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      Disruption of maternal gut microbiota during gestation alters offspring microbiota and immunity

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          Abstract

          Background

          Early life microbiota is an important determinant of immune and metabolic development and may have lasting consequences. The maternal gut microbiota during pregnancy or breastfeeding is important for defining infant gut microbiota. We hypothesized that maternal gut microbiota during pregnancy and breastfeeding is a critical determinant of infant immunity. To test this, pregnant BALB/c dams were fed vancomycin for 5 days prior to delivery (gestation; Mg), 14 days postpartum during nursing (Mn), or during gestation and nursing (Mgn), or no vancomycin (Mc). We analyzed adaptive immunity and gut microbiota in dams and pups at various times after delivery.

          Results

          In addition to direct alterations to maternal gut microbial composition, pup gut microbiota displayed lower α-diversity and distinct community clusters according to timing of maternal vancomycin. Vancomycin was undetectable in maternal and offspring sera, therefore the observed changes in the microbiota of stomach contents (as a proxy for breastmilk) and pup gut signify an indirect mechanism through which maternal intestinal microbiota influences extra-intestinal and neonatal commensal colonization. These effects on microbiota influenced both maternal and offspring immunity. Maternal immunity was altered, as demonstrated by significantly higher levels of both total IgG and IgM in Mgn and Mn breastmilk when compared to Mc. In pups, lymphocyte numbers in the spleens of Pg and Pn were significantly increased compared to Pc. This increase in cellularity was in part attributable to elevated numbers of both CD4+ T cells and B cells, most notable Follicular B cells.

          Conclusion

          Our results indicate that perturbations to maternal gut microbiota dictate neonatal adaptive immunity.

          Electronic supplementary material

          The online version of this article (10.1186/s40168-018-0511-7) contains supplementary material, which is available to authorized users.

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          Most cited references19

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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            The maternal microbiota drives early postnatal innate immune development.

            Postnatal colonization of the body with microbes is assumed to be the main stimulus to postnatal immune development. By transiently colonizing pregnant female mice, we show that the maternal microbiota shapes the immune system of the offspring. Gestational colonization increases intestinal group 3 innate lymphoid cells and F4/80(+)CD11c(+) mononuclear cells in the pups. Maternal colonization reprograms intestinal transcriptional profiles of the offspring, including increased expression of genes encoding epithelial antibacterial peptides and metabolism of microbial molecules. Some of these effects are dependent on maternal antibodies that potentially retain microbial molecules and transmit them to the offspring during pregnancy and in milk. Pups born to mothers transiently colonized in pregnancy are better able to avoid inflammatory responses to microbial molecules and penetration of intestinal microbes.
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              Calypso: a user-friendly web-server for mining and visualizing microbiome–environment interactions

              Abstract Calypso is an easy-to-use online software suite that allows non-expert users to mine, interpret and compare taxonomic information from metagenomic or 16S rDNA datasets. Calypso has a focus on multivariate statistical approaches that can identify complex environment-microbiome associations. The software enables quantitative visualizations, statistical testing, multivariate analysis, supervised learning, factor analysis, multivariable regression, network analysis and diversity estimates. Comprehensive help pages, tutorials and videos are provided via a wiki page. Availability and Implementation: The web-interface is accessible via http://cgenome.net/calypso/. The software is programmed in Java, PERL and R and the source code is available from Zenodo (https://zenodo.org/record/50931). The software is freely available for non-commercial users. Contact: l.krause@uq.edu.au Supplementary information: Supplementary data are available at Bioinformatics online.
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                Author and article information

                Contributors
                hbjaspan@gmail.com
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                7 July 2018
                7 July 2018
                2018
                : 6
                : 124
                Affiliations
                [1 ]ISNI 0000 0004 1937 1151, GRID grid.7836.a, Institute of Infectious Diseases and Molecular Medicine, Department of Pathology, Division of Immunology, , University of Cape Town, ; Cape Town, South Africa
                [2 ]ISNI 0000 0004 1937 1151, GRID grid.7836.a, Institute of Infectious Diseases and Molecular Medicine, Department of Integrative Biomedical Sciences, Division of Computational Biology, , University of Cape Town, ; Cape Town, South Africa
                [3 ]ISNI 0000 0004 1936 7961, GRID grid.26009.3d, Duke University, ; Durham, NC USA
                [4 ]Ottawa Institute of Systems Biology, Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ontario, CA USA
                [5 ]ISNI 0000 0004 1936 7486, GRID grid.6572.6, Institute of Microbiology and Infection, , University of Birmingham, ; Birmingham, B15 2TT UK
                [6 ]ISNI 0000 0001 0217 6921, GRID grid.112485.b, Laboratory of Molecular and Experimental Immunology and Neurogenetics, UMR 7355, , CNRS-University of Orleans and Le Studium Institute for Advanced Studies, ; Rue Dupanloup, 45000 Orléans, France
                [7 ]ISNI 0000 0000 9026 4165, GRID grid.240741.4, Department of Pediatrics and Global Health, University of Washington and Center for Global Infectious Disease Research, , Seattle Children’s Research Institute, ; Seattle, WA USA
                [8 ]ISNI 0000 0000 9026 4165, GRID grid.240741.4, Present Address: Center for Global Infectious Disease Research, , Seattle Children’s Research Institute, ; Seattle, WA USA
                Author information
                http://orcid.org/0000-0002-0745-6073
                Article
                511
                10.1186/s40168-018-0511-7
                6035804
                29981583
                3a514517-b3a0-48f3-9e97-37b251b31256
                © The Author(s). 2018

                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
                : 17 February 2018
                : 2 July 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001323, Poliomyelitis Research Foundation;
                Award ID: 15/70
                Award ID: 15/16
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000192, Ontario Ministry of Economic Development and Innovation;
                Award ID: REG1-4450
                Award Recipient :
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                © The Author(s) 2018

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