1887

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Volume 103, Issue 8

Insights into the human gut virome by sampling a population from the Indian subcontinent No Access

Abstract

Gut virome plays an important role in human physiology but remains poorly understood. This study reports an investigation of the human gut DNA-virome of a previously unexplored ethnic population through metagenomics of faecal samples collected from individuals residing in Northern India. Analysis shows that, similar to the populations investigated earlier, majority of the identified virome belongs to bacteriophages and a smaller fraction (<20 %) consists of viruses that infect animals, archaea, protists, multiple domains or plants. However, crAss-like phages, in this population, are dominated by the genera VI, VII and VIII. Interestingly, it also reveals the presence of a virus family, which has not been detected in the human gut earlier. Viral families, , , , , and are detected in all of the analysed individuals, which supports the existence of a core virome. Lysogeny-associated genes were found in less than 10 % of the assembled genomes and a negative correlation was observed in the richness of bacterial and free-viral species, suggesting that the dominant lifestyle of gut phage is not lysogenic. This is in contrast to some of the earlier studies. Further, several hundred high-quality viral genomes were recovered. Detailed characterization of these genomes would be useful for understanding the biology of these viruses and their significance in human physiology.

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  • Accepted:
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Keyword(s): crAss-like phages , gut virome , Indian subcontinent , metagenomics , temperate , total microbial DNA and virus-like-particles
© 2022 The Authors
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/content/journal/jgv/10.1099/jgv.0.001774
2022-08-11
2024-04-26
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References

  1. Matijašić M, Meštrović T, Paljetak HČ, Perić M, Barešić A et al. Gut microbiota beyond bacteria-mycobiome, virome, archaeome, and eukaryotic parasites in IBD. Int J Mol Sci 2020; 21:2668 [View Article] [PubMed]
     [Google Scholar]
  2. Shkoporov AN, Hill C. Bacteriophages of the human gut: the “Known Unknown” of the microbiome. Cell Host Microbe 2019; 25:195–209 [View Article] [PubMed]
     [Google Scholar]
  3. Guerin E, Hill C. Shining light on human gut bacteriophages. Front Cell Infect Microbiol 2020; 10:481 [View Article] [PubMed]
     [Google Scholar]
  4. Rampelli S, Schnorr SL, Consolandi C, Turroni S, Severgnini M et al. Metagenome sequencing of the Hadza hunter-gatherer gut microbiota. Curr Biol 2015; 25:1682–1693 [View Article] [PubMed]
     [Google Scholar]
  5. Dutilh BE, Cassman N, McNair K, Sanchez SE, Silva GGZ et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat Commun 2014; 5:4498 [View Article] [PubMed]
     [Google Scholar]
  6. Camarillo-Guerrero LF, Almeida A, Rangel-Pineros G, Finn RD, Lawley TD. Massive expansion of human gut bacteriophage diversity. Cell 2021; 184:1098–1109 [View Article] [PubMed]
     [Google Scholar]
  7. Gregory AC, Zablocki O, Zayed AA, Howell A, Bolduc B et al. The gut virome database reveals age-dependent patterns of virome diversity in the human gut. Cell Host Microbe 2020; 28:724–740 [View Article] [PubMed]
     [Google Scholar]
  8. Paez-Espino D, Roux S, Chen I-MA, Palaniappan K, Ratner A et al. IMG/VR v.2.0: an integrated data management and analysis system for cultivated and environmental viral genomes. Nucleic Acids Res 2019; 47:D678–D686 [View Article] [PubMed]
     [Google Scholar]
  9. Monaco CL, Gootenberg DB, Zhao G, Handley SA, Ghebremichael MS et al. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome. Cell Host Microbe 2016; 19:311–322 [View Article] [PubMed]
     [Google Scholar]
  10. Norman JM, Handley SA, Baldridge MT, Droit L, Liu CY et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 2015; 160:447–460 [View Article] [PubMed]
     [Google Scholar]
  11. Aggarwala V, Liang G, Bushman FD. Viral communities of the human gut: metagenomic analysis of composition and dynamics. Mob DNA 2017; 8:12 [View Article] [PubMed]
     [Google Scholar]
  12. Reyes A, Haynes M, Hanson N, Angly FE, Heath AC et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 2010; 466:334–338 [View Article] [PubMed]
     [Google Scholar]
  13. Kim MS, Park EJ, Roh SW, Bae JW. Diversity and abundance of single-stranded DNA viruses in human feces. Appl Environ Microbiol 2011; 77:8062–8070 [View Article] [PubMed]
     [Google Scholar]
  14. Minot S, Sinha R, Chen J, Li H, Keilbaugh SA et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 2011; 21:1616–1625 [View Article] [PubMed]
     [Google Scholar]
  15. Moreno-Gallego JL, Chou S-P, Di Rienzi SC, Goodrich JK, Spector TD et al. Virome diversity correlates with intestinal microbiome diversity in adult monozygotic twins. Cell Host Microbe 2019; 25:261–272 [View Article] [PubMed]
     [Google Scholar]
  16. Shkoporov AN, Clooney AG, Sutton TDS, Ryan FJ, Daly KM et al. The human gut virome is highly diverse, stable, and individual specific. Cell Host Microbe 2019; 26:527–541 [View Article] [PubMed]
     [Google Scholar]
  17. Draper LA, Ryan FJ, Smith MK, Jalanka J, Mattila E et al. Long-term colonisation with donor bacteriophages following successful faecal microbial transplantation. Microbiome 2018; 6:220 [View Article] [PubMed]
     [Google Scholar]
  18. Ott SJ, Waetzig GH, Rehman A, Moltzau-Anderson J, Bharti R et al. Efficacy of sterile fecal filtrate transfer for treating patients with clostridium difficile infection. Gastroenterology 2017; 152:799–811 [View Article] [PubMed]
     [Google Scholar]
  19. Pulipati P, Sarkar P, Jakkampudi A, Kaila V, Sarkar S et al. The Indian gut microbiota-Is it unique?. Indian J Gastroenterol 2020; 39:133–140 [View Article] [PubMed]
     [Google Scholar]
  20. Bag S, Saha B, Mehta O, Anbumani D, Kumar N et al. An improved method for high quality metagenomics DNA extraction from human and environmental samples. Sci Rep 2016; 6:26775 [View Article] [PubMed]
     [Google Scholar]
  21. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
     [Google Scholar]
  22. Zolfo M, Pinto F, Asnicar F, Manghi P, Tett A et al. Detecting contamination in viromes using ViromeQC. Nat Biotechnol 2019; 37:1408–1412 [View Article] [PubMed]
     [Google Scholar]
  23. 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; 31:1674–1676 [View Article] [PubMed]
     [Google Scholar]
  24. Ren J, Ahlgren NA, Lu YY, Fuhrman JA, Sun F. VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data. Microbiome 2017; 5:69 [View Article] [PubMed]
     [Google Scholar]
  25. Ren J, Song K, Deng C, Ahlgren NA, Fuhrman JA et al. Identifying viruses from metagenomic data using deep learning. Quant Biol 2020; 8:64–77 [View Article] [PubMed]
     [Google Scholar]
  26. Guo J, Bolduc B, Zayed AA, Varsani A, Dominguez-Huerta G et al. VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome 2021; 9:37 [View Article] [PubMed]
     [Google Scholar]
  27. Roux S, Enault F, Hurwitz BL, Sullivan MB. VirSorter: mining viral signal from microbial genomic data. PeerJ 20153:e985 [View Article] [PubMed]
     [Google Scholar]
  28. Meijenfeldt F von, Arkhipova K, Cambuy DD, Coutinho FH, Dutilh BE. Robust taxonomic classification of uncharted microbial sequences and bins with CAT and BAT. Bioinformatics 2019217 [View Article]
     [Google Scholar]
  29. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006; 22:1658–1659 [View Article] [PubMed]
     [Google Scholar]
  30. Nayfach S, Camargo AP, Schulz F, Eloe-Fadrosh E, Roux S et al. CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nat Biotechnol 2021; 39:578–585 [View Article] [PubMed]
     [Google Scholar]
  31. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article] [PubMed]
     [Google Scholar]
  32. Menzel P, Ng KL, Krogh A. Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun 2016; 7:11257 [View Article] [PubMed]
     [Google Scholar]
  33. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article] [PubMed]
     [Google Scholar]
  34. Bin Jang H, Bolduc B, Zablocki O, Kuhn JH, Roux S et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat Biotechnol 2019; 37:632–639 [View Article] [PubMed]
     [Google Scholar]
  35. Yan A, Butcher J, Mack D, Stintzi A. Virome sequencing of the human intestinal mucosal-luminal interface. Front Cell Infect Microbiol 2020; 10:582187 [View Article] [PubMed]
     [Google Scholar]
  36. Bairoch A, Apweiler R. The SWISS-PROT protein sequence data bank and its supplement TrEMBL. Nucleic Acids Res 1997; 25:31–36 [View Article] [PubMed]
     [Google Scholar]
  37. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S et al. NCBI BLAST: a better web interface. Nucleic Acids Res 2008; 36:W5–9 [View Article] [PubMed]
     [Google Scholar]
  38. Guerin E, Shkoporov A, Stockdale SR, Clooney AG, Ryan FJ et al. Biology and taxonomy of crAss-like bacteriophages, the most abundant virus in the human gut. Cell Host Microbe 2018; 24:653–664 [View Article] [PubMed]
     [Google Scholar]
  39. Yutin N, Makarova KS, Gussow AB, Krupovic M, Segall A et al. Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nat Microbiol 2018; 3:38–46 [View Article] [PubMed]
     [Google Scholar]
  40. El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A et al. The Pfam protein families database in 2019. Nucleic Acids Res 2019; 47:D427–D432 [View Article] [PubMed]
     [Google Scholar]
  41. Cook R, Hooton S, Trivedi U, King L, Dodd CER et al. Hybrid assembly of an agricultural slurry virome reveals a diverse and stable community with the potential to alter the metabolism and virulence of veterinary pathogens. Microbiome 2021; 9:65 [View Article] [PubMed]
     [Google Scholar]
  42. Rob Finn HMMER: fast and sensitive sequence similarity searches. EBI Resources 2018 [View Article]
     [Google Scholar]
  43. Guerin E, Shkoporov AN, Stockdale SR, Comas JC, Khokhlova EV et al. Isolation and characterisation of ΦcrAss002, a crAss-like phage from the human gut that infects Bacteroides xylanisolvens. Microbiome 2021; 9:89 [View Article] [PubMed]
     [Google Scholar]
  44. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article] [PubMed]
     [Google Scholar]
  45. Rampelli S, Soverini M, Turroni S, Quercia S, Biagi E et al. ViromeScan: a new tool for metagenomic viral community profiling. BMC Genomics 2016; 17:165 [View Article] [PubMed]
     [Google Scholar]
  46. Pruitt KD, Tatusova T, Maglott DR. NCBI reference sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 2005; 33:D501–4 [View Article] [PubMed]
     [Google Scholar]
  47. Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC. Integrative analysis of environmental sequences using MEGAN4. Genome Res 2011; 21:1552–1560 [View Article] [PubMed]
     [Google Scholar]
  48. Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci 2003; 14:927–930 [View Article]
     [Google Scholar]
  49. Keegan KP, Glass EM, Meyer F. MG-RAST, a metagenomics service for analysis of microbial community structure and function. Methods Mol Biol 2016; 1399:207–233 [View Article] [PubMed]
     [Google Scholar]
  50. Sutton TDS, Hill C. Gut bacteriophage: current understanding and challenges. Front Endocrinol (Lausanne) 2019; 10:784 [View Article] [PubMed]
     [Google Scholar]
  51. Manrique P, Bolduc B, Walk ST, van der Oost J, de Vos WM et al. Healthy human gut phageome. Proc Natl Acad Sci U S A 2016; 113:10400–10405 [View Article] [PubMed]
     [Google Scholar]
  52. Yan Q, Wang Y, Chen X, Jin H, Wang G et al. Characterization of the gut DNA and RNA Viromes in a Cohort of Chinese Residents and Visiting Pakistanis. Virus Evol 2021; 7:veab022 [View Article] [PubMed]
     [Google Scholar]
  53. Yolken RH, Jones-Brando L, Dunigan DD, Kannan G, Dickerson F et al. Chlorovirus ATCV-1 is part of the human oropharyngeal virome and is associated with changes in cognitive functions in humans and mice. Proc Natl Acad Sci U S A 2014; 111:16106–16111 [View Article] [PubMed]
     [Google Scholar]
  54. Edwards RA, Vega AA, Norman HM, Ohaeri M, Levi K et al. Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nat Microbiol 2019; 4:1727–1736 [View Article] [PubMed]
     [Google Scholar]
  55. Minot S, Bryson A, Chehoud C, Wu GD, Lewis JD et al. Rapid evolution of the human gut virome. Proc Natl Acad Sci U S A 2013; 110:12450–12455 [View Article] [PubMed]
     [Google Scholar]
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Insights into the human gut virome by sampling a population from the Indian subcontinent
J. Gen. Virol. 103, 001774 (2022); https://doi.org/10.1099/jgv.0.001774
/content/journal/jgv/10.1099/jgv.0.001774
/content/journal/jgv/10.1099/jgv.0.001774
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