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Biogeographic study of human gut-associated crAssphage suggests impacts from industrialization and recent expansion


Autoři: Tanvi P. Honap aff001;  Krithivasan Sankaranarayanan aff001;  Stephanie L. Schnorr aff001;  Andrew T. Ozga aff001;  Christina Warinner aff001;  Cecil M. Lewis, Jr. aff001
Působiště autorů: Laboratories of Molecular Anthropology and Microbiome Research, University of Oklahoma, Norman, Oklahoma, United States of America aff001;  Department of Anthropology, University of Oklahoma, Norman, Oklahoma, United States of America aff002;  Department of Microbiology and Plant Biology, University of Oklahoma, Norman, Oklahoma, United States of America aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226930

Souhrn

CrAssphage (cross-assembly phage) is a bacteriophage that was first discovered in human gut metagenomic data. CrAssphage belongs to a diverse family of crAss-like bacteriophages thought to infect gut commensal bacteria belonging to Bacteroides species. However, not much is known about the biogeography of crAssphage and whether certain strains are associated with specific human populations. In this study, we screened publicly available human gut metagenomic data from 3,341 samples for the presence of crAssphage sensu stricto (NC_024711.1). We found that crAssphage prevalence is low in traditional, hunter-gatherer populations, such as the Hadza from Tanzania and Matses from Peru, as compared to industrialized, urban populations. Statistical comparisons showed no association of crAssphage prevalence with variables such as age, sex, body mass index, and health status of individuals. Phylogenetic analyses show that crAssphage strains reconstructed from the same individual over multiple time-points, cluster together. CrAssphage strains from individuals from the same study population do not always cluster together. Some evidence of clustering is seen at the level of broadly defined geographic regions, however, the relative positions of these clusters within the crAssphage phylogeny are not well-supported. We hypothesize that this lack of strong biogeographic structuring is suggestive of an expansion event within crAssphage. Using a Bayesian dating approach, we estimate that this expansion has occurred fairly recently. Overall, we determine that crAssphage presence is associated with an industrialized lifestyle and the absence of strong biogeographic structuring within global crAssphage strains is likely due to a recent population expansion within this bacteriophage.

Klíčová slova:

Bacteriophages – Bacteroides – Biogeography – Infants – Metagenomics – Phylogenetic analysis – Phylogenetics – Phylogeography


Zdroje

1. Virgin HW. The virome in mammalian physiology and disease. Cell. 2014;157(1):142–50. doi: 10.1016/j.cell.2014.02.032 24679532

2. Rohwer F, Youle M. Consider something viral in your research. Nat Rev Micro. 2011;9(5):308–9.

3. De Paepe M, Leclerc M, Tinsley CR, Petit MA. Bacteriophages: an underestimated role in human and animal health? Frontiers in cellular and infection microbiology. 2014;4:39. doi: 10.3389/fcimb.2014.00039 24734220

4. Reyes A, Semenkovich NP, Whiteson K, Rohwer F, Gordon JI. Going viral: next-generation sequencing applied to phage populations in the human gut. Nat Rev Microbiol. 2012;10(9):607–17. doi: 10.1038/nrmicro2853 22864264

5. Williams SC. The other microbiome. Proc Natl Acad Sci U S A. 2013;110(8):2682–4. doi: 10.1073/pnas.1300923110 23388628

6. Modi SR, Lee HH, Spina CS, Collins JJ. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature. 2013;499(7457):219. doi: 10.1038/nature12212 23748443

7. Manrique P, Bolduc B, Walk ST, van der Oost J, de Vos WM, Young MJ. Healthy human gut phageome. Proceedings of the National Academy of Sciences. 2016;113(37):10400.

8. Shkoporov AN, Hill C. Bacteriophages of the Human Gut: The "Known Unknown" of the Microbiome. Cell Host Microbe. 2019;25(2):195–209. doi: 10.1016/j.chom.2019.01.017 30763534

9. Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GGZ, Boling L, et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat Commun. 2014;5.

10. Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature. 2010;466(7304):334–8. doi: 10.1038/nature09199 20631792

11. Group NHW, Peterson J, Garges S, Giovanni M, McInnes P, Wang L, et al. The NIH Human Microbiome Project. Genome Res. 2009;19(12):2317–23. doi: 10.1101/gr.096651.109 19819907

12. Yutin N, Makarova KS, Gussow AB, Krupovic M, Segall A, Edwards RA, et al. Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nat Microbiol. 2018;3(1):38–46. doi: 10.1038/s41564-017-0053-y 29133882

13. Shkoporov AN, Khokhlova EV, Fitzgerald CB, Stockdale SR, Draper LA, Ross RP, et al. ΦCrAss001 represents the most abundant bacteriophage family in the human gut and infects Bacteroides intestinalis. Nature Communications. 2018;9(1):4781. doi: 10.1038/s41467-018-07225-7 30429469

14. Cinek O, Mazankova K, Kramna L, Odeh R, Alassaf A, Ibekwe MU, et al. Quantitative CrAssphage real-time PCR assay derived from data of multiple geographically distant populations. J Med Virol. 2018;90(4):767–71. doi: 10.1002/jmv.25012 29297933

15. Holmfeldt K, Solonenko N, Shah M, Corrier K, Riemann L, VerBerkmoes NC, et al. Twelve previously unknown phage genera are ubiquitous in global oceans. Proceedings of the National Academy of Sciences. 2013;110(31):12798.

16. Edwards RA, Vega AA, Norman HM, Ohaeri M, Levi K, Dinsdale EA, et al. Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nature Microbiology. 2019.

17. Ahmed W, Lobos A, Senkbeil J, Peraud J, Gallard J, Harwood VJ. Evaluation of the novel crAssphage marker for sewage pollution tracking in storm drain outfalls in Tampa, Florida. Water Res. 2017;131:142–50. doi: 10.1016/j.watres.2017.12.011 29281808

18. Garcia-Aljaro C, Balleste E, Muniesa M, Jofre J. Determination of crAssphage in water samples and applicability for tracking human faecal pollution. Microb Biotechnol. 2017;10(6):1775–80. doi: 10.1111/1751-7915.12841 28925595

19. Stachler E, Kelty C, Sivaganesan M, Li X, Bibby K, Shanks OC. Quantitative CrAssphage PCR Assays for Human Fecal Pollution Measurement. Environ Sci Technol. 2017;51(16):9146–54. doi: 10.1021/acs.est.7b02703 28700235

20. Farkas K, Adriaenssens EM, Walker DI, McDonald JE, Malham SK, Jones DL. Critical Evaluation of CrAssphage as a Molecular Marker for Human-Derived Wastewater Contamination in the Aquatic Environment. Food and Environmental Virology. 2019.

21. Tamburini FB, Sherlock GJ, Bhatt AS. Transmission and persistence of crAssphage, a ubiquitous human-associated bacteriophage. bioRxiv. 2018:460113.

22. Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life. Cell Host Microbe. 2015;17(5):690–703. doi: 10.1016/j.chom.2015.04.004 25974306

23. Guerin E, Shkoporov A, Stockdale SR, Clooney AG, Ryan FJ, Sutton TDS, et al. Biology and Taxonomy of crAss-like Bacteriophages, the Most Abundant Virus in the Human Gut. Cell Host Microbe. 2018;24(5):653–64 e6. doi: 10.1016/j.chom.2018.10.002 30449316

24. Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. The Isme Journal. 2017;11:2639. doi: 10.1038/ismej.2017.119 28731476

25. Sankaranarayanan K, Ozga AT, Warinner C, Tito RY, Obregon-Tito AJ, Xu J, et al. Gut Microbiome Diversity among Cheyenne and Arapaho Individuals from Western Oklahoma. Curr Biol. 2015;25(24):3161–9. doi: 10.1016/j.cub.2015.10.060 26671671

26. Rampelli S, Schnorr Stephanie L, Consolandi C, Turroni S, Severgnini M, Peano C, et al. Metagenome Sequencing of the Hadza Hunter-Gatherer Gut Microbiota. Current Biology. 2015;25(13):1682–93. doi: 10.1016/j.cub.2015.04.055 25981789

27. 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(6353):802. doi: 10.1126/science.aan4834 28839072

28. Zeevi D, Korem T, Zmora N, Israeli D, Rothschild D, Weinberger A, et al. Personalized Nutrition by Prediction of Glycemic Responses. Cell. 2015;163(5):1079–94. doi: 10.1016/j.cell.2015.11.001 26590418

29. Karlsson FH, Tremaroli V, Nookaew I, Bergstrom G, Behre CJ, Fagerberg B, et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013;498(7452):99–103. doi: 10.1038/nature12198 23719380

30. Liu W, Zhang J, Wu C, Cai S, Huang W, Chen J, et al. Unique Features of Ethnic Mongolian Gut Microbiome revealed by metagenomic analysis. Sci Rep. 2016;6:34826. doi: 10.1038/srep34826 27708392

31. 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. doi: 10.1038/ncomms7505 25807110

32. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60. doi: 10.1038/nature11450 23023125

33. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013;500(7464):541–6. doi: 10.1038/nature12506 23985870

34. Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32(8):834–41. doi: 10.1038/nbt.2942 24997786

35. 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(8):822–8. doi: 10.1038/nbt.2939 24997787

36. Xie H, Guo R, Zhong H, Feng Q, Lan Z, Qin B, et al. Shotgun Metagenomics of 250 Adult Twins Reveals Genetic and Environmental Impacts on the Gut Microbiome. Cell Syst. 2016;3(6):572–84 e3. doi: 10.1016/j.cels.2016.10.004 27818083

37. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature Methods. 2012;9:357. doi: 10.1038/nmeth.1923 22388286

38. Li D, Liu C-M, Luo R, Sadakane K, Lam T-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31(10):1674–6. doi: 10.1093/bioinformatics/btv033 25609793

39. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. Journal of Molecular Biology. 1990;215(3):403–10. doi: 10.1016/S0022-2836(05)80360-2 2231712

40. Adriaenssens E, Brister JR. How to Name and Classify Your Phage: An Informal Guide. Viruses. 2017;9(4):70.

41. Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G, et al. Gut microbiome of the Hadza hunter-gatherers. Nature Communications. 2014;5:3654. doi: 10.1038/ncomms4654 24736369

42. 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. doi: 10.1038/nature11053 22699611

43. Maixner F, Krause-Kyora B, Turaev D, Herbig A, Hoopmann MR, Hallows JL, et al. The 5300-year-old Helicobacter pylori genome of the Iceman. Science. 2016;351(6269):162. doi: 10.1126/science.aad2545 26744403

44. Ozga AT. Viral Metagenomics and Anthropology in the Americas [Ph.D. dissertation]. Norman: University of Oklahoma; 2015.

45. Gupta VK, Paul S, Dutta C. Geography, Ethnicity or Subsistence-Specific Variations in Human Microbiome Composition and Diversity. Front Microbiol. 2017;8:1162. doi: 10.3389/fmicb.2017.01162 28690602

46. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology. 2007;7(1):214.

47. Shkoporov AN, Clooney AG, Sutton TDS, Ryan FJ, Daly KM, Nolan JA, et al. The Human Gut Virome Is Highly Diverse, Stable, and Individual Specific. Cell Host & Microbe. 2019;26(4):527–41.e5.

48. Schubert M, Lindgreen S, Orlando L. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Research Notes. 2016;9. doi: 10.1186/s13104-015-1814-4

49. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9. doi: 10.1093/bioinformatics/btp352 19505943

50. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, et al. VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Research. 2012;22(3):568–76. doi: 10.1101/gr.129684.111 22300766

51. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11(1):119.

52. Team RC. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2010.

53. 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(7):5069–72. doi: 10.1128/AEM.03006-05 16820507

54. Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. doi: 10.7717/peerj.2584 27781170

55. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods. 2010;7:335. doi: 10.1038/nmeth.f.303 20383131

56. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research. 2004;32(5):1792–7. doi: 10.1093/nar/gkh340 15034147

57. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–3. doi: 10.1093/bioinformatics/btu033 24451623

58. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Systematic Biology. 2018:syy032–syy.


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