The Gut Microbiota of Rural Papua New Guineans: Composition, Diversity Patterns, and Ecological Processes

Martínez, Inés; Stegen, James C.; Maldonado-Gómez, Maria X.; Eren, A. Murat; Siba, Peter M.; Greenhill, Andrew R.; Walter, Jens

doi:10.1016/j.celrep.2015.03.049

Title: The Gut Microbiota of Rural Papua New Guineans: Composition, Diversity Patterns, and Ecological Processes

Journal Article · Wed Apr 01 00:00:00 EDT 2015 · Cell Reports

DOI: https://doi.org/10.1016/j.celrep.2015.03.049 · OSTI ID:1182902

Martínez, Inés ^[1]; Stegen, James C. ^[2]; Maldonado-Gómez, Maria X. ^[3]; Eren, A. Murat ^[4]; Siba, Peter M. ^[5]; Greenhill, Andrew R. ^[6]; Walter, Jens ^[7]

Univ. of Alberta, Edmonton, AB (Canada); Univ. of Nebraska, Lincoln, NE (United States). Dept. of Food Science and Technology
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Div.
Univ. of Nebraska, Lincoln, NE (United States). Dept. of Food Science and Technology
Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Lab., Woods Hole, MA (United States)
Papua New Guinea Inst. of Medical Research, Goroka, Eastern Highlands Province (Papua New Guinea)
Papua New Guinea Inst. of Medical Research, Goroka, Eastern Highlands Province (Papua New Guinea); Federation Univ. Australia, Churchill, VIC (Australia). School of Applied and Biomedical Sciences
Univ. of Alberta, Edmonton, AB (Canada). Depts. of Agriculture, Food, and Nutritional Science, and Biological Sciences; Univ. of Nebraska, Lincoln, NE (United States). Dept. of Food Science and Technology

Comparisons between the fecal microbiota of humans from industrialized and non-industrialized communities indicate a pronounced impact of westernization on the diversity and composition of the human gut microbiota. However, the exact consequences of westernization on community characteristics are still insufficiently understood, and the ecological processes that drive differences have not been elucidated. Here we have compared the fecal microbiota of adults from two non-industrialized regions in Papua New Guinea (PNG) with that of United States (US) residents. Papua New Guineans harbor communities with greater bacterial diversity but lower inter-individual variation. Although the fecal microbiota in PNG and US was largely dominated by shared bacterial lineages, the relative abundance of 25 families, 45 genera, and 230 species-level OTUs differed, and 47 core OTUs in PNG were undetectable in US residents. To gain insight into the ecological mechanisms that cause the observed differences, we quantified community assembly processes in PNG and US microbiomes using a null modeling approach. This analysis demonstrated a significant higher rate of bacterial dispersal in PNG and divergent selective environments in the US. Interestingly, equivalent findings were obtained for other datasets comparing industrialized and non-industrialized microbiomes. Overall, the findings demonstrate a dominant role for microbial dispersal in shaping the human gut microbiota in non-industrialized societies, and point to differential selection pressures across individuals as a major factor shaping microbiomes associated with modern lifestyle.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (US)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1182902

Journal Information:: Cell Reports, Journal Name: Cell Reports Journal Issue: 4 Vol. 11; ISSN 2211-1247

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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The Gut Microbiota of Healthy Chilean Subjects Reveals a High Abundance of the Phylum Verrucomicrobia Fujio-Vejar, Sayaka; Vasquez, Yessenia; Morales, Pamela Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01221	journal	June 2017
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Ketamine interactions with gut-microbiota in rats: relevance to its antidepressant and anti-inflammatory properties Getachew, Bruk; Aubee, Joseph I.; Schottenfeld, Richard S. BMC Microbiology, Vol. 18, Issue 1 https://doi.org/10.1186/s12866-018-1373-7	journal	December 2018
Taxonomic features and comparisons of the gut microbiome from two edible fungus-farming termites (Macrotermes falciger; M. natalensis) harvested in the Vhembe district of Limpopo, South Africa Schnorr, Stephanie L.; Hofman, Courtney A.; Netshifhefhe, Shandukani R. BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1540-5	journal	July 2019
The human microbiome in evolution Davenport, Emily R.; Sanders, Jon G.; Song, Se Jin BMC Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12915-017-0454-7	journal	December 2017
Gut microbiota dysbiosis in male patients with chronic traumatic complete spinal cord injury Zhang, Chao; Zhang, Wenhao; Zhang, Jie Journal of Translational Medicine, Vol. 16, Issue 1 https://doi.org/10.1186/s12967-018-1735-9	journal	December 2018
Population structure of human gut bacteria in a diverse cohort from rural Tanzania and Botswana Hansen, Matthew E. B.; Rubel, Meagan A.; Bailey, Aubrey G. Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-018-1616-9	journal	January 2019
Convergence of human and Old World monkey gut microbiomes demonstrates the importance of human ecology over phylogeny Amato, Katherine R.; Mallott, Elizabeth K.; McDonald, Daniel Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1807-z	journal	October 2019
Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota Edwards, Joseph; Santos-Medellín, Christian; Nguyen, Bao Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1825-x	journal	October 2019
Ethnic and diet-related differences in the healthy infant microbiome Stearns, Jennifer C.; Zulyniak, Michael A.; de Souza, Russell J. Genome Medicine, Vol. 9, Issue 1 https://doi.org/10.1186/s13073-017-0421-5	journal	March 2017
Gut microbiome of native Arab Kuwaitis Plummer, Erica; Bulach, Dieter; Carter, Glen Gut Pathogens, Vol. 12, Issue 1 https://doi.org/10.1186/s13099-020-00351-y	journal	February 2020
Disease outbreak accompanies the dispersive structure of shrimp gut bacterial community with a simple core microbiota Yao, Zhiyuan; Yang, Kunjie; Huang, Lei AMB Express, Vol. 8, Issue 1 https://doi.org/10.1186/s13568-018-0644-x	journal	July 2018
Variable responses of human and non-human primate gut microbiomes to a Western diet Amato, Katherine R.; Yeoman, Carl J.; Cerda, Gabriela Microbiome, Vol. 3, Issue 1 https://doi.org/10.1186/s40168-015-0120-7	journal	November 2015
The microbiome of the built environment and mental health Hoisington, Andrew J.; Brenner, Lisa A.; Kinney, Kerry A. Microbiome, Vol. 3, Issue 1 https://doi.org/10.1186/s40168-015-0127-0	journal	December 2015
The roles of the outdoors and occupants in contributing to a potential pan-microbiome of the built environment: a review Leung, Marcus H. Y.; Lee, Patrick K. H. Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0165-2	journal	May 2016
Temporal dynamics of the gut microbiota in people sharing a confined environment, a 520-day ground-based space simulation, MARS500 Turroni, Silvia; Rampelli, Simone; Biagi, Elena Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0256-8	journal	March 2017
The Inuit gut microbiome is dynamic over time and shaped by traditional foods Dubois, Geneviève; Girard, Catherine; Lapointe, François-Joseph Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0370-7	journal	November 2017
Seasonal, spatial, and maternal effects on gut microbiome in wild red squirrels Ren, Tiantian; Boutin, Stan; Humphries, Murray M. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0382-3	journal	December 2017
Taxonomic profiling and populational patterns of bacterial bile salt hydrolase (BSH) genes based on worldwide human gut microbiome Song, Ziwei; Cai, Yuanyuan; Lao, Xingzhen Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0628-3	journal	January 2019
Microecological Koch’s postulates reveal that intestinal microbiota dysbiosis contributes to shrimp white feces syndrome Huang, Zhijian; Zeng, Shenzheng; Xiong, Jinbo Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00802-3	journal	March 2020
Variation in gut bacterial composition is associated with Haemonchus contortus parasite infection of sheep Mamun, Md. Abdullah Al; Sandeman, Mark; Rayment, Phil Animal Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/s42523-020-0021-3	journal	February 2020
Germ-free mice exhibit profound gut microbiota-dependent alterations of intestinal endocannabinoidome signaling Manca, Claudia; Boubertakh, Besma; Leblanc, Nadine Journal of Lipid Research, Vol. 61, Issue 1 https://doi.org/10.1194/jlr.ra119000424	journal	November 2019
Recent advances in modulating the microbiome Quigley, Eamonn M. M.; Gajula, Prianka F1000Research, Vol. 9 https://doi.org/10.12688/f1000research.20204.1	journal	January 2020
Experimental bacterial adaptation to the zebrafish gut reveals a primary role for immigration Robinson, Catherine D.; Klein, Helena S.; Murphy, Kyleah D. PLOS Biology, Vol. 16, Issue 12 https://doi.org/10.1371/journal.pbio.2006893	journal	December 2018
Methods for Improving Human Gut Microbiome Data by Reducing Variability through Sample Processing and Storage of Stool Gorzelak, Monika A.; Gill, Sandeep K.; Tasnim, Nishat PLOS ONE, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pone.0134802	journal	August 2015
In Vivo and In Vitro Detection of Luminescent and Fluorescent Lactobacillus reuteri and Application of Red Fluorescent mCherry for Assessing Plasmid Persistence Karimi, Shokoufeh; Ahl, David; Vågesjö, Evelina PLOS ONE, Vol. 11, Issue 3 https://doi.org/10.1371/journal.pone.0151969	journal	March 2016
Evolution in fecal bacterial/viral composition in infants of two central African countries (Gabon and Republic of the Congo) during their first month of life Brazier, Lionel; Elguero, Eric; Koumavor, Claudine Kombila PLOS ONE, Vol. 12, Issue 10 https://doi.org/10.1371/journal.pone.0185569	journal	October 2017
Disentangling factors that shape the gut microbiota in German Shepherd dogs Vilson, Åsa; Ramadan, Ziad; Li, Qinghong PLOS ONE, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pone.0193507	journal	March 2018
Ethnic and diet-related differences in the healthy infant microbiome Stearns, Jennifer C.; Zulyniak, Michael A.; De Souza, Russell J. BioMed Central https://doi.org/10.14288/1.0366940	text	January 2018
The microbiome and inborn errors of metabolism: Why we should look carefully at their interplay? Colonetti, Karina; Roesch, Luiz Fernando; Schwartz, Ida Vanessa Doederlein Genetics and Molecular Biology, Vol. 41, Issue 3 https://doi.org/10.1590/1678-4685-gmb-2017-0235	journal	September 2018
Evaluating the impact of domestication and captivity on the horse gut microbiome. Metcalf, Jessica L.; Song, Se Jin; Morton, James T. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.18005	text	January 2017
The role of gut microbiota in the health and disease of pigs Fouhse, J. M.; Zijlstra, R. T.; Willing, B. P. Animal Frontiers, Vol. 6, Issue 3 https://doi.org/10.2527/af.2016-0031	journal	July 2016
Seasonal, spatial, and maternal effects on gut microbiome in wild red squirrels Ren, Tiantian; Boutin, Stan; Humphries, Murray M. BioMed Central https://doi.org/10.25316/ir-366	text	January 2017
Role of Vitamin D in the Hygiene Hypothesis: The Interplay between Vitamin D, Vitamin D Receptors, Gut Microbiota, and Immune Response Clark, Allison; Mach, Núria Frontiers in Immunology, Vol. 7 https://doi.org/10.3389/fimmu.2016.00627	journal	December 2016
The Maternal Diet, Gut Bacteria, and Bacterial Metabolites during Pregnancy Influence Offspring Asthma Gray, Lawrence E. K.; O’Hely, Martin; Ranganathan, Sarath Frontiers in Immunology, Vol. 8 https://doi.org/10.3389/fimmu.2017.00365	journal	March 2017
Health Challenges of the Pacific Region: Insights From History, Geography, Social Determinants, Genetics, and the Microbiome Horwood, Paul F.; Tarantola, Arnaud; Goarant, Cyrille Frontiers in Immunology, Vol. 10 https://doi.org/10.3389/fimmu.2019.02184	journal	September 2019
Gut Microbiota Diversity and Human Diseases: Should We Reintroduce Key Predators in Our Ecosystem? Mosca, Alexis; Leclerc, Marion; Hugot, Jean P. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00455	journal	March 2016
Variations in the Post-weaning Human Gut Metagenome Profile As Result of Bifidobacterium Acquisition in the Western Microbiome Soverini, Matteo; Rampelli, Simone; Turroni, Silvia Frontiers in Microbiology, Vol. 07 https://doi.org/10.3389/fmicb.2016.01058	journal	July 2016
Impact of Westernized Diet on Gut Microbiota in Children on Leyte Island Nakayama, Jiro; Yamamoto, Azusa; Palermo-Conde, Ladie A. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00197	journal	February 2017
Geography, Ethnicity or Subsistence-Specific Variations in Human Microbiome Composition and Diversity Gupta, Vinod K.; Paul, Sandip; Dutta, Chitra Frontiers in Microbiology, Vol. 8, 16 p. https://doi.org/10.3389/fmicb.2017.01162	journal	June 2017
The Gut Microbiota of Healthy Chilean Subjects Reveals a High Abundance of the Phylum Verrucomicrobia Fujio-Vejar, Sayaka; Vasquez, Yessenia; Morales, Pamela Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01221	journal	June 2017
Linking the Gut Microbial Ecosystem with the Environment: Does Gut Health Depend on Where We Live? Tasnim, Nishat; Abulizi, Nijiati; Pither, Jason Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01935	journal	October 2017
Diet, Environments, and Gut Microbiota. A Preliminary Investigation in Children Living in Rural and Urban Burkina Faso and Italy De Filippo, Carlotta; Di Paola, Monica; Ramazzotti, Matteo Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01979	journal	October 2017
Gut Microbiota in Tibetan Herdsmen Reflects the Degree of Urbanization Li, Huan; Li, Tongtong; Li, Xiangzhen Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01745	journal	July 2018
The Gut Microbiota in the Pathogenesis and Therapeutics of Inflammatory Bowel Disease Zuo, Tao; Ng, Siew C. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02247	journal	September 2018
Gut Microbiome Biomarkers and Functional Diversity Within an Amazonian Semi-Nomadic Hunter–Gatherer Group Conteville, Liliane Costa; Oliveira-Ferreira, Joseli; Vicente, Ana Carolina Paulo Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01743	journal	July 2019
Reciprocal Interactions Between Gut Microbiota and Host Social Behavior Münger, Emmanuelle; Montiel-Castro, Augusto J.; Langhans, Wolfgang Frontiers in Integrative Neuroscience, Vol. 12 https://doi.org/10.3389/fnint.2018.00021	journal	June 2018
The Challenge of Maintaining a Healthy Microbiome during Long-Duration Space Missions Voorhies, Alexander A.; Lorenzi, Hernan A. Frontiers in Astronomy and Space Sciences, Vol. 3 https://doi.org/10.3389/fspas.2016.00023	journal	July 2016
Ecology and Evolution of the Human Microbiota: Fire, Farming and Antibiotics Gillings, Michael; Paulsen, Ian; Tetu, Sasha Genes, Vol. 6, Issue 3 https://doi.org/10.3390/genes6030841	journal	September 2015
Does Soil Contribute to the Human Gut Microbiome? Blum, Winfried E. H.; Zechmeister-Boltenstern, Sophie; Keiblinger, Katharina M. Microorganisms, Vol. 7, Issue 9 https://doi.org/10.3390/microorganisms7090287	journal	August 2019
Elevation is Associated with Human Skin Microbiomes Li, Huan; Wang, Yijie; Yu, Qiaoling Microorganisms, Vol. 7, Issue 12 https://doi.org/10.3390/microorganisms7120611	journal	November 2019
Intestinal Barrier Function in Chronic Kidney Disease Meijers, Björn; Farré, Ricard; Dejongh, Sander Toxins, Vol. 10, Issue 7 https://doi.org/10.3390/toxins10070298	journal	July 2018
Understanding the prebiotic potential of different dietary fibers using an in vitro continuous adult fermentation model (PolyFermS) Poeker, Sophie A.; Geirnaert, Annelies; Berchtold, Laura ETH Zurich https://doi.org/10.3929/ethz-b-000249737	text	January 2018
Microbial transmission from mother to child: improving infant intestinal microbiota development by identifying the obstacles Daele, Emmy Van; Knol, Jan; Belzer, Clara Taylor & Francis https://doi.org/10.6084/m9.figshare.11508696	text	January 2020
Resilience of small intestinal beneficial bacteria to the toxicity of soybean oil fatty acids Di Rienzi, Sara C.; Jacobson, Juliet; Kennedy, Elizabeth A. eLife, Vol. 7 https://doi.org/10.7554/elife.32581	journal	March 2018
Experimental evaluation of the importance of colonization history in early-life gut microbiota assembly Martínez, Inés; Maldonado-Gomez, Maria X.; Gomes-Neto, João Carlos eLife, Vol. 7 https://doi.org/10.7554/elife.36521	journal	September 2018

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