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Traditional Human Populations and Nonhuman Primates Show Parallel Gut Microbiome Adaptations to Analogous Ecological Conditions

. 2020 Dec 22 ; 5 (6) : . [epub] 20201222

Status PubMed-not-MEDLINE Language English Country United States Media electronic

Document type Journal Article

Persistent link   https://www.medvik.cz/link/pmid33361321

Compared with urban-industrial populations, small-scale human communities worldwide share a significant number of gut microbiome traits with nonhuman primates. This overlap is thought to be driven by analogous dietary triggers; however, the ecological and functional bases of this similarity are not fully understood. To start addressing this issue, fecal metagenomes of BaAka hunter-gatherers and traditional Bantu agriculturalists from the Central African Republic were profiled and compared with those of a sympatric western lowland gorilla group (Gorilla gorilla gorilla) across two seasons of variable dietary intake. Results show that gorilla gut microbiomes shared similar functional traits with each human group, depending on seasonal dietary behavior. Specifically, parallel microbiome traits were observed between hunter-gatherers and gorillas when the latter consumed more structural polysaccharides during dry seasons, while small-scale agriculturalist and gorilla microbiomes showed significant functional overlap when gorillas consumed more seasonal ripe fruit during wet seasons. Notably, dominance of microbial transporters, transduction systems, and gut xenobiotic metabolism was observed in association with traditional agriculture and energy-dense diets in gorillas at the expense of a functional microbiome repertoire capable of metabolizing more complex polysaccharides. Differential abundance of bacterial taxa that typically distinguish traditional from industrialized human populations (e.g., Prevotella spp.) was also recapitulated in the human and gorilla groups studied, possibly reflecting the degree of polysaccharide complexity included in each group's dietary niche. These results show conserved functional gut microbiome adaptations to analogous diets in small-scale human populations and nonhuman primates, highlighting the role of plant dietary polysaccharides and diverse environmental exposures in this convergence.IMPORTANCE The results of this study highlight parallel gut microbiome traits in human and nonhuman primates, depending on subsistence strategy. Although these similarities have been reported before, the functional and ecological bases of this convergence are not fully understood. Here, we show that this parallelism is, in part, likely modulated by the complexity of plant carbohydrates consumed and by exposures to diverse xenobiotics of natural and artificial origin. Furthermore, we discuss how divergence from these parallel microbiome traits is typically associated with adverse health outcomes in human populations living under culturally westernized subsistence patterns. This is important information as we trace the specific dietary and environmental triggers associated with the loss and gain of microbial functions as humans adapt to various dietary niches.

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Moeller AH, Caro-Quintero A, Mjungu D, Georgiev AV, Lonsdorf EV, Muller MN, Pusey AE, Peeters M, Hahn BH, Ochman H. 2016. Cospeciation of gut microbiota with hominids. Science 353:380–382. doi:10.1126/science.aaf3951. PubMed DOI PMC

Ochman H, Worobey M, Kuo C-H, Ndjango J-BN, Peeters M, Hahn BH, Hugenholtz P. 2010. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol 8:e1000546. doi:10.1371/journal.pbio.1000546. PubMed DOI PMC

Amato KR, Sanders JG, Song SJ, Nute M, Metcalf JL, Thompson LR, Morton JT, Amir A, McKenzie VJ, Humphrey G, Gogul G, Gaffney J, Baden AL, Britton GAO, Cuozzo FP, Di Fiore A, Dominy NJ, Goldberg TL, Gomez A, Kowalewski MM, Lewis RJ, Link A, Sauther ML, Tecot S, White BA, Nelson KE, Stumpf RM, Knight R, Leigh SR. 2019. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J 13:576–587. doi:10.1038/s41396-018-0175-0. PubMed DOI PMC

Amato KR, Mallott EK, McDonald D, Dominy NJ, Goldberg T, Lambert JE, Swedell L, Metcalf JL, Gomez A, Britton GAO, Stumpf RM, Leigh SR, Knight R. 2019. Convergence of human and Old World monkey gut microbiomes demonstrates the importance of human ecology over phylogeny. Genome Biol 20:201. doi:10.1186/s13059-019-1807-z. PubMed DOI PMC

Gomez A, Sharma AK, Mallott EK, Petrzelkova KJ, Jost Robinson CA, Yeoman CJ, Carbonero F, Pafco B, Rothman JM, Ulanov A, Vlckova K, Amato KR, Schnorr SL, Dominy NJ, Modry D, Todd A, Torralba M, Nelson KE, Burns MB, Blekhman R, Remis M, Stumpf RM, Wilson BA, Gaskins HR, Garber PA, White BA, Leigh SR. 2019. Plasticity in the human gut microbiome defies evolutionary constraints. mSphere 4:e00271-19. doi:10.1128/mSphere.00271-19. PubMed DOI PMC

Moeller AH, Li Y, Mpoudi Ngole E, Ahuka-Mundeke S, Lonsdorf EV, Pusey AE, Peeters M, Hahn BH, Ochman H. 2014. Rapid changes in the gut microbiome during human evolution. Proc Natl Acad Sci U S A 111:16431–16435. doi:10.1073/pnas.1419136111. PubMed DOI PMC

Gomez A, Petrzelkova KJ, Burns MB, Yeoman CJ, Amato KR, Vlckova K, Modry D, Todd A, Jost Robinson CA, Remis MJ, Torralba MG, Morton E, Umaña JD, Carbonero F, Gaskins HR, Nelson KE, Wilson BA, Stumpf RM, White BA, Leigh SR, Blekhman R. 2016. Gut microbiome of coexisting BaAka pygmies and Bantu reflects gradients of traditional subsistence patterns. Cell Rep 14:2142–2153. doi:10.1016/j.celrep.2016.02.013. PubMed DOI

Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G, Turroni S, Biagi E, Peano C, Severgnini M, Fiori J, Gotti R, De Bellis G, Luiselli D, Brigidi P, Mabulla A, Marlowe F, Henry AG, Crittenden AN. 2014. Gut microbiome of the Hadza hunter-gatherers. Nat Commun 5:3654. doi:10.1038/ncomms4654. PubMed DOI PMC

Clayton JB, Vangay P, Huang H, Ward T, Hillmann BM, Al-Ghalith GA, Travis DA, Long HT, Van Tuan B, Van Minh V, Cabana F, Nadler T, Toddes B, Murphy T, Glander KE, Johnson TJ, Knights D. 2016. Captivity humanizes the primate microbiome. Proc Natl Acad Sci U S A 113:10376–10381. doi:10.1073/pnas.1521835113. PubMed DOI PMC

Candela M, Biagi E, Maccaferri S, Turroni S, Brigidi P. 2012. Intestinal microbiota is a plastic factor responding to environmental changes. Trends Microbiol 20:385–391. doi:10.1016/j.tim.2012.05.003. PubMed DOI

Vangay P, Johnson AJ, Ward TL, Al-Ghalith GA, Shields-Cutler RR, Hillmann BM, Lucas SK, Beura LK, Thompson EA, Till LM, Batres R, Paw B, Pergament SL, Saenyakul P, Xiong M, Kim AD, Kim G, Masopust D, Martens EC, Angkurawaranon C, McGready R, Kashyap PC, Culhane-Pera KA, Knights D. 2018. US immigration Westernizes the human gut microbiome. Cell 175:962–972.e10. doi:10.1016/j.cell.2018.10.029. PubMed DOI PMC

Remis MJ, Jost Robinson CA. 2014. Examining short-term nutritional status among BaAka foragers in transitional economies. Am J Phys Anthropol 154:365–375. doi:10.1002/ajpa.22521. PubMed DOI

Gomez A, Rothman JM, Petrzelkova K, Yeoman CJ, Vlckova K, Umaña JD, Carr M, Modry D, Todd A, Torralba M, Nelson KE, Stumpf RM, Wilson BA, Blekhman R, White BA, Leigh SR. 2016. Temporal variation selects for diet-microbe co-metabolic traits in the gut of Gorilla spp. ISME J 10:514–526. doi:10.1038/ismej.2015.146. PubMed DOI PMC

Remis MJ, Dierenfeld ES, Mowry CB, Carroll RW. 2001. Nutritional aspects of western lowland gorilla (Gorilla gorilla gorilla) diet during seasons of fruit scarcity at Bai Hokou, Central African Republic. Int J Primatol 22:807–836. doi:10.1023/A:1012021617737. DOI

Belury MA. 2002. Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action. Annu Rev Nutr 22:505–531. doi:10.1146/annurev.nutr.22.021302.121842. PubMed DOI

Farvid MS, Ding M, Pan A, Sun Q, Chiuve SE, Steffen LM, Willett WC, Hu FB. 2014. Dietary linoleic acid and risk of coronary heart disease: a systematic review and meta-analysis of prospective cohort studies. Circulation 130:1568–1578. doi:10.1161/CIRCULATIONAHA.114.010236. PubMed DOI PMC

Manara S, Asnicar F, Beghini F, Bazzani D, Cumbo F, Zolfo M, Nigro E, Karcher N, Manghi P, Metzger MI, Pasolli E, Segata N. 2019. Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species. Genome Biol 20:299. doi:10.1186/s13059-019-1923-9. PubMed DOI PMC

Obregon-Tito AJ, Tito RY, Metcalf J, Sankaranarayanan K, Clemente JC, Ursell LK, Zech Xu Z, Van Treuren W, Knight R, Gaffney PM, Spicer P, Lawson P, Marin-Reyes L, Trujillo-Villarroel O, Foster M, Guija-Poma E, Troncoso-Corzo L, Warinner C, Ozga AT, Lewis CM. 2015. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat Commun 6:6505. doi:10.1038/ncomms7505. PubMed DOI PMC

Stewart RD, Auffret MD, Warr A, Walker AW, Roehe R, Watson M. 2019. Compendium of 4,941 rumen metagenome-assembled genomes for rumen microbiome biology and enzyme discovery. Nat Biotechnol 37:953–961. doi:10.1038/s41587-019-0202-3. PubMed DOI PMC

Smits SA, Leach J, Sonnenburg ED, Gonzalez CG, Lichtman JS, Reid G, Knight R, Manjurano A, Changalucha J, Elias JE, Dominguez-Bello MG, Sonnenburg JL. 2017. Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. Science 357:802–806. doi:10.1126/science.aan4834. PubMed DOI PMC

Milton K. 1999. Nutritional characteristics of wild primate foods: do the diets of our closest living relatives have lessons for us? Nutrition 15:488–498. doi:10.1016/s0899-9007(99)00078-7. PubMed DOI

Pontzer H, Wood BM, Raichlen DA. 2018. Hunter-gatherers as models in public health. Obes Rev 19(Suppl 1):24–35. doi:10.1111/obr.12785. PubMed DOI

Sonnenburg JL, Sonnenburg ED. 2019. Vulnerability of the industrialized microbiota. Science 366:eaaw9255. doi:10.1126/science.aaw9255. PubMed DOI

Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031. doi:10.1038/nature05414. PubMed DOI

Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. 2005. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102:11070–11075. doi:10.1073/pnas.0504978102. PubMed DOI PMC

Zhang X, Chen Y, Zhu J, Zhang M, Ho C-T, Huang Q, Cao J. 2018. Metagenomics analysis of gut microbiota in a high fat diet–induced obesity mouse model fed with (−)-epigallocatechin 3-O-(3-O-methyl) gallate (EGCG3″Me). Mol Nutr Food Res 62:1800274. doi:10.1002/mnfr.201800274. PubMed DOI

Hildebrandt MA, Hoffmann C, Sherrill–Mix SA, Keilbaugh SA, Hamady M, Chen Y, Knight R, Ahima RS, Bushman F, Wu GD. 2009. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137:1716–1724.e2. doi:10.1053/j.gastro.2009.08.042. PubMed DOI PMC

Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. 2009. A core gut microbiome in obese and lean twins. Nature 457:480–484. doi:10.1038/nature07540. PubMed DOI PMC

El-Awady R, Saleh E, Hashim A, Soliman N, Dallah A, Elrasheed A, Elakraa G. 2016. The role of eukaryotic and prokaryotic ABC transporter family in failure of chemotherapy. Front Pharmacol 7:535. doi:10.3389/fphar.2016.00535. PubMed DOI PMC

Bhagirath AY, Li Y, Patidar R, Yerex K, Ma X, Kumar A, Duan K. 2019. Two component regulatory systems and antibiotic resistance in Gram-negative pathogens. Int J Mol Sci 20:1781. doi:10.3390/ijms20071781. PubMed DOI PMC

Remis MJ. 1997. Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: use of variable resources. Am J Primatol 43:87–109. doi:10.1002/(SICI)1098-2345(1997)43:2<87::AID-AJP1>3.0.CO;2-T. PubMed DOI

Masi S, Mundry R, Ortmann S, Cipolletta C, Boitani L, Robbins MM. 2015. The influence of seasonal frugivory on nutrient and energy intake in wild Western gorillas. PLoS One 10:e0129254. doi:10.1371/journal.pone.0129254. PubMed DOI PMC

Hall GH, Patrinos HA. 2012. Indigenous peoples, poverty, and development. Cambridge University Press, Cambridge, United Kingdom.

Masi S, Cipolletta C, Robbins MM. 2009. Western lowland gorillas (Gorilla gorilla gorilla) change their activity patterns in response to frugivory. Am J Primatol 71:91–100. doi:10.1002/ajp.20629. PubMed DOI

Johnson AJ, Vangay P, Al-Ghalith GA, Hillmann BM, Ward TL, Shields-Cutler RR, Kim AD, Shmagel AK, Syed AN, Personalized Microbiome Class Students, Walter J, Menon R, Koecher K, Knights D. 2019. Daily sampling reveals personalized diet-microbiome associations in humans. Cell Host Microbe 25:789–802.e5. doi:10.1016/j.chom.2019.05.005. PubMed DOI

Carlson JL, Erickson JM, Hess JM, Gould TJ, Slavin JL. 2017. Prebiotic dietary fiber and gut health: comparing the in vitro fermentations of beta-glucan, inulin and xylooligosaccharide. Nutrients 9:1361. doi:10.3390/nu9121361. PubMed DOI PMC

Smits SA, Marcobal A, Higginbottom S, Sonnenburg JL, Kashyap PC. 2016. Individualized responses of gut microbiota to dietary intervention modeled in humanized mice. mSystems 1:e00098-16. doi:10.1128/mSystems.00098-16. PubMed DOI PMC

Koo H, Hakim JA, Crossman DK, Kumar R, Lefkowitz EJ, Morrow CD. 2019. Individualized recovery of gut microbial strains post antibiotics. NPJ Biofilms Microbiomes 5:30. doi:10.1038/s41522-019-0103-8. PubMed DOI PMC

Maldonado-Gómez MX, Martínez I, Bottacini F, O’Callaghan A, Ventura M, van Sinderen D, Hillmann B, Vangay P, Knights D, Hutkins RW, Walter J. 2016. Stable engraftment of Bifidobacterium longum AH1206 in the human gut depends on individualized features of the resident microbiome. Cell Host Microbe 20:515–526. doi:10.1016/j.chom.2016.09.001. PubMed DOI

Marlowe FW, Colette Berbesque J, Wood B, Crittenden A, Porter C, Mabulla A. 2014. Honey, Hadza, hunter-gatherers, and human evolution. J Hum Evol 71:119–128. doi:10.1016/j.jhevol.2014.03.006. PubMed DOI

Yasar Yildiz S, Toksoy Oner E. 2014. Mannan as a promising bioactive material for drug nanocarrier systems In Sezer AD. (ed), Application of nanotechnology in drug delivery. InTechOpen, London, United Kingdom.

Macfarlane GT, Allison C, Gibson SA, Cummings JH. 1988. Contribution of the microflora to proteolysis in the human large intestine. J Appl Bacteriol 64:37–46. doi:10.1111/j.1365-2672.1988.tb02427.x. PubMed DOI

Yoon M-S. 2016. The emerging role of branched-chain amino acids in insulin resistance and metabolism. Nutrients 8:405. doi:10.3390/nu8070405. PubMed DOI PMC

Neis EPJG, Dejong CHC, Rensen SS. 2015. The role of microbial amino acid metabolism in host metabolism. Nutrients 7:2930–2946. doi:10.3390/nu7042930. PubMed DOI PMC

Gomez-Arango LF, Barrett HL, Wilkinson SA, Callaway LK, McIntyre HD, Morrison M, Dekker Nitert M. 2018. Low dietary fiber intake increases Collinsella abundance in the gut microbiota of overweight and obese pregnant women. Gut Microbes 9:189–201. doi:10.1080/19490976.2017.1406584. PubMed DOI PMC

Candela M, Biagi E, Soverini M, Consolandi C, Quercia S, Severgnini M, Peano C, Turroni S, Rampelli S, Pozzilli P, Pianesi M, Fallucca F, Brigidi P. 2016. Modulation of gut microbiota dysbioses in type 2 diabetic patients by macrobiotic Ma-Pi 2 diet. Br J Nutr 116:80–93. doi:10.1017/S0007114516001045. PubMed DOI PMC

Kassinen A, Krogius-Kurikka L, Mäkivuokko H, Rinttilä T, Paulin L, Corander J, Malinen E, Apajalahti J, Palva A. 2007. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 133:24–33. doi:10.1053/j.gastro.2007.04.005. PubMed DOI

Richards AL, Muehlbauer AL, Alazizi A, Burns MB, Findley A, Messina F, Gould TJ, Cascardo C, Pique-Regi R, Blekhman R, Luca F. 2019. Gut microbiota has a widespread and modifiable effect on host gene regulation. mSystems 4:e00323-18. doi:10.1128/mSystems.00323-18. PubMed DOI PMC

Roediger WE. 1982. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83:424–429. doi:10.1016/S0016-5085(82)80339-9. PubMed DOI

Miyamoto J, Ohue-Kitano R, Mukouyama H, Nishida A, Watanabe K, Igarashi M, Irie J, Tsujimoto G, Satoh-Asahara N, Itoh H, Kimura I. 2019. Ketone body receptor GPR43 regulates lipid metabolism under ketogenic conditions. Proc Natl Acad Sci U S A 116:23813–23821. doi:10.1073/pnas.1912573116. PubMed DOI PMC

Oelschlägel M, Zimmerling J, Tischler D. 2018. A review: the styrene metabolizing cascade of side-chain oxygenation as biotechnological basis to gain various valuable compounds. Front Microbiol 9:490. doi:10.3389/fmicb.2018.00490. PubMed DOI PMC

Rampelli S, Schnorr SL, Consolandi C, Turroni S, Severgnini M, Peano C, Brigidi P, Crittenden AN, Henry AG, Candela M. 2015. Metagenome sequencing of the Hadza hunter-gatherer gut microbiota. Curr Biol 25:1682–1693. doi:10.1016/j.cub.2015.04.055. PubMed DOI

Hansen MEB, Rubel MA, Bailey AG, Ranciaro A, Thompson SR, Campbell MC, Beggs W, Dave JR, Mokone GG, Mpoloka SW, Nyambo T, Abnet C, Chanock SJ, Bushman FD, Tishkoff SA. 2019. Population structure of human gut bacteria in a diverse cohort from rural Tanzania and Botswana. Genome Biol 20:16. doi:10.1186/s13059-018-1616-9. PubMed DOI PMC

Collins SL, Patterson AD. 2020. The gut microbiome: an orchestrator of xenobiotic metabolism. Acta Pharm Sin B 10:19–32. doi:10.1016/j.apsb.2019.12.001. PubMed DOI PMC

Gomez A, Petrzelkova K, Yeoman CJ, Vlckova K, Mrázek J, Koppova I, Carbonero F, Ulanov A, Modry D, Todd A, Torralba M, Nelson KE, Gaskins HR, Wilson B, Stumpf RM, White BA, Leigh SR. 2015. Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Mol Ecol 24:2551–2565. doi:10.1111/mec.13181. PubMed DOI

Ferla MP, Patrick WM. 2014. Bacterial methionine biosynthesis. Microbiology (Reading) 160:1571–1584. doi:10.1099/mic.0.077826-0. PubMed DOI

Brock M, Maerker C, Schütz A, Völker U, Buckel W. 2002. Oxidation of propionate to pyruvate in Escherichia coli. Involvement of methylcitrate dehydratase and aconitase. Eur J Biochem 269:6184–6194. doi:10.1046/j.1432-1033.2002.03336.x. PubMed DOI

Lima J, Auffret MD, Stewart RD, Dewhurst RJ, Duthie C-A, Snelling TJ, Walker AW, Freeman TC, Watson M, Roehe R. 2019. Identification of rumen microbial genes involved in pathways linked to appetite, growth, and feed conversion efficiency in cattle. Front Genet 10:701. doi:10.3389/fgene.2019.00701. PubMed DOI PMC

Ze X, Duncan SH, Louis P, Flint HJ. 2012. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J 6:1535–1543. doi:10.1038/ismej.2012.4. PubMed DOI PMC

Vital M, Howe A, Bergeron N, Krauss RM, Jansson JK, Tiedje JM. 2018. Metagenomic insights into the degradation of resistant starch by human gut microbiota. Appl Environ Microbiol 84:e01562-18. doi:10.1128/AEM.01562-18. PubMed DOI PMC

Zhang C, Derrien M, Levenez F, Brazeilles R, Ballal SA, Kim J, Degivry M-C, Quéré G, Garault P, van Hylckama Vlieg JET, Garrett WS, Doré J, Veiga P. 2016. Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes. ISME J 10:2235–2245. doi:10.1038/ismej.2016.13. PubMed DOI PMC

Yang J, McDowell A, Kim EK, Seo H, Yum K, Lee WH, Jee Y-K, Kim Y-K. 2019. Consumption of a Leuconostoc holzapfelii-enriched synbiotic beverage alters the composition of the microbiota and microbial extracellular vesicles. Exp Mol Med 51:1–11. doi:10.1038/s12276-019-0288-1. PubMed DOI PMC

Ambrose SH. 2001. Paleolithic technology and human evolution. Science 291:1748–1753. doi:10.1126/science.1059487. PubMed DOI

Henrich J. 2017. The secret of our success: how culture is driving human evolution, domesticating our species, and making us smarter. Princeton University Press, Princeton, NJ.

Segata N. 2015. Gut microbiome: Westernization and the disappearance of intestinal diversity. Curr Biol 25:R611–R613. doi:10.1016/j.cub.2015.05.040. PubMed DOI

Tett A, Huang KD, Asnicar F, Fehlner-Peach H, Pasolli E, Karcher N, Armanini F, Manghi P, Bonham K, Zolfo M, De Filippis F, Magnabosco C, Bonneau R, Lusingu J, Amuasi J, Reinhard K, Rattei T, Boulund F, Engstrand L, Zink A, Collado MC, Littman DR, Eibach D, Ercolini D, Rota-Stabelli O, Huttenhower C, Maixner F, Segata N. 2019. The Prevotella copri complex comprises four distinct clades underrepresented in Westernized populations. Cell Host Microbe 26:666–679.e7. doi:10.1016/j.chom.2019.08.018. PubMed DOI PMC

Tito RY, Knights D, Metcalf J, Obregon-Tito AJ, Cleeland L, Najar F, Roe B, Reinhard K, Sobolik K, Belknap S, Foster M, Spicer P, Knight R, Lewis CM Jr. 2012. Insights from characterizing extinct human gut microbiomes. PLoS One 7:e51146. doi:10.1371/journal.pone.0051146. PubMed DOI PMC

Yamauchi T, Sato H, Kawamura K. 2014. Nutritional status and physical fitness of Pygmy hunter-gatherers living in the African rainforests. Afr Study Monogr 47(Suppl):25–34.

Masi S, Chauffour S, Bain O, Todd A, Guillot J, Krief S. 2012. Seasonal effects on great ape health: a case study of wild chimpanzees and Western gorillas. PLoS One 7:e49805. doi:10.1371/journal.pone.0049805. PubMed DOI PMC

Doran DM, McNeilage A, Greer D, Bocian C, Mehlman P, Shah N. 2002. Western lowland gorilla diet and resource availability: new evidence, cross-site comparisons, and reflections on indirect sampling methods. Am J Primatol 58:91–116. doi:10.1002/ajp.10053. PubMed DOI

Isong EU, Adewusi SAR, Nkanga EU, Umoh EE, Offiong EE. 1999. Nutritional and phytogeriatological studies of three varieties of Gnetum africanum (“afang”). Food Chem 64:489–493. doi:10.1016/S0308-8146(98)00139-3. DOI

Patel RK, Jain M. 2012. NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619. doi:10.1371/journal.pone.0030619. PubMed DOI PMC

Schmieder R, Edwards R. 2011. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864. doi:10.1093/bioinformatics/btr026. PubMed DOI PMC

Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. doi:10.1093/bioinformatics/btu170. PubMed DOI PMC

Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. doi:10.1038/nmeth.1923. PubMed DOI PMC

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079. doi:10.1093/bioinformatics/btp352. PubMed DOI PMC

Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842. doi:10.1093/bioinformatics/btq033. PubMed DOI PMC

Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. 2017. metaSPAdes: a new versatile metagenomic assembler. Genome Res 27:824–834. doi:10.1101/gr.213959.116. PubMed DOI PMC

Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. doi:10.1186/1471-2105-11-119. PubMed DOI PMC

Li W, Godzik A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659. doi:10.1093/bioinformatics/btl158. PubMed DOI

Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. doi:10.1093/bioinformatics/btp324. PubMed DOI PMC

Kanehisa M, Goto S. 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30. doi:10.1093/nar/28.1.27. PubMed DOI PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2. PubMed DOI

Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495. doi:10.1093/nar/gkt1178. PubMed DOI PMC

Wishart DS, Knox C, Guo AC, Cheng D, Shrivastava S, Tzur D, Gautam B, Hassanali M. 2008. DrugBank: a knowledgebase for drugs, drug actions and drug targets. Nucleic Acids Res 36:D901–D906. doi:10.1093/nar/gkm958. PubMed DOI PMC

Dhakan DB, Maji A, Sharma AK, Saxena R, Pulikkan J, Grace T, Gomez A, Scaria J, Amato KR, Sharma VK. 2019. The unique composition of Indian gut microbiome, gene catalogue, and associated fecal metabolome deciphered using multi-omics approaches. Gigascience 8:giz004. doi:10.1093/gigascience/giz004. PubMed DOI PMC

Huson DH, Auch AF, Qi J, Schuster SC. 2007. MEGAN analysis of metagenomic data. Genome Res 17:377–386. doi:10.1101/gr.5969107. PubMed DOI PMC

Li D, Liu C-M, Luo R, Sadakane K, Lam T-W. 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31:1674–1676. doi:10.1093/bioinformatics/btv033. PubMed DOI

Kang DD, Froula J, Egan R, Wang Z. 2015. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3:e1165. doi:10.7717/peerj.1165. PubMed DOI PMC

Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. 2015. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055. doi:10.1101/gr.186072.114. PubMed DOI PMC

Wu Y-W. 2018. ezTree: an automated pipeline for identifying phylogenetic marker genes and inferring evolutionary relationships among uncultivated prokaryotic draft genomes. BMC Genomics 19:921. doi:10.1186/s12864-017-4327-9. PubMed DOI PMC

Tanizawa Y, Fujisawa T, Nakamura Y. 2018. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 34:1037–1039. doi:10.1093/bioinformatics/btx713. PubMed DOI PMC

Oksanen J. 2015. Vegan: an introduction to ordination. http://cranr-project.org/web/packages/vegan/vignettes/introvegan pdf 8:19.

Paradis E, Claude J, Strimmer K. 2004. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20:289–290. doi:10.1093/bioinformatics/btg412. PubMed DOI

Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2013. Package “vegan.” Community ecology package, version 2:1–295.

Väremo L, Nielsen J, Nookaew I. 2013. Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods. Nucleic Acids Res 41:4378–4391. doi:10.1093/nar/gkt111. PubMed DOI PMC

Gillis N. 2017. Introduction to nonnegative matrix factorization. arXiv: 1703.00663 [cs.NA].

Schwager E, Weingart G, Bielski C, Huttenhower C. 2014. CCREPE: Compositionality corrected by Permutation and Renormalization.

Graffelman J. 2012. A guide to scatterplot and biplot calibration.

Wickham H, François R, Henry L, Müller K. 2020. dplyr: a grammar of data manipulation. R package version 1.0.2 https://CRAN.R-project.org/package=dplyr.

Kassambara A, Mundt F. 2017. Package “factoextra.” Extract and visualize the results of multivariate data analyses 76.

Gómez-Rubio V. 2017. ggplot2 - elegant graphics for data analysis (2nd edition). J Stat Softw 77:1–3. doi:10.18637/jss.v077.b02. DOI

Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T. 2011. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27:431–432. doi:10.1093/bioinformatics/btq675. PubMed DOI PMC

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