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      Functional diversity of microbial ecologies estimated from ancient human coprolites and dental calculus

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          Abstract

          Human microbiome studies are increasingly incorporating macroecological approaches, such as community assembly, network analysis and functional redundancy to more fully characterize the microbiome. Such analyses have not been applied to ancient human microbiomes, preventing insights into human microbiome evolution. We address this issue by analysing published ancient microbiome datasets: coprolites from Rio Zape ( n = 7; 700 CE Mexico) and historic dental calculus ( n = 44; 1770–1855 CE, UK), as well as two novel dental calculus datasets: Maya ( n = 7; 170 BCE-885 CE, Belize) and Nuragic Sardinians ( n = 11; 1400–850 BCE, Italy). Periodontitis-associated bacteria ( Treponema denticola, Fusobacterium nucleatum and Eubacterium saphenum) were identified as keystone taxa in the dental calculus datasets. Coprolite keystone taxa included known short-chain fatty acid producers ( Eubacterium biforme, Phascolarctobacterium succinatutens) and potentially disease-associated bacteria ( Escherichia, Brachyspira). Overlap in ecological profiles between ancient and modern microbiomes was indicated by similarity in functional response diversity profiles between contemporary hunter–gatherers and ancient coprolites, as well as parallels between ancient Maya, historic UK, and modern Spanish dental calculus; however, the ancient Nuragic dental calculus shows a distinct ecological structure. We detected key ecological signatures from ancient microbiome data, paving the way to expand understanding of human microbiome evolution.

          This article is part of the theme issue ‘Insights into health and disease from ancient biomolecules’.

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          A metagenome-wide association study of gut microbiota in type 2 diabetes.

          Assessment and characterization of gut microbiota has become a major research area in human disease, including type 2 diabetes, the most prevalent endocrine disease worldwide. To carry out analysis on gut microbial content in patients with type 2 diabetes, we developed a protocol for a metagenome-wide association study (MGWAS) and undertook a two-stage MGWAS based on deep shotgun sequencing of the gut microbial DNA from 345 Chinese individuals. We identified and validated approximately 60,000 type-2-diabetes-associated markers and established the concept of a metagenomic linkage group, enabling taxonomic species-level analyses. MGWAS analysis showed that patients with type 2 diabetes were characterized by a moderate degree of gut microbial dysbiosis, a decrease in the abundance of some universal butyrate-producing bacteria and an increase in various opportunistic pathogens, as well as an enrichment of other microbial functions conferring sulphate reduction and oxidative stress resistance. An analysis of 23 additional individuals demonstrated that these gut microbial markers might be useful for classifying type 2 diabetes.
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            A core gut microbiome in obese and lean twins

            The human distal gut harbors a vast ensemble of microbes (the microbiota) that provide us with important metabolic capabilities, including the ability to extract energy from otherwise indigestible dietary polysaccharides1–6. Studies of a small number of unrelated, healthy adults have revealed substantial diversity in their gut communities, as measured by sequencing 16S rRNA genes6–8, yet how this diversity relates to function and to the rest of the genes in the collective genomes of the microbiota (the gut microbiome) remains obscure. Studies of lean and obese mice suggest that the gut microbiota affects energy balance by influencing the efficiency of calorie harvest from the diet, and how this harvested energy is utilized and stored3–5. To address the question of how host genotype, environmental exposures, and host adiposity influence the gut microbiome, we have characterized the fecal microbial communities of adult female monozygotic and dizygotic twin pairs concordant for leanness or obesity, and their mothers. Analysis of 154 individuals yielded 9,920 near full-length and 1,937,461 partial bacterial 16S rRNA sequences, plus 2.14 gigabases from their microbiomes. The results reveal that the human gut microbiome is shared among family members, but that each person’s gut microbial community varies in the specific bacterial lineages present, with a comparable degree of co-variation between adult monozygotic and dizygotic twin pairs. However, there was a wide array of shared microbial genes among sampled individuals, comprising an extensive, identifiable ‘core microbiome’ at the gene, rather than at the organismal lineage level. Obesity is associated with phylum-level changes in the microbiota, reduced bacterial diversity, and altered representation of bacterial genes and metabolic pathways. These results demonstrate that a diversity of organismal assemblages can nonetheless yield a core microbiome at a functional level, and that deviations from this core are associated with different physiologic states (obese versus lean).
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              Obesity alters gut microbial ecology.

              We have analyzed 5,088 bacterial 16S rRNA gene sequences from the distal intestinal (cecal) microbiota of genetically obese ob/ob mice, lean ob/+ and wild-type siblings, and their ob/+ mothers, all fed the same polysaccharide-rich diet. Although the majority of mouse gut species are unique, the mouse and human microbiota(s) are similar at the division (superkingdom) level, with Firmicutes and Bacteroidetes dominating. Microbial-community composition is inherited from mothers. However, compared with lean mice and regardless of kinship, ob/ob animals have a 50% reduction in the abundance of Bacteroidetes and a proportional increase in Firmicutes. These changes, which are division-wide, indicate that, in this model, obesity affects the diversity of the gut microbiota and suggest that intentional manipulation of community structure may be useful for regulating energy balance in obese individuals. The sequences reported in this paper have been deposited in the GenBank database [accession nos. DQ 014552--DQ 015671 (mothers) and AY 989911--AY 993908 (offspring)].
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                Author and article information

                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos Trans R Soc Lond B Biol Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                23 November 2020
                05 October 2020
                05 October 2020
                : 375
                : 1812 , Theme issue ‘Insights into health and disease from ancient biomolecules’ compiled and edited by Anne C. Stone, Verena J. Schuenemann and Cecil M. Lewis
                : 20190586
                Affiliations
                [1 ]Laboratories of Molecular Anthropology and Microbiome Research (LMAMR), University of Oklahoma , Norman, OK, USA
                [2 ]Department of Anthropology, University of Oklahoma , Norman, OK, USA
                [3 ]Department of Sociology, Anthropology, and Social Work, Texas Tech University , Lubbock, TX, USA
                [4 ]Department of Anthropology, Northwestern University , Evanston, IL, USA
                [5 ]Department of Life and Environmental Sciences, University of Cagliari , Cagliari, Sardinia, Italy
                Author notes

                One contribution of 14 to a theme issue ‘ Insights into health and disease from ancient biomolecules’.

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.5095994.

                Author information
                http://orcid.org/0000-0001-5271-9162
                http://orcid.org/0000-0002-2490-5870
                http://orcid.org/0000-0002-2198-3427
                Article
                rstb20190586
                10.1098/rstb.2019.0586
                7702801
                33012230
                a5acb386-c424-4115-bfeb-adb2ef3d4301
                © 2020 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 13 July 2020
                Funding
                Funded by: The Alphawood Foundation;
                Funded by: National Institute of General Medical Sciences, http://dx.doi.org/10.13039/100000057;
                Award ID: NIH R01 GM089886
                Categories
                1001
                60
                200
                Articles
                Research Article
                Custom metadata
                November 23, 2020

                Philosophy of science
                dental calculus,coprolites,microbiome,resilience,keystone,networks
                Philosophy of science
                dental calculus, coprolites, microbiome, resilience, keystone, networks

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