Biology and Taxonomy of crAss-like Bacteriophages, the Most Abundant Virus in the Human Gut

Cell Host and Microbe

Volumn 24, Issue 5, 2018, Pages 653-664.e6

  Guerin, Emma ^a,b   Shkoporov, Andrey ^a   Stockdale, Stephen R ^a,c   Clooney, Adam G ^a   Ryan, Feargal J ^a   Sutton, Thomas D S ^a,b   Draper, Lorraine A ^a   Gonzalez Tortuero, Enrique ^a   Ross, R Paul ^a,b,c   Hill, Colin ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c TEAGASC FOOD RESEARCH CENTRE   (Ireland)

Author keywords

bacteriophages; crAssphage; gut microbiota; human microbiome; phage characterization; phage taxonomy

Indexed keywords

CAPSID PROTEIN; CONTIG; DNA VIRUS; VIRAL PROTEIN;

ARTICLE; BACTERIOPHAGE; COMPUTER MODEL; CRASS LIKE BACTERIOPHAGE; ELECTRON MICROSCOPY; EX VIVO STUDY; FECES ANALYSIS; FERMENTATION; GENE SEQUENCE; INTESTINE; MASS SPECTROMETRY; METAGENOMICS; MICROBIOME; NONHUMAN; PRIORITY JOURNAL; TAXONOMY; VIRUS GENOME; VIRUS MORPHOLOGY; CLASSIFICATION; FECES; GENETICS; GENOMICS; HUMAN; INTESTINE FLORA; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PROCEDURES; SEQUENCE ANALYSIS; ULTRASTRUCTURE; VIROLOGY;

BACTERIOPHAGES; BASE SEQUENCE; CAPSID PROTEINS; DNA VIRUSES; FECES; FERMENTATION; GASTROINTESTINAL MICROBIOME; GENOME, VIRAL; GENOMICS; HUMANS; METAGENOMICS; PHYLOGENY; SEQUENCE ANALYSIS; VIRAL PROTEINS;

EID: 85056591119     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2018.10.002     Document Type: Article

References (63)

1. Adriaenssens, E., Brister, J.R., How to name and classify your phage: an informal guide. Viruses, 9, 2017, 10.3390/v9040070.
2. Allard, G., Ryan, F.J., Jeffery, I.B., Claesson, M.J., SPINGO: a rapid species-classifier for microbial amplicon sequences. BMC Bioinformatics, 16, 2015, 324.
3. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997), 3389–3402.
4. Anderson, M.J., A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26 (2001), 32–46.
5. Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D.R., Fernandes, G.R., Tap, J., Bruls, T., Batto, J.-M., et al. Enterotypes of the humangutmicrobiome. Nature 473 (2011), 174–180.
6. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Pham, S., Prjibelski, A.D., et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19 (2012), 455–477.
7. Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 (2014), 2114–2120.
8. Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13 (2016), 581–583.
9. Cinek, O., Kramna, L., Lin, J., Oikarinen, S., Kolarova, K., Ilonen, J., Simell, O., Veijola, R., Autio, R., Hyöty, H., Imbalance of bacteriome profiles within the Finnish Diabetes Prediction and Prevention study: parallel use of 16S profiling and virome sequencing in stool samples from children with islet autoimmunity and matched controls. Pediatr. Diabetes 18 (2017), 588–598.
10. Cinek, O., Mazankova, K., Kramna, L., Odeh, R., Alassaf, A., Ibekwe, M.U., Ahmadov, G., Mekki, H., Abdullah, M.A., Elmahi, B.M.E., et al. Quantitative CrAssphage real-time PCR assay derived from data of multiple geographically distant populations. J. Med. Virol. 90 (2018), 767–771.
11. Claesson, M.J., Jeffery, I.B., Conde, S., Power, S.E., O'Connor, E.M., Cusack, S., Harris, H.M.B., Coakley, M., Lakshminarayanan, B., O'Sullivan, O., et al. Gut microbiota composition correlates with diet and health in the elderly. Nature 488 (2012), 178–184.
12. Cryan, J.F., Dinan, T.G., Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13 (2014), 701–712.
13. Duncan, S.H., Hold, G.L., Harmsen, H.J.M., Stewart, C.S., Flint, H.J., Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 52 (2002), 2141–2146.
14. Dutilh, B.E., Cassman, N., McNair, K., Sanchez, S.E., Silva, G.G.Z., Boling, L., Barr, J.J., Speth, D.R., Seguritan, V., Aziz, R.K., et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun., 5, 2014, 5498.
15. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 (2010), 2460–2461.
16. Edwards, R.A., McNair, K., Faust, K., Raes, J., Dutilh, B.E., Computational approaches to predict bacteriophage–host relationships. FEMS Microbiol. Rev. 40 (2016), 258–272.
17. Everard, A., Cani, P.D., Diabetes, obesity and gut microbiota. Best Pract. Res. Clin. Gastroenterol. 27 (2013), 73–83.
18. Filippo, C.D., Cavalieri, D., Paola, M.D., 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. U S A 107 (2010), 14691–14696.
19. Frank, D.N., Robertson, C.E., Hamm, C.M., Kpadeh, Z., Zhang, T., Chen, H., Zhu, W., Sartor, R.B., Boedeker, E.C., Harpaz, N., et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm. Bowel Dis. 17 (2011), 179–184.
20. García-Aljaro, C., Ballesté, E., Muniesa, M., Jofre, J., Determination of crAssphage in water samples and applicability for tracking human faecal pollution. Microb. Biotechnol. 10 (2017), 1775–1780.
21. Garneau, J.R., Depardieu, F., Fortier, L.-C., Bikard, D., Monot, M., PhageTerm: a tool for fast and accurate determination of phage termini and packaging mechanism using next-generation sequencing data. Sci. Rep., 7, 2017, 8292.
22. Gorvitovskaia, A., Holmes, S.P., Huse, S.M., Interpreting Prevotella and Bacteroides as biomarkers of diet and lifestyle. Microbiome, 4, 2016, 15.
23. Henry, M., Bobay, L.-M., Chevallereau, A., Saussereau, E., Ceyssens, P.-J., Debarbieux, L., The search for therapeutic bacteriophages uncovers one new subfamily and two new genera of pseudomonas-infecting myoviridae. PLoS One, 10, 2015, e0117163.
24. Hyatt, D., Chen, G.-L., LoCascio, P.F., Land, M.L., Larimer, F.W., Hauser, L.J., Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics, 11, 2010, 119.
25. Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., Glöckner, F.O., Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res., 41, 2013, e1.
26. Langmead, B., Salzberg, S.L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 (2012), 357–359.
27. Laslett, D., Canback, B., ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res. 32 (2004), 11–16.
28. Lavigne, R., Seto, D., Mahadevan, P., Ackermann, H.-W., Kropinski, A.M., Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res. Microbiol. 159 (2008), 406–414.
29. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., The sequence alignment/map format and SAMtools. Bioinformatics 25 (2009), 2078–2079.
30. Li, L., Stoeckert, C.J., Roos, D.S., OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13 (2003), 2178–2189.
31. Liang, Y., Jin, X., Huang, Y., Chen, S., Development and application of a real-time polymerase chain reaction assay for detection of a novel gut bacteriophage (crAssphage). J. Med. Virol. 90 (2018), 464–468.
32. Liang, Y.Y., Zhang, W., Tong, Y.G., Chen, S.P., crAssphage is not associated with diarrhoea and has high genetic diversity. Epidemiol. Infect. 144 (2016), 3549–3553.
33. Lucks, J.B., Nelson, D.R., Kudla, G.R., Plotkin, J.B., Genome landscapes and bacteriophage codon usage. PLoS Comput. Biol., 4, 2008, e1000001.
34. van der Maaten, L., Hinton, G., Visualizing data using t-SNE. J. Mach. Learn. Res. 9 (2008), 2579–2605.
35. Manrique, P., Bolduc, B., Walk, S.T., van der Oost, J., de Vos, W.M., Young, M.J., Healthy human gut phageome. Proc. Natl. Acad. Sci. U S A 113 (2016), 10400–10405.
36. Manrique, P., Dills, M., Young, M.J., The human gut phage community and its implications for health and disease. Viruses, 9, 2017, 141.
37. Marshall, O.J., PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20 (2004), 2471–2472.
38. Mavrich, T.N., Hatfull, G.F., Bacteriophage evolution differs by host, lifestyle and genome. Nat. Microbiol., 2, 2017, 17112.
39. Mills, S., Shanahan, F., Stanton, C., Hill, C., Coffey, A., Ross, R.P., Movers and shakers: influence of bacteriophages in shaping the mammalian gut microbiota. Gut Microbes 4 (2013), 4–16.
40. Milne, I., Bayer, M., Cardle, L., Shaw, P., Stephen, G., Wright, F., Marshall, D., Tablet—next generation sequence assembly visualization. Bioinformatics 26 (2010), 401–402.
41. Minot, S., Sinha, R., Chen, J., Li, H., Keilbaugh, S.A., Wu, G.D., Lewis, J.D., Bushman, F.D., The human gut virome: inter-individual variation and dynamic response to diet. Genome Res. 21 (2011), 1616–1625.
42. Norman, J.M., Handley, S.A., Baldridge, M.T., Droit, L., Liu, C.Y., Keller, B.C., Kambal, A., Monaco, C.L., Zhao, G., Fleshner, P., et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160 (2015), 447–460.
43. Nurk, S., Meleshko, D., Korobeynikov, A., Pevzner, P.A., metaSPAdes: a new versatile metagenomic assembler. Genome Res. 27 (2017), 824–834.
44. O'Donnell, M.M., Rea, M.C., O'Sullivan, Ó., Flynn, C., Jones, B., McQuaid, A., Shanahan, F., Ross, R.P., Preparation of a standardised faecal slurry for ex-vivo microbiota studies which reduces inter-individual donor bias. J. Microbiol. Methods 129 (2016), 109–116.
45. Pride, D.T., Wassenaar, T.M., Ghose, C., Blaser, M.J., Evidence of host-virus co-evolution in tetranucleotide usage patterns of bacteriophages and eukaryotic viruses. BMC Genomics, 7, 2006, 8.
46. Reyes, A., Haynes, M., Hanson, N., Angly, F.E., Heath, A.C., Rohwer, F., Gordon, J.I., Viruses in the fecal microbiota of monozygotic twins and their mothers. Nature 466 (2010), 334–338.
47. Reyes, A., Wu, M., McNulty, N.P., Rohwer, F.L., Gordon, J.I., Gnotobiotic mouse model of phage-bacterial host dynamics in the human gut. Proc. Natl. Acad. Sci. U S A. 110 (2013), 20236–20241.
48. Reyes, A., Blanton, L.V., Cao, S., Zhao, G., Manary, M., Trehan, I., Smith, M.I., Wang, D., Virgin, H.W., Rohwer, F., et al. Gut DNA viromes of Malawian twins discordant for severe acute malnutrition. Proc. Natl. Acad. Sci. U S A. 112 (2015), 11941–11946.
49. Roux, S., Krupovic, M., Poulet, A., Debroas, D., Enault, F., Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLoS One, 7, 2012, e40418.
50. Roux, S., Hallam, S.J., Woyke, T., Sullivan, M.B., Viral dark matter and virus–host interactions resolved from publicly available microbial genomes. Elife, 4, 2015, e08490.
51. Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75 (2009), 7537–7541.
52. Shkoporov, A., Khokhlova, E.V., Fitzgerald, C.B., Stockdale, S.R., Draper, L.A., Ross, R.P., Hill, C., ΦCrAss001, a member of the most abundant bacteriophage family in the human gut, infects Bacteroides. bioRxiv, 2018, 10.1101/354837.
53. Smith, M.I., Yatsunenko, T., Manary, M.J., Trehan, I., Mkakosya, R., Cheng, J., Kau, A.L., Rich, S.S., Concannon, P., Mychaleckyj, J.C., et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339 (2013), 548–554.
54. Söding, J., Biegert, A., Lupas, A.N., The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33 (2005), W244–W248.
55. Stachler, E., Kelty, C., Sivaganesan, M., Li, X., Bibby, K., Shanks, O.C., Quantitative CrAssphage PCR assays for human fecal pollution measurement. Environ. Sci. Technol. 51 (2017), 9146–9154.
56. Sullivan, M.J., Petty, N.K., Beatson, S.A., Easyfig: a genome comparison visualizer. Bioinformatics 27 (2011), 1009–1010.
57. Tremaroli, V., Bäckhed, F., Functional interactions between the gut microbiota and host metabolism. Nature, 489, 2012, 242.
58. Vollmers, J., Wiegand, S., Kaster, A.-K., Comparing and evaluating metagenome assembly tools from a microbiologist's perspective—not only size matters!. PLoS One, 12, 2017, e0169662.
59. Ward, J.H.J., Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58 (1963), 236–244.
60. Wickham, H., ggplot2: Elegant Graphics for Data Analysis. 2009, Springer-Verlag.
61. Yutin, N., Makarova, K.S., Gussow, A.B., Krupovic, M., Segall, A., Edwards, R.A., Koonin, E.V., Discovery of an expansive bacteriophage family that includes the most abundant viruses from the human gut. Nat. Microbiol. 3 (2018), 38–46.
62. Zhong, X., Guidoni, B., Jacas, L., Jacquet, S., Structure and diversity of ssDNA Microviridae viruses in two peri-alpine lakes (Annecy and Bourget, France). Res. Microbiol. 166 (2015), 644–654.
63. Zimmermann, L., Stephens, A., Nam, S.-Z., Rau, D., Kübler, J., Lozajic, M., Gabler, F., Söding, J., Lupas, A.N., Alva, V., A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J. Mol. Biol. 430 (2017), 2237–2243.