutrient deficiency was associated with increased enrichment of genes and gene networks encoded by pathogenic bacteria that are directly or indirectly associated with intrinsic antibiotic resistance. Bacterial oxidative stress was associated with intrinsic antibiotic resistance in these mice. This analysis reveals multi-kingdom alterations in the gut microbiome as a result of co-occurring multiple micronutrient deficiencies and the implications for antibiotic resistance. A postnatal multiple micronutrient deficiency mouse model reveals shifts in bacterial, fungal and viral components of the gut microbiome with implications for microbiome-encoded intrinsic antibiotic resistance mechanisms.
{"title":"Multiple micronutrient deficiencies in early life cause multi-kingdom alterations in the gut microbiome and intrinsic antibiotic resistance genes in mice","authors":"Paula T. Littlejohn, Avril Metcalfe-Roach, Erick Cardenas Poire, Ravi Holani, Haggai Bar-Yoseph, Yiyun M. Fan, Sarah E. Woodward, B. Brett Finlay","doi":"10.1038/s41564-023-01519-3","DOIUrl":"10.1038/s41564-023-01519-3","url":null,"abstract":"Globally, ~340 million children suffer from multiple micronutrient deficiencies, accompanied by high pathogenic burden and death due to multidrug-resistant bacteria. The microbiome is a reservoir of antimicrobial resistance (AMR), but the implications of undernutrition on the resistome is unclear. Here we used a postnatal mouse model that is deficient in multiple micronutrients (that is, zinc, folate, iron, vitamin A and vitamin B12 deficient) and shotgun metagenomic sequencing of faecal samples to characterize gut microbiome structure and functional potential, and the resistome. Enterobacteriaceae were enriched in micronutrient-deficient mice compared with mice fed an isocaloric experimental control diet. The mycobiome and virome were also altered with multiple micronutrient deficiencies including increased fungal pathogens such as Candida dubliniensis and bacteriophages. Despite being antibiotic naïve, micronutrient deficiency was associated with increased enrichment of genes and gene networks encoded by pathogenic bacteria that are directly or indirectly associated with intrinsic antibiotic resistance. Bacterial oxidative stress was associated with intrinsic antibiotic resistance in these mice. This analysis reveals multi-kingdom alterations in the gut microbiome as a result of co-occurring multiple micronutrient deficiencies and the implications for antibiotic resistance. A postnatal multiple micronutrient deficiency mouse model reveals shifts in bacterial, fungal and viral components of the gut microbiome with implications for microbiome-encoded intrinsic antibiotic resistance mechanisms.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"8 12","pages":"2392-2405"},"PeriodicalIF":28.3,"publicationDate":"2023-11-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136398337","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-11-16DOI: 10.1038/s41564-023-01502-y
Pim Goossens, Jelle Spooren, Kim C. M. Baremans, Annemiek Andel, Dmitry Lapin, Nakisa Echobardo, Corné M. J. Pieterse, Guido Van den Ackerveken, Roeland L. Berendsen
Hyaloperonospora arabidopsidis (Hpa) is an obligately biotrophic downy mildew that is routinely cultured on Arabidopsis thaliana hosts that harbour complex microbiomes. We hypothesized that the culturing procedure proliferates Hpa-associated microbiota (HAM) in addition to the pathogen and exploited this model system to investigate which microorganisms consistently associate with Hpa. Using amplicon sequencing, we found nine bacterial sequence variants that are shared between at least three out of four Hpa cultures in the Netherlands and Germany and comprise 34% of the phyllosphere community of the infected plants. Whole-genome sequencing showed that representative HAM bacterial isolates from these distinct Hpa cultures are isogenic and that an additional seven published Hpa metagenomes contain numerous sequences of the HAM. Although we showed that HAM benefit from Hpa infection, HAM negatively affect Hpa spore formation. Moreover, we show that pathogen-infected plants can selectively recruit HAM to both their roots and shoots and form a soil-borne infection-associated microbiome that helps resist the pathogen. Understanding the mechanisms by which infection-associated microbiomes are formed might enable breeding of crop varieties that select for protective microbiomes. Near-identical downy-mildew-associated microbiomes are recruited by infected Arabidopsis plants in different laboratories and reduce the impact of subsequent infection.
{"title":"Obligate biotroph downy mildew consistently induces near-identical protective microbiomes in Arabidopsis thaliana","authors":"Pim Goossens, Jelle Spooren, Kim C. M. Baremans, Annemiek Andel, Dmitry Lapin, Nakisa Echobardo, Corné M. J. Pieterse, Guido Van den Ackerveken, Roeland L. Berendsen","doi":"10.1038/s41564-023-01502-y","DOIUrl":"10.1038/s41564-023-01502-y","url":null,"abstract":"Hyaloperonospora arabidopsidis (Hpa) is an obligately biotrophic downy mildew that is routinely cultured on Arabidopsis thaliana hosts that harbour complex microbiomes. We hypothesized that the culturing procedure proliferates Hpa-associated microbiota (HAM) in addition to the pathogen and exploited this model system to investigate which microorganisms consistently associate with Hpa. Using amplicon sequencing, we found nine bacterial sequence variants that are shared between at least three out of four Hpa cultures in the Netherlands and Germany and comprise 34% of the phyllosphere community of the infected plants. Whole-genome sequencing showed that representative HAM bacterial isolates from these distinct Hpa cultures are isogenic and that an additional seven published Hpa metagenomes contain numerous sequences of the HAM. Although we showed that HAM benefit from Hpa infection, HAM negatively affect Hpa spore formation. Moreover, we show that pathogen-infected plants can selectively recruit HAM to both their roots and shoots and form a soil-borne infection-associated microbiome that helps resist the pathogen. Understanding the mechanisms by which infection-associated microbiomes are formed might enable breeding of crop varieties that select for protective microbiomes. Near-identical downy-mildew-associated microbiomes are recruited by infected Arabidopsis plants in different laboratories and reduce the impact of subsequent infection.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"8 12","pages":"2349-2364"},"PeriodicalIF":28.3,"publicationDate":"2023-11-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136398338","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-11-16DOI: 10.1038/s41564-023-01518-4
Hannah Jeckel, Kazuki Nosho, Konstantin Neuhaus, Alasdair D. Hastewell, Dominic J. Skinner, Dibya Saha, Niklas Netter, Nicole Paczia, Jörn Dunkel, Knut Drescher
Development of microbial communities is a complex multiscale phenomenon with wide-ranging biomedical and ecological implications. How biological and physical processes determine emergent spatial structures in microbial communities remains poorly understood due to a lack of simultaneous measurements of gene expression and cellular behaviour in space and time. Here we combined live-cell microscopy with a robotic arm for spatiotemporal sampling, which enabled us to simultaneously acquire phenotypic imaging data and spatiotemporal transcriptomes during Bacillus subtilis swarm development. Quantitative characterization of the spatiotemporal gene expression patterns revealed correlations with cellular and collective properties, and phenotypic subpopulations. By integrating these data with spatiotemporal metabolome measurements, we discovered a spatiotemporal cross-feeding mechanism fuelling swarm development: during their migration, earlier generations deposit metabolites which are consumed by later generations that swarm across the same location. These results highlight the importance of spatiotemporal effects during the emergence of phenotypic subpopulations and their interactions in bacterial communities. Spatiotemporal transcriptomes during multicellular development of Bacillus subtilis swarms reveal supra-generational cooperation.
{"title":"Simultaneous spatiotemporal transcriptomics and microscopy of Bacillus subtilis swarm development reveal cooperation across generations","authors":"Hannah Jeckel, Kazuki Nosho, Konstantin Neuhaus, Alasdair D. Hastewell, Dominic J. Skinner, Dibya Saha, Niklas Netter, Nicole Paczia, Jörn Dunkel, Knut Drescher","doi":"10.1038/s41564-023-01518-4","DOIUrl":"10.1038/s41564-023-01518-4","url":null,"abstract":"Development of microbial communities is a complex multiscale phenomenon with wide-ranging biomedical and ecological implications. How biological and physical processes determine emergent spatial structures in microbial communities remains poorly understood due to a lack of simultaneous measurements of gene expression and cellular behaviour in space and time. Here we combined live-cell microscopy with a robotic arm for spatiotemporal sampling, which enabled us to simultaneously acquire phenotypic imaging data and spatiotemporal transcriptomes during Bacillus subtilis swarm development. Quantitative characterization of the spatiotemporal gene expression patterns revealed correlations with cellular and collective properties, and phenotypic subpopulations. By integrating these data with spatiotemporal metabolome measurements, we discovered a spatiotemporal cross-feeding mechanism fuelling swarm development: during their migration, earlier generations deposit metabolites which are consumed by later generations that swarm across the same location. These results highlight the importance of spatiotemporal effects during the emergence of phenotypic subpopulations and their interactions in bacterial communities. Spatiotemporal transcriptomes during multicellular development of Bacillus subtilis swarms reveal supra-generational cooperation.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"8 12","pages":"2378-2391"},"PeriodicalIF":28.3,"publicationDate":"2023-11-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10686836/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136398339","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-11-16DOI: 10.1038/s41564-023-01514-8
Michael E. Van Nuland, S. Caroline Daws, Joseph K. Bailey, Jennifer A. Schweitzer, Posy E. Busby, Kabir G. Peay
Understanding drivers of terrestrial fungal communities over large scales is an important challenge for predicting the fate of ecosystems under climate change and providing critical ecological context for bioengineering plant–microbe interactions in model systems. We conducted an extensive molecular and microscopy field study across the contiguous United States measuring natural variation in the Populus fungal microbiome among tree species, plant niche compartments and key symbionts. Our results show clear biodiversity hotspots and regional endemism of Populus-associated fungal communities explained by a combination of climate, soil and geographic factors. Modelling climate change impacts showed a deterioration of Populus mycorrhizal associations and an increase in potentially pathogenic foliar endophyte diversity and prevalence. Geographic differences among these symbiont groups in their sensitivity to environmental change are likely to influence broader forest health and ecosystem function. This dataset provides an above- and belowground atlas of Populus fungal biodiversity at a continental scale. This Resource defines fungal diversity of Populus trees and associations with climate variables on a continental scale.
{"title":"Above- and belowground fungal biodiversity of Populus trees on a continental scale","authors":"Michael E. Van Nuland, S. Caroline Daws, Joseph K. Bailey, Jennifer A. Schweitzer, Posy E. Busby, Kabir G. Peay","doi":"10.1038/s41564-023-01514-8","DOIUrl":"10.1038/s41564-023-01514-8","url":null,"abstract":"Understanding drivers of terrestrial fungal communities over large scales is an important challenge for predicting the fate of ecosystems under climate change and providing critical ecological context for bioengineering plant–microbe interactions in model systems. We conducted an extensive molecular and microscopy field study across the contiguous United States measuring natural variation in the Populus fungal microbiome among tree species, plant niche compartments and key symbionts. Our results show clear biodiversity hotspots and regional endemism of Populus-associated fungal communities explained by a combination of climate, soil and geographic factors. Modelling climate change impacts showed a deterioration of Populus mycorrhizal associations and an increase in potentially pathogenic foliar endophyte diversity and prevalence. Geographic differences among these symbiont groups in their sensitivity to environmental change are likely to influence broader forest health and ecosystem function. This dataset provides an above- and belowground atlas of Populus fungal biodiversity at a continental scale. This Resource defines fungal diversity of Populus trees and associations with climate variables on a continental scale.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"8 12","pages":"2406-2419"},"PeriodicalIF":28.3,"publicationDate":"2023-11-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136398336","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-11-16DOI: 10.1038/s41564-023-01524-6
Andrew M. King, Zhengan Zhang, Emerson Glassey, Piro Siuti, Jon Clardy, Christopher A. Voigt
Human-associated bacteria secrete modified peptides to control host physiology and remodel the microbiota species composition. Here we scanned 2,229 Human Microbiome Project genomes of species colonizing skin, gastrointestinal tract, urogenital tract, mouth and trachea for gene clusters encoding RiPPs (ribosomally synthesized and post-translationally modified peptides). We found 218 lanthipeptides and 25 lasso peptides, 70 of which were synthesized and expressed in E. coli and 23 could be purified and functionally characterized. They were tested for activity against bacteria associated with healthy human flora and pathogens. New antibiotics were identified against strains implicated in skin, nasal and vaginal dysbiosis as well as from oral strains selectively targeting those in the gut. Extended- and narrow-spectrum antibiotics were found against methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococci. Mining natural products produced by human-associated microbes will enable the elucidation of ecological relationships and may be a rich resource for antimicrobial discovery. An analysis of over 2,000 genomes from Human Microbiome Project metagenomic data led to the identification of several extended- and narrow-spectrum antibiotics against clinical multidrug-resistant pathogens, including methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococci.
{"title":"Systematic mining of the human microbiome identifies antimicrobial peptides with diverse activity spectra","authors":"Andrew M. King, Zhengan Zhang, Emerson Glassey, Piro Siuti, Jon Clardy, Christopher A. Voigt","doi":"10.1038/s41564-023-01524-6","DOIUrl":"10.1038/s41564-023-01524-6","url":null,"abstract":"Human-associated bacteria secrete modified peptides to control host physiology and remodel the microbiota species composition. Here we scanned 2,229 Human Microbiome Project genomes of species colonizing skin, gastrointestinal tract, urogenital tract, mouth and trachea for gene clusters encoding RiPPs (ribosomally synthesized and post-translationally modified peptides). We found 218 lanthipeptides and 25 lasso peptides, 70 of which were synthesized and expressed in E. coli and 23 could be purified and functionally characterized. They were tested for activity against bacteria associated with healthy human flora and pathogens. New antibiotics were identified against strains implicated in skin, nasal and vaginal dysbiosis as well as from oral strains selectively targeting those in the gut. Extended- and narrow-spectrum antibiotics were found against methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococci. Mining natural products produced by human-associated microbes will enable the elucidation of ecological relationships and may be a rich resource for antimicrobial discovery. An analysis of over 2,000 genomes from Human Microbiome Project metagenomic data led to the identification of several extended- and narrow-spectrum antibiotics against clinical multidrug-resistant pathogens, including methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococci.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"8 12","pages":"2420-2434"},"PeriodicalIF":28.3,"publicationDate":"2023-11-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136398340","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}