Recent urbanization in China is correlated with a Westernized microbiome encoding increased virulence and antibiotic resistance genes

Microbiome

Volumn 5, Issue 1, 2017, Pages

  Winglee, Kathryn ^a   Howard, Annie Green ^b   Sha, Wei ^a   Gharaibeh, Raad Z ^a,e   Liu, Jiawu ^c   Jin, Donghui ^c   Fodor, Anthony A ^a   Gordon Larsen, Penny ^d  

^a University of North Carolina at Charlotte   (United States)

^b University of North Carolina at Chapel Hill   (United States)

^c Hunan Center for Disease Control and Prevention   (China)

^d University of North Carolina   (United States)

^e UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

China; Metabolome; Metagenomics; Microbiome; Urbanization

Indexed keywords

1 ARACHIDONOLYL GPA; 1,5 ANHYDROSORBITOL; 2 AMINOHEPTANOATE; AMINO ACID; ANDROSTERONE; BETA LACTAMASE; BIOLOGICAL MARKER; CARBOHYDRATE; CHOLESTANOL; CHOLESTEROL; EPIANDROSTERONE; GAMMA GLUTAMYLVALINE; GLUTAMIC ACID; GUANOSINE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INOSINE; INSULIN; LACTIC ACID; LINOLEIC ACID; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PEPTIDE; RIBOSE; RNA 16S; SEROTONIN; THEOPHYLLINE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADULT; AGED; ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENE; ARTICLE; BACTERIAL VIRULENCE; BACTEROIDES; CLOSTRIDIUM; COLLINSELLA; DIABETES MELLITUS; ESCHERICHIA; FAECALIBACTERIUM; FEMALE; GENE; GENE EXPRESSION; HUMAN; MALE; MASS FRAGMENTOGRAPHY; METAGENOMICS; MICROBIAL DIVERSITY; MICROBIOME; NONHUMAN; OBESITY; PARABACTEROIDES; PHYLOGENETIC TREE; POPULATION ABUNDANCE; PREVOTELLA; PRIORITY JOURNAL; RNA SEQUENCE; RUMINOCOCCUS; RURAL AREA; SHIGELLA; URBANIZATION; VIRULENCE; VIRUS; WHOLE GENOME SEQUENCING; BACTERIUM; CHINA; ESCHERICHIA COLI; FEEDING BEHAVIOR; GENETIC VARIATION; GENETICS; HIGH THROUGHPUT SEQUENCING; INTESTINE FLORA; METABOLOME; MIDDLE AGED; PATHOGENICITY; WESTERN DIET;

AGED; BACTERIA; CHINA; DIET, WESTERN; DRUG RESISTANCE, MICROBIAL; ESCHERICHIA COLI; FEEDING BEHAVIOR; FEMALE; GASTROINTESTINAL MICROBIOME; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MALE; METABOLOME; METAGENOMICS; MIDDLE AGED; SHIGELLA; URBANIZATION; VIRULENCE;

EID: 85041490246     PISSN: None     EISSN: 20492618     Source Type: Journal    
DOI: 10.1186/s40168-017-0338-7     Document Type: Article

References (42)

1. Carrillo-Larco RM, Bernabe-Ortiz A, Pillay TD, Gilman RH, Sanchez JF, Poterico JA, Quispe R, Smeeth L, Miranda JJ Obesity risk in rural, urban and rural-to-urban migrants: prospective results of the PERU MIGRANT study. Int J Obes. 2016; 40: 181-5.
2. Zhou M, Astell-Burt T, Yin P, Feng X, Page A, Liu Y, Liu J, Li Y, Liu S, Wang L, Wang L, Wang L. Spatiotemporal variation in diabetes mortality in China: multilevel evidence from 2006 and 2012. BMC Public Health. 2015; 15: 633.
3. Song HN, Go SI, Lee WS, Kim Y, Choi HJ, Lee US, Kang MH, Lee GW, Kim HG, Kang JH, Kang YS, Lee JH, Jung JM, Hong SC Population-based regional cancer incidence in Korea: comparison between urban and rural areas. Cancer Res Treat. 2016; 48: 789-97.
4. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D, Peng Y, Zhang D, Jie Z, Wu W, Qin Y, Xue W, Li J, Han L, Lu D, Wu P, Dai Y, Sun X, Li Z, Tang A, Zhong S, Li X, Chen W, Xu R, Wang M, Feng Q, Gong M, Yu J, Zhang Y, Zhang M, Hansen T, Sanchez G, Raes J, Falony G, Okuda S, Almeida M, LeChatelier E, Renault P, Pons N, Batto JM, Zhang Z, Chen H, Yang R, Zheng W, Li S, Yang H, Wang J, Ehrlich SD, Nielsen R, Pedersen O, Kristiansen K, Wang J. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012; 490: 55-60.
5. Arthur JC, Gharaibeh RZ, Muhlbauer M, Perez-Chanona E, Uronis JM, McCafferty J, Fodor AA, Jobin C. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat Commun. 2014; 5: 4724.
6. Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology. 2014; 146: 1489-99.
7. 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 A core gut microbiome in obese and lean twins. Nature. 2009; 457: 480-4.
8. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, Louis P, McIntosh F, Johnstone AM, Lobley GE, Parkhill J, Flint HJ. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011; 5: 220-30.
9. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, Biddinger SB, Dutton RJ, Turnbaugh PJ Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014; 505: 559-63.
10. O'Keefe SJ, Li JV, Lahti L, Ou J, Carbonero F, Mohammed K, Posma JM, Kinross J, Wahl E, Ruder E, Vipperla K, Naidoo V, Mtshali L, Tims S, Puylaert PG, DeLany J, Krasinskas A, Benefiel AC, Kaseb HO, Newton K, Nicholson JK, de Vos WM, Gaskins HR, Zoetendal EG. Fat, fibre and cancer risk in African Americans and rural Africans. Nat Commun. 2015; 6: 6342.
11. Wu GD, Compher C, Chen EZ, Smith SA, Shah RD, Bittinger K, Chehoud C, Albenberg LG, Nessel L, Gilroy E, Star J, Weljie AM, Flint HJ, Metz DC, Bennett MJ, Li H, Bushman FD, Lewis JD. Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut. 2016; 65: 63-72.
12. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010; 107: 14691-6.
13. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kuczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI. Human gut microbiome viewed across age and geography. Nature. 2012; 486: 222-7.
14. Tyakht AV, Alexeev DG, Popenko AS, Kostryukova ES, Govorun VM. Rural and urban microbiota: to be or not to be? Gut Microbes. 2014; 5: 351-6.
15. Vatanen T, Kostic AD, d'Hennezel E, Siljander H, Franzosa EA, Yassour M, Kolde R, Vlamakis H, Arthur TD, Hamalainen AM, Peet A, Tillmann V, Uibo R, Mokurov S, Dorshakova N, Ilonen J, Virtanen SM, Szabo SJ, Porter JA, Lahdesmaki H, Huttenhower C, Gevers D, Cullen TW, Knip M, Group DS, Xavier RJ. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell. 2016; 165: 842-53.
16. Gong P, Liang S, Carlton EJ, Jiang Q, Wu J, Wang L, Remais JV Urbanisation and health in China. Lancet. 2012; 379: 843-52.
17. Carrillo-Larco RM, Bernabe-Ortiz A, Pillay TD, Gilman RH, Sanchez JF, Poterico JA, Quispe R, Smeeth L, Miranda JJ Obesity risk in rural, urban and rural-to-urban migrants: prospective results of the PERU MIGRANT study. Int J Obes. 2015
18. Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature. 2012; 486: 207-14.
19. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013; 41:D590-6.
20. Group NHW, Peterson J, Garges S, Giovanni M, McInnes P, Wang L, Schloss JA, Bonazzi V, JE ME, Wetterstrand KA, Deal C, Baker CC, Di Francesco V, Howcroft TK, Karp RW, Lunsford RD, Wellington CR, Belachew T, Wright M, Giblin C, David H, Mills M, Salomon R, Mullins C, Akolkar B, Begg L, Davis C, Grandison L, Humble M, Khalsa J, Little AR, Peavy H, Pontzer C, Portnoy M, Sayre MH, Starke-Reed P, Zakhari S, Read J, Watson B, Guyer M. The NIH Human Microbiome Project. Genome Res. 2009; 19: 2317-23.
21. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S. Host-gut microbiota metabolic interactions. Science. 2012; 336: 1262-7.
22. Wu GD, Compher C, Chen EZ, Smith SA, Shah RD, Bittinger K, Chehoud C, Albenberg LG, Nessel L, Gilroy E, Star J, Weljie AM, Flint HJ, Metz DC, Bennett MJ, Li H, Bushman FD, Lewis JD. Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut. 2014; 65(1): 63-72.
23. Brugere JF, Borrel G, Gaci N, Tottey W, O'Toole PW, Malpuech-Brugere C. Archaebiotics: proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease. Gut Microbes. 2014; 5: 5-10.
24. Lurie-Weinberger MN, Gophna U. Archaea in and on the human Body: health implications and future directions. PLoS Pathog. 2015; 11: e1004833.
25. Kernbauer E, Ding Y, Cadwell K. An enteric virus can replace the beneficial function of commensal bacteria. Nature. 2014; 516: 94-8.
26. Pfeiffer JK, Virgin HW Viral immunity. Transkingdom control of viral infection and immunity in the mammalian intestine. Science. 2016; 351
27. Endo A, Tanizawa Y, Tanaka N, Maeno S, Kumar H, Shiwa Y, Okada S, Yoshikawa H, Dicks L, Nakagawa J, Arita M. Comparative genomics of Fructobacillus spp. and Leuconostoc spp. reveals niche-specific evolution of Fructobacillus spp. BMC Genomics. 2015; 16: 1117.
28. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, Bousvaros A, Korzenik J, Sands BE, Xavier RJ, Huttenhower C. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012; 13:R79.
29. Cross AJ, Moore SC, Boca S, Huang WY, Xiong X, Stolzenberg-Solomon R, Sinha R, Sampson JN A prospective study of serum metabolites and colorectal cancer risk. Cancer. 2014; 120: 3049-57.
30. Wishart DS, Jewison T, Guo AC, Wilson M, Knox C, Liu Y, Djoumbou Y, Mandal R, Aziat F, Dong E, Bouatra S, Sinelnikov I, Arndt D, Xia J, Liu P, Yallou F, Bjorndahl T, Perez-Pineiro R, Eisner R, Allen F, Neveu V, Greiner R, Scalbert A. HMDB 3.0-The Human Metabolome Database in 2013. Nucleic Acids Res. 2013; 41:D801-7.
31. McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, Bhullar K, Canova MJ, De Pascale G, Ejim L, Kalan L, King AM, Koteva K, Morar M, Mulvey MR, O'Brien JS, Pawlowski AC, Piddock LJ, Spanogiannopoulos P, Sutherland AD, Tang I, Taylor PL, Thaker M, Wang W, Yan M, Yu T, Wright GD. The comprehensive antibiotic resistance database. Antimicrob Agents Chemother. 2013; 57: 3348-57.
32. Zhou CE, Smith J, Lam M, Zemla A, Dyer MD, Slezak T. MvirDB-a microbial database of protein toxins, virulence factors and antibiotic resistance genes for bio-defence applications. Nucleic Acids Res. 2007; 35:D391-4.
33. Zhang J, Guo Z, Xue Z, Sun Z, Zhang M, Wang L, Wang G, Wang F, Xu J, Cao H, Xu H, Lv Q, Zhong Z, Chen Y, Qimuge S, Menghe B, Zheng Y, Zhao L, Chen W, Zhang H. A phylo-functional core of gut microbiota in healthy young Chinese cohorts across lifestyles, geography and ethnicities. ISME J. 2015; 9: 1979-90.
34. Nakayama J, Watanabe K, Jiang J, Matsuda K, Chao SH, Haryono P, La-Ongkham O, Sarwoko MA, Sujaya IN, Zhao L, Chen KT, Chen YP, Chiu HH, Hidaka T, Huang NX, Kiyohara C, Kurakawa T, Sakamoto N, Sonomoto K, Tashiro K, Tsuji H, Chen MJ, Leelavatcharamas V, Liao CC, Nitisinprasert S, Rahayu ES, Ren FZ, Tsai YC, Lee YK. Diversity in gut bacterial community of school-age children in Asia. Sci Rep. 2015; 5: 8397.
35. Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL Diet-induced extinctions in the gut microbiota compound over generations. Nature. 2016; 529: 212-5.
36. Arthur JC, Perez-Chanona E, Muhlbauer M, Tomkovich S, Uronis JM, Fan TJ, Campbell BJ, Abujamel T, Dogan B, Rogers AB, Rhodes JM, Stintzi A, Simpson KW, Hansen JJ, Keku TO, Fodor AA, Jobin C. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 2012; 338: 120-3.
37. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, de Roos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, Rudensky AY. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013; 504: 451-5.
38. Marchesi JR, Adams DH, Fava F, Hermes GD, Hirschfield GM, Hold G, Quraishi MN, Kinross J, Smidt H, Tuohy KM, Thomas LV, Zoetendal EG, Hart A. The gut microbiota and host health: a new clinical frontier. Gut. 2016; 65: 330-9.
39. Zhang YJ, Li S, Gan RY, Zhou T, Xu DP, Li HB Impacts of gut bacteria on human health and diseases. Int J Mol Sci. 2015; 16: 7493-519.
40. Wang Q, Garrity GM, Tiedje JM, Cole JR Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007; 73: 5261-7.
41. Wood DE, Salzberg SL Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 2014; 15:R46.
42. Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, Rodriguez-Mueller B, Zucker J, Thiagarajan M, Henrissat B, White O, Kelley ST, Methe B, Schloss PD, Gevers D, Mitreva M, Huttenhower C. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol. 2012; 8: e1002358.