US Immigration Westernizes the Human Gut Microbiome

Cell

Volumn 175, Issue 4, 2018, Pages 962-972.e10

  Vangay, Pajau ^a   Johnson, Abigail J ^a   Ward, Tonya L ^a   Al Ghalith, Gabriel A ^a   Shields Cutler, Robin R ^a   Hillmann, Benjamin M ^b   Lucas, Sarah K ^c   Beura, Lalit K ^c   Thompson, Emily A ^c   Till, Lisa M ^d   Batres, Rodolfo ^e   Paw, Bwei ^e   Pergament, Shannon L ^e   Saenyakul, Pimpanitta ^e   Xiong, Mary ^e   Kim, Austin D ^f   Kim, Grant ^a   Masopust, David ^c   Martens, Eric C ^g   Angkurawaranon, Chaisiri ^h   McGready, Rose ^i,j   Kashyap, Purna C ^d   Culhane Pera, Kathleen A ^e   Knights, Dan ^a,b   more..

^a UNIVERSITY OF MINNESOTA   (United States)

^b University of Minnesota   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d MAYO CLINIC   (United States)

^e and Hmong Partnership for Health and Wellness   (United States)

^f MACALESTER COLLEGE   (United States)

^g UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^h Faculty of Medicine Chiang Mai University   (Thailand)

ⁱ SHOKLO MALARIA RESEARCH UNIT   (Thailand)

^j UNIVERSITY OF OXFORD   (United Kingdom)

more..

Author keywords

Bacteriodes; immigrant health; immigration; metagenomics; microbiome; microbiota; obesity; Prevotella; refugee health

Indexed keywords

DNA; GLYCOSIDASE;

ADULT; AGED; ARTICLE; BACTEROIDES; BODY MASS; CONTROLLED STUDY; CULTURAL FACTOR; DIETARY FIBER; DNA SEQUENCE; ETHNICITY; FEMALE; FOOD PREFERENCE; GENE SEQUENCE; HMONG (PEOPLE); HUMAN; IMMIGRATION; INTESTINE FLORA; KAREN (PEOPLE); MACRONUTRIENT; MALE; MICROBIAL DIVERSITY; NONHUMAN; OBESITY; PHYLOGENY; POPULATION ABUNDANCE; PREVALENCE; PREVOTELLA; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN INTAKE; SEQUENCE ALIGNMENT; SPECIES RICHNESS; THAILAND; UNITED STATES; WESTERN DIET;

EID: 85055249203     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2018.10.029     Document Type: Article

References (67)

1. Abubucker, S., Segata, N., Goll, J., Schubert, A.M., Izard, J., Cantarel, B.L., Rodriguez-Mueller, B., Zucker, J., Thiagarajan, M., Henrissat, B., et al. Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput. Biol., 8, 2012, e1002358.
2. Al-Ghalith, G., Knights, D., BURST enables optimal exhaustive DNA alignment for big data. 2017, Zenodo.
3. Al-Ghalith, G., Knights, D., aKronyMer enables database-free metagenome comparison. 2018, Zenodo.
4. Al-Ghalith, G.A., Hillmann, B., Ang, K., Shields-Cutler, R., Knights, D., SHI7 Is a Self-Learning Pipeline for Multipurpose Short-Read DNA Quality Control. mSystems, 3, 2018.
5. Allen, M.L., Culhane-Pera, K.A., Call, K.T., Pergament, S.L., Partners in research: curricula to prepare community and faculty for CBPR partnerships. CES4healthinfo, 2011.
6. Arcan, C., Larson, N., Bauer, K., Berge, J., Story, M., Neumark-Sztainer, D., Dietary and weight-related behaviors and body mass index among Hispanic, Hmong, Somali, and white adolescents. J. Acad. Nutr. Diet. 114 (2014), 375–383.
7. Asnicar, F., Weingart, G., Tickle, T.L., Huttenhower, C., Segata, N., Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ, 3, 2015, e1029.
8. Blaser, M.J., Falkow, S., What are the consequences of the disappearing human microbiota?. Nat. Rev. Microbiol. 7 (2009), 887–894.
9. Bokulich, N.A., Chung, J., Battaglia, T., Henderson, N., Jay, M., Li, H., D Lieber, A., Wu, F., Perez-Perez, G.I., Chen, Y., et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci. Transl. Med., 8, 2016, 343ra82.
10. Britten, P., SuperTracker Incorporates Food Composition Data into Innovative Online Consumer Tool. Procedia Food Sci. 2 (2013), 172–179.
11. Bureau of Population, Refugees and Migration (2004). Long Wait is Over: Hmong from Wat Tham Krabok Begin Arriving in U.S. U.S. Refugee Admissions Program News 2.
12. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 (2010), 335–336.
13. Careyva, B., LaNoue, M., Bangura, M., de la Paz, A., Gee, A., Patel, N., Mills, G., The effect of living in the United States on body mass index in refugee patients. J. Health Care Poor Underserved 26 (2015), 421–430.
14. Caspi, R., Foerster, H., Fulcher, C.A., Kaipa, P., Krummenacker, M., Latendresse, M., Paley, S., Rhee, S.Y., Shearer, A.G., Tissier, C., et al. The MetaCyc Database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res. 36 (2008), D623–D631.
15. Center for Disease Control (2007). National Health and Nutrition Examination Survey (NHANES): Anthropometry Procedures Manual.
16. Clemente, J.C., Pehrsson, E.C., Blaser, M.J., Sandhu, K., Gao, Z., Wang, B., Magris, M., Hidalgo, G., Contreras, M., Noya-Alarcón, Ó., et al. The microbiome of uncontacted Amerindians. Sci. Adv., 1, 2015.
17. Dahlqvist, A., Thomson, D.L., The digestion and absorption of sucrose by the intact rat. J. Physiol. 167 (1963), 193–209.
18. David, L.A., Maurice, C.F., Carmody, R.N., Gootenberg, D.B., Button, J.E., Wolfe, B.E., Ling, A.V., Devlin, A.S., Varma, Y., Fischbach, M.A., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505 (2014), 559–563.
19. Dawson-Hahn, E., Pak-Gorstein, S., Matheson, J., Zhou, C., Yun, K., Scott, K., Payton, C., Stein, E., Holland, A., Grow, H.M., Mendoza, J.A., Growth Trajectories of Refugee and Nonrefugee Children in the United States. Pediatrics, 138, 2016, 138.
20. De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J.B., 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. USA 107 (2010), 14691–14696.
21. El Kaoutari, A., Armougom, F., Gordon, J.I., Raoult, D., Henrissat, B., The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat. Rev. Microbiol. 11 (2013), 497–504.
22. Faith, D.P., Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61 (1992), 1–10.
23. Febinia, C.A., The Gut Microbiota of Bali among the World Populations: Connecting Diet, Urbanisation, and Obesity. 2017, University of Sydney.
24. Flint, H.J., Scott, K.P., Duncan, S.H., Louis, P., Forano, E., Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3 (2012), 289–306.
25. Franzen, L., Smith, C., Acculturation and environmental change impacts dietary habits among adult Hmong. Appetite 52 (2009), 173–183.
26. Goel, M.S., McCarthy, E.P., Phillips, R.S., Wee, C.C., Obesity among US immigrant subgroups by duration of residence. JAMA 292 (2004), 2860–2867.
27. Gohl, D.M., Vangay, P., Garbe, J., MacLean, A., Hauge, A., Becker, A., Gould, T.J., Clayton, J.B., Johnson, T.J., Hunter, R., et al. Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies. Nat. Biotechnol. 34 (2016), 942–949.
28. Gomez, A., Petrzelkova, K.J., Burns, M.B., Yeoman, C.J., Amato, K.R., Vlckova, K., Modry, D., Todd, A., Jost Robinson, C.A., Remis, M.J., et al. Gut Microbiome of Coexisting BaAka Pygmies and Bantu Reflects Gradients of Traditional Subsistence Patterns. Cell Rep. 14 (2016), 2142–2153.
29. Heney, J.H., Dimock, C.C., Friedman, J.F., Lewis, C., Pediatric refugees in Rhode Island: increases in BMI percentile, overweight, and obesity following resettlement. R.I. Med. J. (2013) 98 (2014), 43–47.
30. Hervey, K., Vargas, D., Klesges, L., Fischer, P.R., Trippel, S., Juhn, Y.J., Overweight among refugee children after arrival in the United States. J. Health Care Poor Underserved 20 (2009), 246–256.
31. Hildebrandt, M.A., Hoffmann, C., Sherrill-Mix, S.A., Keilbaugh, S.A., Hamady, M., Chen, Y.Y., Knight, R., Ahima, R.S., Bushman, F., Wu, G.D., High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137 (2009), 1716–1724.
32. Kooiman, P., Structures of the galactomannans from seeds of Annona muricata, Arenga saccharifera, Cocos nucifera, Convolvulus tricolor, and Sophora japonica. Carbohydr. Res. 20 (1971), 329–337.
33. Kwok, L.-Y., Zhang, J., Guo, Z., Gesudu, Q., Zheng, Y., Qiao, J., Huo, D., Zhang, H., Characterization of fecal microbiota across seven Chinese ethnic groups by quantitative polymerase chain reaction. PLoS ONE, 9, 2014, e93631.
34. Lauderdale, D.S., Rathouz, P.J., Body mass index in a US national sample of Asian Americans: effects of nativity, years since immigration and socioeconomic status. Int. J. Obes. Relat. Metab. Disord. 24 (2000), 1188–1194.
35. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P.M., Henrissat, B., The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42 (2014), D490–D495.
36. Lozupone, C., Lladser, M.E., Knights, D., Stombaugh, J., Knight, R., UniFrac: an effective distance metric for microbial community comparison. ISME J. 5 (2011), 169–172.
37. Minnesota Department of Health (2017). Refugee Health Statistics. http://www.health.state.mn.us/refugee/stats/.
38. Mishra, A., Malhotra, A.V., Tamarind xyloglucan: a polysaccharide with versatile application potential. J. Mater. Chem. 19 (2009), 8528–8536.
39. Muegge, B.D., Kuczynski, J., Knights, D., Clemente, J.C., González, A., Fontana, L., Henrissat, B., Knight, R., Gordon, J.I., Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332 (2011), 970–974.
40. Mulasi-Pokhriyal, U., Smith, C., Franzen-Castle, L., Investigating dietary acculturation and intake among US-born and Thailand/Laos-born Hmong-American children aged 9-18 years. Public Health Nutr. 15 (2012), 176–185.
41. Nurk, S., Meleshko, D., Korobeynikov, A., Pevzner, P.A., metaSPAdes: a new versatile metagenomic assembler. Genome Res. 27 (2017), 824–834.
42. O'Leary, N.A., Wright, M.W., Brister, J.R., Ciufo, S., Haddad, D., McVeigh, R., Rajput, B., Robbertse, B., Smith-White, B., Ako-Adjei, D., et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44:D1 (2016), D733–D745.
43. Obregon-Tito, A.J., Tito, R.Y., Metcalf, J., Sankaranarayanan, K., Clemente, J.C., Ursell, L.K., Zech Xu, Z., Van Treuren, W., Knight, R., Gaffney, P.M., et al. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat. Commun., 6, 2015, 6505.
44. Pangsri, P., Piwpankaew, Y., Ingkakul, A., Nitisinprasert, S., Keawsompong, S., Characterization of mannanase from Bacillus circulans NT 6.7 and its application in mannooligosaccharides preparation as prebiotic. Springerplus, 4, 2015, 771.
45. Pawlowsky-Glahn, V., Buccianti, A., Compositional Data Analysis: Theory and Applications. 2011, John Wiley & Sons.
46. Pfeifer, M.E., Thao, B.K., State of the Hmong American Community. 2013, Hmong National Development.
47. Rothschild, D., Weissbrod, O., Barkan, E., Kurilshikov, A., Korem, T., Zeevi, D., Costea, P.I., Godneva, A., Kalka, I.N., Bar, N., et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 555 (2018), 210–215.
48. Schnorr, S.L., Candela, M., Rampelli, S., Centanni, M., Consolandi, C., Basaglia, G., Turroni, S., Biagi, E., Peano, C., Severgnini, M., et al. Gut microbiome of the Hadza hunter-gatherers. Nat. Commun., 5, 2014, 3654.
49. Schulfer, A.F., Battaglia, T., Alvarez, Y., Bijnens, L., Ruiz, V.E., Ho, M., Robinson, S., Ward, T., Cox, L.M., Rogers, A.B., et al. Intergenerational transfer of antibiotic-perturbed microbiota enhances colitis in susceptible mice. Nat. Microbiol. 3 (2018), 234–242.
50. Seemann, T., Prokka: rapid prokaryotic genome annotation. Bioinformatics 30 (2014), 2068–2069.
51. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., Ideker, T., Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13 (2003), 2498–2504.
52. Smits, S.A., Leach, J., Sonnenburg, E.D., Gonzalez, C.G., Lichtman, J.S., Reid, G., Knight, R., Manjurano, A., Changalucha, J., Elias, J.E., et al. Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. Science 357 (2017), 802–806.
53. Sonnenburg, E.D., Smits, S.A., Tikhonov, M., Higginbottom, S.K., Wingreen, N.S., Sonnenburg, J.L., Diet-induced extinctions in the gut microbiota compound over generations. Nature 529 (2016), 212–215.
54. Speek, A.J., Speek-Saichua, S., Schreurs, W.H.P., Determination of macronutrient and micronutrient levels in thai foods: An evaluation of the Thai Food Composition Table. Food Chem. 40 (1991), 251–262.
55. Subrahmanyan, V., Bains, G.S., Natarajan, C.P., Bhatia, D.S., The carbohydrates of tender kernel of palmyra palm (Borassus flabellifer, L.). Arch. Biochem. Biophys. 60 (1956), 27–34.
56. Suzek, B.E., Wang, Y., Huang, H., McGarvey, P.B., Wu, C.H., UniProt Consortium. UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches. Bioinformatics 31 (2015), 926–932.
57. Sze, M.A., Schloss, P.D., Looking for a Signal in the Noise: Revisiting Obesity and the Microbiome. MBio, 7, 2016.
58. Tatusova, T., DiCuccio, M., Badretdin, A., Chetvernin, V., Ciufo, S., Li, W., The NCBI handbook. 2013, National Center for Biotechnology Information.
59. Tippett, K.S., Enns, C.W., Moshfegh, A.J., Food consumption surveys in the US Department of Agriculture. Nutr. Today 34 (1999), 33–46.
60. Turnbaugh, P.J., Gordon, J.I., The core gut microbiome, energy balance and obesity. J. Physiol. 587 (2009), 4153–4158.
61. Turnbaugh, P.J., Ridaura, V.K., Faith, J.J., Rey, F.E., Knight, R., Gordon, J.I., The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med., 1, 2009, 6ra14.
62. United Nations (2017). International Migration Report 2017. http://www.un.org/en/development/desa/population/migration/publications/migrationreport/docs/MigrationReport2017_Highlights.pdf.
63. United States Department of Agriculture. USDA Food Composition Databases. https://ndb.nal.usda.gov/ndb/.
64. van Rossum, G., Drake, F.L., The Python Language Reference Manual. 2011, Network Theory Ltd.
65. Wu, G.D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y.-Y., Keilbaugh, S.A., Bewtra, M., Knights, D., Walters, W.A., Knight, R., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334 (2011), 105–108.
66. Yatsunenko, T., Rey, F.E., Manary, M.J., Trehan, I., Dominguez-Bello, M.G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R.N., Anokhin, A.P., et al. Human gut microbiome viewed across age and geography. Nature 486 (2012), 222–227.
67. Yin, Y., Mao, X., Yang, J., Chen, X., Mao, F., Xu, Y., dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res., 40, 2012 W445-51.