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
{"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":"10.1038/s41564-024-01858-9","url":null,"abstract":"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. Coffee consumption is associated with the presence and abundance of a specific member of the human gut microbiome, Lawsonibacter asaccharolyticus, and changes to the plasma metabolome.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3120-3134"},"PeriodicalIF":20.5,"publicationDate":"2024-11-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41564-024-01858-9.pdf","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":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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
{"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":"10.1038/s41564-024-01849-w","url":null,"abstract":"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. Increased IL-13 drives increased bacterial dissemination and mortality following Acinetobacter baumannii lung infection of zinc-deficient mice and can be countered by anti-IL-13 antibody therapy.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3196-3209"},"PeriodicalIF":20.5,"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}
Richard J. Henshaw, Jonathan Moon, Michael R. Stehnach, Benjamin P. Bowen, Suzanne M. Kosina, Trent R. Northen, Jeffrey S. Guasto, Sheri A. Floge
{"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":"10.1038/s41564-024-01843-2","url":null,"abstract":"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. The authors use time-resolved metabolomics and microfluidics to characterize enhanced heterotroph chemoattraction to metabolites released from cyanobacteria during early stages of phage infection.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3184-3195"},"PeriodicalIF":20.5,"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}
{"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":"10.1038/s41564-024-01846-z","url":null,"abstract":"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. Time-lapse imaging of Mycobacterium tuberculosis cells loaded in microfluidic chambers reveals heterogeneity in growth characteristics, atypical modes of polar growth initiation and linear growth at the single-cell level.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3332-3344"},"PeriodicalIF":20.5,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41564-024-01846-z.pdf","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":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Estimates of microbiome heritability across hosts","authors":"Andrew H. Morris, Brendan J. M. Bohannan","doi":"10.1038/s41564-024-01865-w","DOIUrl":"10.1038/s41564-024-01865-w","url":null,"abstract":"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. In this Perspective, Morris and Bohannan discuss heritability of microbiome-mediated traits across hosts and future research questions with implications for animal and plant breeding.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3110-3119"},"PeriodicalIF":20.5,"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}
{"title":"A method to detect origin of transfer sequences for plasmid conjugation","authors":"","doi":"10.1038/s41564-024-01845-0","DOIUrl":"10.1038/s41564-024-01845-0","url":null,"abstract":"Plasmid conjugation has been extensively studied over the past decades. Yet, in most plasmids, the minimal region required for conjugation (the origin of transfer (oriT) sequence) is unknown. The characterization of known oriTs enabled the development of a validated method to identify genomic regions with novel families of oriTs across bacterial plasmids.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3095-3096"},"PeriodicalIF":20.5,"publicationDate":"2024-11-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142601053","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}
Raquel Peixoto, Christian R. Voolstra, Lisa Y. Stein, Philip Hugenholtz, Joana Falcao Salles, Shady A. Amin, Max Häggblom, Ann Gregory, Thulani P. Makhalanyane, Fengping Wang, Nadège Adoukè Agbodjato, Yinzhao Wang, Nianzhi Jiao, Jay T. Lennon, Antonio Ventosa, Patrik M. Bavoil, Virginia Miller, Jack A. Gilbert
{"title":"Microbial solutions must be deployed against climate catastrophe","authors":"Raquel Peixoto, Christian R. Voolstra, Lisa Y. Stein, Philip Hugenholtz, Joana Falcao Salles, Shady A. Amin, Max Häggblom, Ann Gregory, Thulani P. Makhalanyane, Fengping Wang, Nadège Adoukè Agbodjato, Yinzhao Wang, Nianzhi Jiao, Jay T. Lennon, Antonio Ventosa, Patrik M. Bavoil, Virginia Miller, Jack A. Gilbert","doi":"10.1038/s41564-024-01861-0","DOIUrl":"10.1038/s41564-024-01861-0","url":null,"abstract":"This paper is a call to action. By publishing concurrently across journals like an emergency bulletin, we are not merely making a plea for awareness about climate change. Instead, we are demanding immediate, tangible steps that harness the power of microbiology and the expertise of researchers and policymakers to safeguard the planet for future generations.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3084-3085"},"PeriodicalIF":20.5,"publicationDate":"2024-11-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.nature.com/articles/s41564-024-01861-0.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142599126","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}
Manuel Ares-Arroyo, Amandine Nucci, Eduardo P. C. Rocha
{"title":"Expanding the diversity of origin of transfer-containing sequences in mobilizable plasmids","authors":"Manuel Ares-Arroyo, Amandine Nucci, Eduardo P. C. Rocha","doi":"10.1038/s41564-024-01844-1","DOIUrl":"10.1038/s41564-024-01844-1","url":null,"abstract":"Conjugative plasmids are important drivers of bacterial evolution. Most plasmids lack genes for conjugation and characterized origins of transfer (oriT), which has hampered our understanding of plasmid mobility. Here we used bioinformatic analyses to characterize occurrences of known oriT families across 38,057 plasmids, confirming that most conjugative and mobilizable plasmids lack identifiable oriTs. Recognizable oriT sequences tend to be intergenic, upstream of relaxase genes and specifically associated with relaxase types. We used these criteria to develop a computational method to search for and identify 21 additional families of oriT-containing sequences in plasmids from the pathogens Escherichia coli, Klebsiella pneumoniae and Acinetobacter baumannii. Sequence analyses found 3,072 occurrences of these oriT-containing sequences across 2,976 plasmids, many of which encoded antimicrobial resistance genes. Six candidate oriT-containing sequences were validated experimentally and were shown to facilitate conjugation in E. coli. These findings expand our understanding of plasmid mobility. Characterization of known plasmid oriT features facilitates identification of 21 oriT-containing sequence families which, alongside candidate sequence validation, expands our understanding of plasmid mobility, including plasmids encoding antibiotic resistance.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3240-3253"},"PeriodicalIF":20.5,"publicationDate":"2024-11-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142597656","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}
Susu Jiang, Chao Chen, Wanqiu Huang, Yue He, Xuan Du, Yi Wang, Hongda Ou, Zixin Deng, Congrui Xu, Lixu Jiang, Lianrong Wang, Shi Chen
{"title":"A widespread phage-encoded kinase enables evasion of multiple host antiphage defence systems","authors":"Susu Jiang, Chao Chen, Wanqiu Huang, Yue He, Xuan Du, Yi Wang, Hongda Ou, Zixin Deng, Congrui Xu, Lixu Jiang, Lianrong Wang, Shi Chen","doi":"10.1038/s41564-024-01851-2","DOIUrl":"10.1038/s41564-024-01851-2","url":null,"abstract":"DNA degradation (Dnd) is a widespread bacterial antiphage defence system that relies on DNA phosphorothioate (PT) modification for self/non-self discrimination and subsequent degradation of unmodified DNA. Phages employ counterstrategies to evade host immunity, but anti-Dnd immunity has not been characterized. Here we report an immune evasion protein encoded by the Salmonella phage JSS1 that contributes to subverting Dnd and other defence systems. Using quantitative proteomic and phosphoproteomic analyses, we show that the protein JSS1_004 employs N-terminal Ser/Thr/Tyr protein kinase activity to catalyse the multisite phosphorylation of host DndFGH. Notably, JSS1_004 also phosphorylates other bacterial immune systems to varying degrees, including CRISPR‒Cas, QatABCD, SIR2+HerA and DUF4297+HerA. Given that JSS1_004 and its homologues are widespread in phylogenetically diverse phages, we suggest that this strategy constitutes a family of immune evasion proteins that increases the chances of phage proliferation even when a host deploys multiple defence systems. An immune evasion protein encoded by the Salmonella phage JSS1 subverts multiple host antiphage defence systems using protein kinase activity.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3226-3239"},"PeriodicalIF":20.5,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142588686","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}
Luis Vigetti, Bastien Touquet, Delphine Debarre, Thierry Rose, Lionel Bureau, Dima Abdallah, Galina V. Dubacheva, Isabelle Tardieux
{"title":"Submicrometre spatiotemporal characterization of the Toxoplasma adhesion strategy for gliding motility","authors":"Luis Vigetti, Bastien Touquet, Delphine Debarre, Thierry Rose, Lionel Bureau, Dima Abdallah, Galina V. Dubacheva, Isabelle Tardieux","doi":"10.1038/s41564-024-01818-3","DOIUrl":"10.1038/s41564-024-01818-3","url":null,"abstract":"Toxoplasma gondii is a protozoan apicomplexan parasite that uses an adhesion-dependent mode of motility termed gliding to access host cells and disseminate into tissues. Previous studies on Apicomplexa motile morphotypes, including the T. gondii tachyzoite, have identified a cortical actin–myosin motor system that drives the rearward translocation of transmembrane adhesins, thus powering forward movement. However, this model is currently questioned. Here, combining micropatterning and tunable surface chemistry (to edit parasite surface ligands) with flow force and live or super-resolution imaging, we show that tachyzoites build only one apical anchoring contact with the substrate, over which it slides. Furthermore, we show that glycosaminoglycan–parasite interactions are sufficient to promote such force-productive contact and find that the apicobasal flow is set up independent of adhesin release and surface interactions. These findings should enable further characterization of the molecular functions at the T. gondii–substrate mechanosensitive interface and their comparison across apicomplexans. Live imaging, combined with micropatterning and tunable surface chemistry, reveals the adhesive strategy evolved by Toxoplasma gondii for helical gliding.","PeriodicalId":18992,"journal":{"name":"Nature Microbiology","volume":"9 12","pages":"3148-3164"},"PeriodicalIF":20.5,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142574466","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}