Urbanization is associated with shifts in human lifestyles, thus possibly influencing the diversity, interaction and assembly of gut microbiota. However, the question regarding how human gut microbiota adapts to varying lifestyles remains elusive. To understand the relationship between gut microbiota and urbanization, we compared the diversity, interaction and assembly of gut microbial communities of herdsmen from three regions with different levels of urbanization, namely traditional herdsmen (TH), semi-urban herdsmen (SUH) and urban herdsmen (UH). The relative abundance of Prevotella decreased with the degree of urbanization (from TH to UH), whereas that of Bacteroides, Faecalibacterium, and Blautia showed an opposite trend. Although the alpha diversity measures (observed OTUs and phylogenetic diversity) of gut microbiota were unaffected by urbanization, the beta diversity (Jaccard or Bray-Curtis distances) was significantly influenced by urbanization. Metagenome prediction revealed that the gene functions associated with metabolism (i.e., carbohydrate and lipid metabolism) had significant differences between TH and UH. Network analysis showed that the modularity increased with the degree of urbanization, indicating a high extent of niche differentiation in UH. Meanwhile the trend of network density was opposite, indicating a more complex network in TH. Notably, the relative importance of environmental filtering that governed the community assembly increased with the degree of urbanization, which indicated that deterministic factors (e.g., low-fiber diet) play more important roles than stochastic factors (e.g., stochastic dispersal) in shaping the gut microbiota. A quantification of ecological processes showed a stronger signal of variable selection in UH than TH, implying that different selective pressures cause divergent gut community compositions due to urban lifestyles. Our results suggest that beta diversity, network interactions and ecological processes of gut microbiota may reflect the degree of urbanization, and highlight the adaptation of human gut microbiota to lifestyle changes.

Department of Applied Biology College of Biotechnology and Bioengineering Zhejiang University of Technology Hangzhou China

Institute of Occupational Health and Environmental Health School of Public Health Lanzhou University Lanzhou China

Institute of Soil Biology Czech Academy of Sciences České Budějovice Czechia

Key Laboratory of Adaptation and Evolution of Plateau Biota Northwest Institute of Plateau Biology Chinese Academy of Sciences Xining China

Key Laboratory of Environmental and Applied Microbiology Environmental Microbiology Key Laboratory of Sichuan Province Chengdu Institute of Biology Chinese Academy of Sciences Chengdu China

Qinghai Provincial Key Laboratory of Restoration Ecology in Cold Region Xining China

The Rowland Institute at Harvard Harvard University Cambridge MA United States

Zobrazit více v PubMed

Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D. R., et al. (2014). Enterotypes of the human gut microbiome. Nature 473 174–180. 10.1038/nature09944 PubMed DOI PMC

Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 335–336. 10.1038/nmeth.f.303 PubMed DOI PMC

Carrillo-Larco R. M., Bernabe-Ortiz A., Pillay T. D., Gilman R. H., Sanchez J. F., Poterico J. A., et al. (2016). Obesity risk in rural, urban and rural-to-urban migrants: prospective results of the PERU MIGRANT study. Int. J. Obes. 40 181–185. 10.1038/ijo.2015.140 PubMed DOI PMC

Costello E. K., Stagaman K., Dethlefsen L., Bohannan B. J., Relman D. A. (2012). The application of ecological theory toward an understanding of the human microbiome. Science 336 1255–1262. 10.1126/science.1224203 PubMed DOI PMC

Deng Y., Jiang Y. H., Yang Y., He Z., Luo F., Zhou J. (2012). Molecular ecological network analyses. BMC Bioinformatics 13:113. 10.1186/1471-2105-13-113 PubMed DOI PMC

DeSantis T., Hugenholtz P., Larsen N., Rojas M., Brodie E., Keller K., et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72 5069–5072. 10.1128/AEM.03006-05 PubMed DOI PMC

Dill-McFarland K. A., Weimer P. J., Pauli J. N., Peery M. Z., Suen G. (2015). Diet specialization selects for an unusual and simplified gut microbiota in two- and three-toed sloths. Environ. Microbiol. 18 1391–1402. 10.1111/1462-2920.13022 PubMed DOI

Dufrêne M., Legendre P. (1997). Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67 345–366. 10.2307/2963459 DOI

Edgar R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 2460–2461. 10.1093/bioinformatics/btq461 PubMed DOI

Faust K., Raes J. (2012). Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10 538–550. 10.1038/nrmicro2832 PubMed DOI

Gomez A., Petrzelkova K. J., Burns M. B., Yeoman C. J., Amato K. R., Vlckova K., et al. (2016). Gut microbiome of coexisting BaAka pygmies and bantu reflects gradients of traditional subsistence patterns. Cell Rep. 14 2142–2153. 10.1016/j.celrep.2016.02.013 PubMed DOI

Inglis R., Gardner A., Cornelis P., Buckling A. (2009). Spite and virulence in the bacterium Pseudomonas Aeruginosa. Proc. Natl. Acad. Sci. U.S.A. 106 5703–5707. 10.1073/pnas.0810850106 PubMed DOI PMC

Jia Y. (2016). Review of benefit evaluation research on ecological migration in China. Resour. Sci. 38 87–92.

Jousset A., Schulz W., Scheu S., Eisenhauer N. (2011). Intraspecific genotypic richness and relatedness predict the invasibility of microbial communities. ISME J. 5 1108–1114. 10.1038/ismej.2011.9 PubMed DOI PMC

Kara E. L., Hanson P. C., Hu Y. H., Winslow L., McMahon K. D. (2012). A decade of seasonal dynamics and co-occurrences within freshwater bacterioplankton communities from eutrophic Lake Mendota. WI, USA. ISME J. 7 680–684. 10.1038/ismej.2012.118 PubMed DOI PMC

Kembel S. W., Cowan P. D., Helmus M. R., Cornwell W. K., Morlon H., Ackerly D. D., et al. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26 1463–1464. 10.1093/bioinformatics/btq166 PubMed DOI

Langille M. G., Zaneveld J., Caporaso J. G., McDonald D., Knights D., Reyes J. A., et al. (2013). Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotech. 31 814–821. 10.1038/nbt.2676 PubMed DOI PMC

Li H., Li T., Beasley D. E., Hedenec P., Xiao Z., Zhang S., et al. (2016a). Diet diversity is associated with beta but not alpha diversity of pika gut microbiota. Front. Microbiol. 7:1169 10.3389/fmicb.2016.01169 PubMed DOI PMC

Li H., Li T., Tu B., Kou Y., Li X. (2017). Host species shapes the co-occurrence patterns rather than diversity of stomach bacterial communities in pikas. Appl. Microbiol. Biotechnol. 101 5519–5529. 10.1007/s00253-017-8254-0 PubMed DOI

Li H., Li T., Yao M., Li J., Zhang S., Wirth S., et al. (2016b). Pika gut may select for rare but diverse environmental bacteria. Front. Microbiol. 7:1269. 10.3389/fmicb.2016.01269 PubMed DOI PMC

Li H., Qu J., Li T., Li J., Lin Q., Li X. (2016c). Pika population density is associated with composition and diversity of gut microbiota. Front. Microbiol. 7:758. 10.3389/fmicb.2016.00758 PubMed DOI PMC

Lin Q., De Vrieze J., Li C., Li J., Li J., Yao M., et al. (2017). Temperature regulates deterministic processes and the succession of microbial interactions in anaerobic digestion process. Water Res. 123 134–143. 10.1016/j.watres.2017.06.051 PubMed DOI

Magoc T., Salzberg S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27 2957–2963. 10.1093/bioinformatics/btr507 PubMed DOI PMC

Martinez I., Stegen J. C., Maldonado-Gomez M. X., Eren A. M., Siba P. M., Greenhill A. R., et al. (2015). The gut microbiota of rural papua new guineans: composition, diversity patterns, and ecological processes. Cell Rep. 11 527–538. 10.1016/j.celrep.2015.03.049 PubMed DOI

McArdle B. H., Anderson M. J. (2001). Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82 290–297. 10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2 DOI

Meyerhof M. S., Wilson J. M., Dawson M. N., Michael Beman J. (2016). Microbial community diversity, structure and assembly across oxygen gradients in meromictic marine lakes, Palau. Environ. Microbiol. 18 4907–4919. 10.1111/1462-2920.13416 PubMed DOI

Obregon-Tito A. J., Tito R. Y., Metcalf J., Sankaranarayanan K., Clemente J. C., Ursell L. K., et al. (2015). Subsistence strategies in traditional societies distinguish gut microbiomes. Nat. Commun. 6:6505. 10.1038/ncomms7505 PubMed DOI PMC

O’Keefe S. J., Li J. V., Lahti L., Ou J., Carbonero F., Mohammed K., et al. (2015). Fat, fibre and cancer risk in African Americans and rural Africans. Nat. Commun. 6:6342. 10.1038/ncomms7342 PubMed DOI PMC

Purves D. W., Turnbull L. A. (2010). Different but equal: the implausible assumption at the heart of neutral theory. J. Anim. Ecol. 79 1215–1225. 10.1038/ncomms7342 PubMed DOI PMC

Ramayo-Caldas Y., Mach N., Lepage P., Levenez F., Denis C., Lemonnier G., et al. (2016). Phylogenetic network analysis applied to pig gut microbiota identifies an ecosystem structure linked with growth traits. ISME J. 10 2973–2977. 10.1038/ismej.2016.77 PubMed DOI PMC

Rampelli S., Schnorr S. L., Consolandi C., Turroni S., Severgnini M., Peano C., et al. (2015). Metagenome sequencing of the Hadza hunter-gatherer gut Microbiota. Curr. Biol. 25 1682–1693. 10.1016/j.cub.2015.04.055 PubMed DOI

Riva A., Borgo F., Lassandro C., Verduci E., Morace G., Borghi E., et al. (2016). Pediatric obesity is associated with an altered gut microbiota and discordant shifts in Firmicutes populations. Environ. Microbiol. 48:e268. 10.1111/1462-2920.13463 PubMed DOI PMC

Roberts D. (2007). labdsv: ordination and multivariate analysis for ecology. R Package Version 1:3.

Rosindell J., Hubbell S. P., He F., Harmon L. J., Etienne R. S. (2012). The case for ecological neutral theory. Trends Ecol. Evol. 27 203–208. 10.1016/j.tree.2012.01.004 PubMed DOI

Saito R., Smoot M., Ono K., Ruscheinski J., Wang P., Lotia S., et al. (2012). A travel guide to cytoscape plugins. Nat. Methods 9 1069–1076. 10.1038/nmeth.2212 PubMed DOI PMC

Schnorr S. L., Candela M., Rampelli S., Centanni M., Consolandi C., Basaglia G., et al. (2014). Gut microbiome of the Hadza hunter-gatherers. Nat. Commun. 5:3654. 10.1038/ncomms4654 PubMed DOI PMC

Song H.-N., Go S.-I., Lee W. S., Kim Y., Choi H. J., Lee U. S., et al. (2016). Population-based regional cancer incidence in Korea: comparison between urban and rural areas. Cancer Res. Treat. 48 789–797. 10.4143/crt.2015.062 PubMed DOI PMC

Sonnenburg E. D., Smits S. A., Tikhonov M., Higginbottom S. K., Wingreen N. S., Sonnenburg J. L. (2016). Diet-induced extinctions in the gut microbiota compound over generations. Nature 529 212–215. 10.1038/nature16504 PubMed DOI PMC

Stegen J. C., Lin X., Fredrickson J. K., Chen X., Kennedy D. W., Murray C. J., et al. (2013). Quantifying community assembly processes and identifying features that impose them. ISME J. 7 2069–2079. 10.1038/ismej.2013.93 PubMed DOI PMC

Stegen J. C., Lin X., Fredrickson J. K., Konopka A. E. (2015). Estimating and mapping ecological processes influencing microbial community assembly. Front. Microbiol. 6:370. 10.3389/fmicb.2015.00370 PubMed DOI PMC

Stegen J. C., Lin X., Konopka A. E., Fredrickson J. K. (2012). Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J. 6 1653–1664. 10.1038/ismej.2012.22 PubMed DOI PMC

Tamaki H., Wright C., Li X., Lin Q., Hwang C., Wang S., et al. (2011). Analysis of 16S rRNA amplicon sequencing options on the Roche/454 next-generation titanium sequencing platform. PLoS One 6:e25263. 10.1371/journal.pone.0025263 PubMed DOI PMC

Vellend M. (2010). Conceptual synthesis in community ecology. Q. Rev. Biol. 85 183–206. 10.1086/652373 PubMed DOI

Vellend M., Srivastava D. S., Anderson K. M., Brown C. D., Jankowski J. E., Kleynhans E. J., et al. (2014). Assessing the relative importance of neutral stochasticity in ecological communities. Oikos 123 1420–1430. 10.1111/oik.01493 DOI

Wang Q., Garrity G. M., Tiedje J. M., Cole J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73 5261–5267. 10.1128/AEM.00062-07 PubMed DOI PMC

Werner U., Nicholas J. G. (2010). Null model analysis of species associations using abundance data. Ecology 91 3384–3397. 10.1890/09-2157.1 PubMed DOI

Winglee K., Howard A. G., Sha W., Gharaibeh R. Z., Liu J., Jin D., et al. (2017). Recent urbanization in China is correlated with a Westernized microbiome encoding increased virulence and antibiotic resistance genes. Microbiome 5:121. 10.1186/s40168-017-0338-7 PubMed DOI PMC

Wu G. D., Chen J., Hoffmann C., Bittinger K., Chen Y. Y., Keilbaugh S. A., et al. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science 334 105–108. 10.1126/science.1208344 PubMed DOI PMC

Xiong J., Dai W., Zhu J., Liu K., Dong C., Qiu Q. (2017). The underlying ecological processes of gut microbiota among cohabitating retarded, overgrown and normal shrimp. Microb. Ecol. 73 988–999. 10.1007/s00248-016-0910-x PubMed DOI

Yan Q., Li J., Yu Y., Wang J., He Z., Van Nostrand J. D., et al. (2016). Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ. Microbiol. 18 4739–4754. 10.1111/1462-2920.13365 PubMed DOI

Yatsunenko T., Rey F. E., Manary M. J., Trehan I., Dominguez-Bello M. G., Contreras M., et al. (2012). Human gut microbiome viewed across age and geography. Nature 486 222–227. 10.1038/nature11053 PubMed DOI PMC

Zhou J., Deng Y., Zhang P., Xue K., Liang Y., Van Nostrand J. D., et al. (2014). Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proc. Natl. Acad. Sci. U.S.A. 111 E836–E845. 10.1073/pnas.1324044111 PubMed DOI PMC

Zhou M., Astell-Burt T., Yin P., Feng X., Page A., Liu Y., et al. (2015). Spatiotemporal variation in diabetes mortality in China: multilevel evidence from 2006 and 2012. BMC Public Health 15:633. 10.1186/s12889-015-1982-0 PubMed DOI PMC