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      A review of 10 years of human microbiome research activities at the US National Institutes of Health, Fiscal Years 2007-2016

      review-article
      NIH Human Microbiome Portfolio Analysis Team
      Microbiome
      BioMed Central
      Microbiome, Microbiota, Metagenomics, Human disease, Animal models, NIH funding, Human Microbiome Project (HMP), Fast Track Action Committee on Mapping the Microbiome (FTAC-MM), National Microbiome Initiative (NMI)

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          Abstract

          The National Institutes of Health (NIH) is the primary federal government agency for biomedical research in the USA. NIH provides extensive support for human microbiome research with 21 of 27 NIH Institutes and Centers (ICs) currently funding this area through their extramural research programs. This analysis of the NIH extramural portfolio in human microbiome research briefly reviews the early history of this field at NIH, summarizes the program objectives and the resources developed in the recently completed 10-year (fiscal years 2007–2016) $215 M Human Microbiome Project (HMP) program, evaluates the scope and range of the $728 M NIH investment in extramural human microbiome research activities outside of the HMP over fiscal years 2012–2016, and highlights some specific areas of research which emerged from this investment. This analysis closes with a few comments on the technical needs and knowledge gaps which remain for this field to be able to advance over the next decade and for the outcomes of this research to be able to progress to microbiome-based interventions for treating disease and supporting health.

          Electronic supplementary material

          The online version of this article (10.1186/s40168-019-0620-y) contains supplementary material, which is available to authorized users.

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          Most cited references58

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          Gut microbiome modulates response to anti–PD-1 immunotherapy in melanoma patients

          Pre-clinical mouse models suggest that the gut microbiome modulates tumor response to checkpoint blockade immunotherapy; however, this has not been well-characterized in human cancer patients. Here we examined the oral and gut microbiome of melanoma patients undergoing anti-PD-1 immunotherapy (n=112). Significant differences were observed in the diversity and composition of the patient gut microbiome of responders (R) versus non-responders (NR). Analysis of patient fecal microbiome samples (n=43, 30R, 13NR) showed significantly higher alpha diversity (p<0.01) and relative abundance of Ruminococcaceae bacteria (p<0.01) in responding patients. Metagenomic studies revealed functional differences in gut bacteria in R including enrichment of anabolic pathways. Immune profiling suggested enhanced systemic and anti-tumor immunity in responding patients with a favorable gut microbiome, as well as in germ-free mice receiving fecal transplants from responding patients. Together, these data have important implications for the treatment of melanoma patients with immune checkpoint inhibitors.
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            Human genetics shape the gut microbiome.

            Host genetics and the gut microbiome can both influence metabolic phenotypes. However, whether host genetic variation shapes the gut microbiome and interacts with it to affect host phenotype is unclear. Here, we compared microbiotas across >1,000 fecal samples obtained from the TwinsUK population, including 416 twin pairs. We identified many microbial taxa whose abundances were influenced by host genetics. The most heritable taxon, the family Christensenellaceae, formed a co-occurrence network with other heritable Bacteria and with methanogenic Archaea. Furthermore, Christensenellaceae and its partners were enriched in individuals with low body mass index (BMI). An obese-associated microbiome was amended with Christensenella minuta, a cultured member of the Christensenellaceae, and transplanted to germ-free mice. C. minuta amendment reduced weight gain and altered the microbiome of recipient mice. Our findings indicate that host genetics influence the composition of the human gut microbiome and can do so in ways that impact host metabolism.
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              Extensive impact of non-antibiotic drugs on human gut bacteria

              A few commonly used non-antibiotic drugs have recently been associated with changes in gut microbiome composition, but the extent of this phenomenon is unknown. We screened >1000 marketed drugs against 40 representative gut bacterial strains, and found that 24% of the drugs with human targets, including members of all therapeutic classes, inhibited the growth of at least one strain. Particular classes such as the chemically diverse antipsychotics were overrepresented. The effects of human-targeted drugs on gut bacteria are reflected on their antibiotic-like side effects in humans and are concordant with existing human cohort studies, providing in vivo relevance for our screen. Susceptibility to antibiotics and human-targeted drugs correlates across bacterial species, suggesting that non-antibiotics may promote antibiotic resistance. Our results provide a comprehensive resource for future research on drug-microbiome interactions, opening new paths for side effect control and drug repurposing, and broaden our view on antibiotic resistance.
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                Author and article information

                Contributors
                lita.proctor@nih.gov
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                26 February 2019
                26 February 2019
                2019
                : 7
                : 31
                Affiliations
                ISNI 0000 0001 2297 5165, GRID grid.94365.3d, National Institutes of Health, ; Bethesda, MD USA
                Article
                620
                10.1186/s40168-019-0620-y
                6391833
                30808411
                28a3ed90-0dc1-4bfb-ab55-1f846a35a5bb
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 24 May 2018
                : 3 January 2019
                Categories
                Review
                Custom metadata
                © The Author(s) 2019

                microbiome,microbiota,metagenomics,human disease,animal models,nih funding,human microbiome project (hmp),fast track action committee on mapping the microbiome (ftac-mm),national microbiome initiative (nmi)

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