in

The microbiome and resistome of chimpanzees, gorillas, and humans across host lifestyle and geography

  • 1.

    Hicks AL, Lee KJ, Couto-Rodriguez M, Patel J, Sinha R, Guo C, et al. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat Commun. 2018;9:1786.

    • Google Scholar
  • 2.

    Clayton JB, Vangay P, Huang H, Ward T, Hillmann BM, Al-Ghalith GA, et al. Captivity humanizes the primate microbiome. Proc Natl Acad Sci. 2016;113:10376.

    • Google Scholar
  • 3.

    Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222.

    • Google Scholar
  • 4.

    Clemente JC, Pehrsson EC, Blaser MJ, Sandhu K, Gao Z, Wang B, et al. The microbiome of uncontacted Amerindians. Sci Adv. 2015;1:e1500183.

    • Google Scholar
  • 5.

    Obregon-Tito AJ, Tito RY, Metcalf J, Sankaranarayanan K, Clemente JC, Ursell LK, et al. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat Commun. 2015;6:6505.

    • Google Scholar
  • 6.

    Rampelli S, Schnorr SL, Consolandi C, Turroni S, Severgnini M, Peano C, et al. Metagenome sequencing of the Hadza hunter-gatherer gut microbiota. Curr Biol. 2015;25:1682–93.

    • Google Scholar
  • 7.

    Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G, et al. Gut microbiome of the Hadza hunter-gatherers. Nat Commun. 2014;5:3654.

    • Google Scholar
  • 8.

    Gomez A, Petrzelkova KJ, Burns MB, Yeoman CJ, Amato KR, Vlckova K, et al. Gut microbiome of coexisting BaAka pygmies and Bantu reflects gradients of traditional subsistence patterns. Cell Rep. 2016;14:2142–53.

    • Google Scholar
  • 9.

    David LA, Materna AC, Friedman J, Campos-Baptista MI, Blackburn MC, Perrotta A, et al. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 2014;15:R89.

    • Google Scholar
  • 10.

    Tsukayama P, Boolchandani M, Patel S, Pehrsson EC, Gibson MK, Chiou KL, et al. Characterization of wild and captive baboon gut microbiota and their antibiotic resistomes. mSystems. 2018;3:e00016–18.

    • Google Scholar
  • 11.

    Moeller AH, Caro-Quintero A, Mjungu D, Georgiev AV, Lonsdorf EV, Muller MN, et al. Cospeciation of gut microbiota with hominids. Science. 2016;353:380.

    • Google Scholar
  • 12.

    Moeller AH, Li Y, Mpoudi Ngole E, Ahuka-Mundeke S, Lonsdorf EV, Pusey AE, et al. Rapid changes in the gut microbiome during human evolution. Proc Natl Acad Sci USA. 2014;111:16431–5.

    • Google Scholar
  • 13.

    Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science. 2008;320:1647–51.

    • Google Scholar
  • 14.

    Moeller AH, Peeters M, Ndjango JB, Li Y, Hahn BH, Ochman H. Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res. 2013;23:1715–20.

    • Google Scholar
  • 15.

    Rwego IB, Isabirye-Basuta G, Gillespie TR, Goldberg TL. Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv Biol. 2008;22:1600–7.

    • Google Scholar
  • 16.

    Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, et al. Cohabiting family members share microbiota with one another and with their dogs. eLife. 2013;2:e00458.

    • Google Scholar
  • 17.

    Dunay E, Apakupakul K, Leard S, Palmer JL, Deem SL. Pathogen transmission from humans to great apes is a growing threat to primate conservation. EcoHealth. 2018;15:148–62.

    • Google Scholar
  • 18.

    Walsh PD, Abernethy KA, Bermejo M, Beyers R, De Wachter P, Akou ME, et al. Catastrophic ape decline in western equatorial Africa. Nature. 2003;422:611–4.

    • Google Scholar
  • 19.

    Wittemyer G, Elsen P, Bean WT, Burton ACO, Brashares JS. Accelerated human population growth at protected area edges. Science. 2008;321:123.

    • Google Scholar
  • 20.

    Kondgen S, Kuhl H, N’Goran PK, Walsh PD, Schenk S, Ernst N, et al. Pandemic human viruses cause decline of endangered great apes. Curr Biol. 2008;18:260–4.

    • Google Scholar
  • 21.

    Gomez A, Rothman JM, Petrzelkova K, Yeoman CJ, Vlckova K, Umaña JD, et al. Temporal variation selects for diet–microbe co-metabolic traits in the gut of Gorilla spp. ISMEJ. 2015;10:514.

    • Google Scholar
  • 22.

    Fujimura KE, Slusher NA, Cabana MD, Lynch SV. Role of the gut microbiota in defining human health. Expert Rev Anti Infect Ther. 2010;8:435–54.

    • Google Scholar
  • 23.

    King T, Chamerlan C. Orphan gorilla management and reintroduction: progress and perspectives. Gorilla J. 2007;34:21–5.

    • Google Scholar
  • 24.

    Pehrsson EC, Tsukayama P, Patel S, Mejía-Bautista M, Sosa-Soto G, Navarrete KM, et al. Interconnected microbiomes and resistomes in low-income human habitats. Nature. 2016;533:212.

    • Google Scholar
  • 25.

    Porse A, Gumpert H, Kubicek-Sutherland JZ, Karami N, Adlerberth I, Wold AE, et al. Genome dynamics of Escherichia coli during antibiotic treatment: transfer, loss, and persistence of genetic elements in situ of the infant gut. Front Cell Infect Microbiol. 2017;7:126.

    • Google Scholar
  • 26.

    Ferreiro A, Crook N, Gasparrini AJ, Dantas G. Multiscale evolutionary dynamics of host-associated microbiomes. Cell. 2018;172:1216–27.

    • Google Scholar
  • 27.

    D’Costa VM, King CE, Kalan L, Morar M, Sung WWL, Schwarz C, et al. Antibiotic resistance is ancient. Nature. 2011;477:457.

    • Google Scholar
  • 28.

    Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G. The shared antibiotic resistome of soil bacteria and human pathogens. Science. 2012;337:1107–11.

    • Google Scholar
  • 29.

    Karami N, Martner A, Enne VI, Swerkersson S, Adlerberth I, Wold AE. Transfer of an ampicillin resistance gene between two Escherichia coli strains in the bowel microbiota of an infant treated with antibiotics. J Antimicrob Chemother. 2007;60:1142–5.

    • Google Scholar
  • 30.

    Sommer MOA, Dantas G, Church GM. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science. 2009;325:1128–31.

    • Google Scholar
  • 31.

    Smits SA, Leach J, Sonnenburg ED, Gonzalez CG, Lichtman JS, Reid G, et al. Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. Science. 2017;357:802.

    • Google Scholar
  • 32.

    Ellis RJ, Bruce KD, Jenkins C, Stothard JR, Ajarova L, Mugisha L, et al. Comparison of the distal gut microbiota from people and animals in Africa. PloS One. 2013;8:e54783.

    • Google Scholar
  • 33.

    Morgan D, Sanz C. Naive encounters with chimpanzees in the Goualougo Triangle, Republic of Congo. Int J Primatol. 2003;24:369–81.

    • Google Scholar
  • 34.

    Wilson ML, Boesch C, Fruth B, Furuichi T, Gilby IC, Hashimoto C, et al. Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature. 2014;513:414.

    • Google Scholar
  • 35.

    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.

    • Google Scholar
  • 36.

    McKenzie VJ, Song SJ, Delsuc F, Prest TL, Oliverio AM, Korpita TM, et al. The effects of captivity on the mammalian gut microbiome. Integr Comp Biol. 2017;57:690–704.

    • Google Scholar
  • 37.

    Basabose AK. Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. Am J Primatol. 2002;58:1–21.

    • Google Scholar
  • 38.

    Calvert JJ. Food selection by western gorillas (G.g. gorilla) in relation to food chemistry. Oecologia. 1985;65:236–46.

    • Google Scholar
  • 39.

    Elizabeth Rogers M, Maisels F, Williamson EA, Fernandez M, Tutin CE. Gorilla diet in the Lope Reserve, Gabon:: a nutritional analysis. Oecologia. 1990;84:326–39.

    • Google Scholar
  • 40.

    Martinez-Medina M, Denizot J, Dreux N, Robin F, Billard E, Bonnet R, et al. Western diet induces dysbiosis with increased E coli in CEABAC10 mice, alters host barrier function favouring AIEC colonisation. Gut. 2014;63:116–24.

    • Google Scholar
  • 41.

    Vangay P, Johnson AJ, Ward TL, Al-Ghalith GA, Shields-Cutler RR, Hillmann BM, et al. US immigration westernizes the human gut microbiome. Cell. 2018;175:962–72.

    • Google Scholar
  • 42.

    Less EH, Lukas KE, Bergl R, Ball R, Kuhar CW, Lavin SR, et al. Implementing a low-starch biscuit-free diet in zoo gorillas: the impact on health. Zoo Biol. 2014;33:74–80.

    • Google Scholar
  • 43.

    Greene LK, Bornbusch SL, McKenney EA, Harris RL, Gorvetzian SR, Yoder AD, et al. The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs. Am J Primatol. 2019;81:e22974.

    • Google Scholar
  • 44.

    AZA Gorilla Species Survival Plan. Gorilla Care Manual. Silver Spring, MD: Association of Zoos and Aquariums; 2017.

    • Google Scholar
  • 45.

    AZA Ape TAG. Chimpanzee (Pan troglodytes) Care Manual. Association of Zoos and Aquariums, Silver Spring, MD. 2010.

  • 46.

    Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60.

    • Google Scholar
  • 47.

    Amato KR, Yeoman CJ, Cerda G, A. Schmitt C, Cramer JD, Miller MEB, et al. Variable responses of human and non-human primate gut microbiomes to a Western diet. Microbiome. 2015;3:53.

    • Google Scholar
  • 48.

    Precup G, Vodnar DC. Gut Prevotella as a possible biomarker of diet and its eubiotic versus dysbiotic roles: a comprehensive literature review. Br J Nutr. 2019;122:131–40.

    • Google Scholar
  • 49.

    De Filippis F, Pasolli E, Tett A, Tarallo S, Naccarati A, De Angelis M, et al. Distinct genetic and functional traits of human intestinal prevotella copri strains are associated with different habitual diets. Cell Host Microbe. 2019;25:444–53.e3.

    • Google Scholar
  • 50.

    Han C, Gronow S, Teshima H, Lapidus A, Nolan M, Lucas S, et al. Complete genome sequence of Treponema succinifaciens type strain (6091). Stand Genom Sci. 2011;4:361–70.

    • Google Scholar
  • 51.

    Soverini M, Rampelli S, Turroni S, Schnorr SL, Quercia S, Castagnetti A, et al. Variations in the post-weaning human gut metagenome profile as result of bifidobacterium acquisition in the western microbiome. Front Microbiol. 2016;7:1058.

    • Google Scholar
  • 52.

    Suzek BE, Wang Y, Huang H, McGarvey PB, Wu CH, Consortium tU. UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches. Bioinformatics. 2014;31:926–32.

    • Google Scholar
  • 53.

    Franzosa EA, McIver LJ, Rahnavard G, Thompson LR, Schirmer M, Weingart G, et al. Species-level functional profiling of metagenomes and metatranscriptomes. Nat Methods. 2018;15:962–8.

    • Google Scholar
  • 54.

    Caspi R, Billington R, Fulcher CA, Keseler IM, Kothari A, Krummenacker M, et al. The MetaCyc database of metabolic pathways and enzymes. Nucleic Acids Res. 2018;46:D633–39.

    • Google Scholar
  • 55.

    Fernandez CI, Wiley AS. Rethinking the starch digestion hypothesis for AMY1 copy number variation in humans. Am J Phys Anthropol. 2017;163:645–57.

    • Google Scholar
  • 56.

    Boolchandani M, Patel S, Dantas G. Functional metagenomics to study antibiotic resistance. Methods Mol Biol. 2017;1520:307–29.

    • Google Scholar
  • 57.

    Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 2017;45:D566–73.

    • Google Scholar
  • 58.

    Kaminski J, Gibson MK, Franzosa EA, Segata N, Dantas G, Huttenhower C. High-specificity targeted functional profiling in microbial communities with ShortBRED. PLOS Comput Biol. 2015;11:e1004557.

    • Google Scholar
  • 59.

    Ramirez MS, Tolmasky ME. Aminoglycoside modifying enzymes. Drug Resist Updat. 2010;13:151–71.

    • Google Scholar
  • 60.

    Wachino J, Arakawa Y. Exogenously acquired 16S rRNA methyltransferases found in aminoglycoside-resistant pathogenic Gram-negative bacteria: an update. Drug Resist Updat. 2012;15:133–48.

    • Google Scholar
  • 61.

    Galimand M, Courvalin P, Lambert T. Plasmid-mediated high-level resistance to aminoglycosides in Enterobacteriaceae due to 16S rRNA methylation. Antimicrobial agents Chemother. 2003;47:2565–71.

    • Google Scholar
  • 62.

    Vlckova K, Gomez A, Petrzelkova KJ, Whittier CA, Todd AF, Yeoman CJ, et al. Effect of antibiotic treatment on the gastrointestinal microbiome of free-ranging Western Lowland Gorillas (Gorilla g. gorilla). Micro Ecol. 2016;72:943–54.

    • Google Scholar
  • 63.

    Fair RJ, Tor Y. Antibiotics and bacterial resistance in the 21st century. Perspect Med Chem. 2014;6:25–64.

    • Google Scholar
  • 64.

    Gillings MR. Evolutionary consequences of antibiotic use for the resistome, mobilome and microbial pangenome. Front Microbiol. 2013;4:4.

    • Google Scholar
  • 65.

    Forsberg KJ, Patel S, Wencewicz TA, Dantas G. The tetracycline destructases: a novel family of tetracycline-inactivating enzymes. Chem Biol. 2015;22:888–97.

    • Google Scholar
  • 66.

    Jørgensen TS, Kiil AS, Hansen MA, Sørensen SJ, Hansen LH. Current strategies for mobilome research. Front Microbiol. 2015;5:750.

    • Google Scholar
  • 67.

    Sorensen SJ, Bailey M, Hansen LH, Kroer N, Wuertz S. Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol. 2005;3:700–10.

    • Google Scholar
  • 68.

    Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature. 2010;467:420–5.

    • Google Scholar
  • 69.

    Nishida AH, Ochman H. A great-ape view of the gut microbiome. Nat Rev Genet. 2019;20:195–206.

    • Google Scholar
  • 70.

    Leroy EM, Rouquet P, Formenty P, Souquiere S, Kilbourne A, Froment JM, et al. Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science. 2004;303:387–90.

    • Google Scholar
  • 71.

    Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis. 2016;16:161–8.

    • Google Scholar
  • 72.

    Schuchat A, Hilger T, Zell E, Farley MM, Reingold A, Harrison L, et al. Active bacterial core surveillance of the emerging infections program network. Emerg Infect Dis. 2001;7:92–9.

    • Google Scholar
  • 73.

    Roca I, Akova M, Baquero F, Carlet J, Cavaleri M, Coenen S, et al. The global threat of antimicrobial resistance: science for intervention. N. Microbes N. Infect. 2015;6:22–9.

    • Google Scholar
  • 74.

    Morgan D, Mundry R, Sanz C, Ayina CE, Strindberg S, Lonsdorf E, et al. African apes coexisting with logging: Comparing chimpanzee (Pan troglodytes troglodytes) and gorilla (Gorilla gorilla gorilla) resource needs and responses to forestry activities. Biol Conserv. 2018;218:277–86.

    • Google Scholar
  • 75.

    Junker J, Blake S, Boesch C, Campbell G, Toit Ld, Duvall C, et al. Recent decline in suitable environmental conditions for African great apes. Diversity Distrib. 2012;18:1077–91.

    • Google Scholar
  • 76.

    Biswas S, Brunel J-M, Dubus J-C, Reynaud-Gaubert M, Rolain J-M. Colistin: an update on the antibiotic of the 21st century. Expert Rev Anti-infective Ther. 2012;10:917–34.

    • Google Scholar
  • 77.

    Nielsen HB, Almeida M, Juncker AS, Rasmussen S, Li J, Sunagawa S, et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat Biotechnol. 2014;32:822–8.

    • Google Scholar
  • 78.

    AbuOun M, Stubberfield EJ, Duggett NA, Kirchner M, Dormer L, Nunez-Garcia J, et al. mcr-1 and mcr-2 variant genes identified in Moraxella species isolated from pigs in Great Britain from 2014 to 2015. J Antimicrob Chemother. 2017;72:2745–9.

    • Google Scholar
  • 79.

    Poirel L, Kieffer N, Fernandez-Garayzabal JF, Vela AI, Larpin Y, Nordmann P. MCR-2-mediated plasmid-borne polymyxin resistance most likely originates from Moraxella pluranimalium. J Antimicrob Chemother. 2017;72:2947–9.

    • Google Scholar
  • 80.

    Wei W, Srinivas S, Lin J, Tang Z, Wang S, Ullah S, et al. Defining ICR-Mo, an intrinsic colistin resistance determinant from Moraxella osloensis. PLOS Genet. 2018;14:e1007389.

    • Google Scholar
  • 81.

    Koren O, Knights D, Gonzalez A, Waldron L, Segata N, Knight R, et al. A guide to enterotypes across the human body: meta-analysis of microbial community structures in human microbiome datasets. PLoS Comput Biol. 2013;9:e1002863.

    • Google Scholar
  • 82.

    Pasolli E, Truong DT, Malik F, Waldron L, Segata N. Machine learning meta-analysis of large metagenomic datasets: tools and biological insights. PLOS Comput Biol. 2016;12:e1004977.

    • Google Scholar
  • 83.

    Martinez I, Stegen JC, Maldonado-Gomez MX, Eren AM, Siba PM, Greenhill AR, et al. The gut microbiota of rural papua new guineans: composition, diversity patterns, and ecological processes. Cell Rep. 2015;11:527–38.

    • Google Scholar
  • 84.

    Kunin CM, Lipton HL, Tupasi T, Sacks T, Scheckler WE, Jivani A, et al. Social, behavioral, and practical factors affecting antibiotic use worldwide: report of Task Force 4. Rev Infect Dis. 1987;9:S270–85.

    • Google Scholar
  • 85.

    Parnell R. Signification et interpretation des pistes et traces d’animaux. In: White L, Edwards A, (editors.) Conservation en foret pluviale africaine: Methods de recherche. New York: Wildlife Conservation Society; 2000. p. 153–86.

  • 86.

    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISMEJ. 2012;6:1621–4.

    • Google Scholar
  • 87.

    Baym M, Kryazhimskiy S, Lieberman TD, Chung H, Desai MM, Kishony R. Inexpensive multiplexed library preparation for megabase-sized genomes. PloS One. 2015;10:e0128036.

    • Google Scholar
  • 88.

    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581.

    • Google Scholar
  • 89.

    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.

    • Google Scholar
  • 90.

    McMurdie PJ, Holmes S. phyloseq: An R Package for reproducible interactive analysis and graphics of microbiome census data. PloS one. 2013;8:e61217.

    • Google Scholar
  • 91.

    Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2010;27:592–3.

    • Google Scholar
  • 92.

    Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.

    • Google Scholar
  • 93.

    Schmieder R, Edwards R. Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PloS One. 2011;6:e17288.

    • Google Scholar
  • 94.

    Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27:863–4.

    • Google Scholar
  • 95.

    Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods. 2012;9:811.

    • Google Scholar
  • 96.

    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Vegan: community ecology package. R package version 2.5-4 ed. 2019. https://CRAN.R-project.org/package=vegan.

  • 97.

    Martinez Abizu P. PairwiseAdonis: pairwise multilevel comparison using adonis. R package version 03. 2019. https://github.com/pmartinezarbizu/pairwiseAdonis.

  • 98.

    Gibson MK, Forsberg KJ, Dantas G. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. Isme j. 2015;9:207–16.

    • Google Scholar
  • 99.

    Andrews S. FastQC: a quality control tool for high throughput sequence data. 2010. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.


  • Source: Ecology - nature.com

    Staring into the vortex

    Marine virus predation by non-host organisms