Scaffolding bacterial genomes and probing host-virus interactions in gut microbiome by proximity ligation (chromosome capture) assay

Science Advances

Volumn 3, Issue 2, 2017, Pages

  Marbouty, Martial ^a,b   Baudry, Lyam ^a,b   Cournac, Axel ^a,b   Koszul, Romain ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ECOLOGY; ECOSYSTEMS; MOLECULES; SCAFFOLDS; VIRUSES;

BACTERIAL GENOMES; BIOCHEMICAL ACTIVITY; COMPUTATIONAL APPROACH; GENOMIC STRUCTURE; GUT MICROBIOTA; HOST-VIRUS INTERACTIONS; MICROBIAL COMMUNITIES; PHYSICAL CONTACTS;

GENES;

ANIMAL; BACTERIAL GENOME; BACTERIOPHAGE; BACTERIUM; GENETICS; INTESTINE FLORA; MALE; METABOLISM; MOUSE; VIROLOGY; VIRUS GENOME;

ANIMALS; BACTERIA; BACTERIOPHAGES; GASTROINTESTINAL MICROBIOME; GENOME, BACTERIAL; GENOME, VIRAL; MALE; MICE;

EID: 85020779896     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1602105     Document Type: Article

References (64)

1. J. Handelsman, M. R. Rondon, S. F. Brady, J. Clardy, R. M. Goodman, Molecular biological access to the chemistry of unknown soil microbes: A new frontier for natural products. Chem. Biol. 5, R245–R249 (1998).
2. P. Hugenholtz, B. M. Goebel, N. R. Pace, Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180, 4765–4774 (1998).
3. J. Qin, R. Li, J. Raes, M. Arumugam, K. S. Burgdorf, C. Manichanh, T. Nielsen, N. Pons, F. Levenez, T. Yamada, D. R. Mende, J. Li, J. Xu, S. Li, D. Li, J. Cao, B. Wang, H. Liang, H. Zheng, Y. Xie, J. Tap, P. Lepage, M. Bertalan, J.-M. Batto, T. Hansen, D. Le Paslier, A. Linneberg, H. B. Nielsen, E. Pelletier, P. Renault, T. Sicheritz-Ponten, K. Turner, H. Zhu, C. Yu, S. Li, M. Jian, Y. Zhou, Y. Li, X. Zhang, S. Li, N. Qin, H. Yang, J. Wang, S. Brunak, J. Doré, F. Guarner, K. Kristiansen, O. Pedersen, J. Parkhill, J. Weissenbach; MetaHIT Consortium, P. Bork, S. D. Ehrlich, J. Wang, A human gut microbial gene catalog established by metagenomic sequencing. Nature 464, 59–65 (2010).
4. J. C. Venter, K. Remington, J. F. Heidelberg, A. L. Halpern, D. Rusch, J. A. Eisen, D. Wu, I. Paulsen, K. E. Nelson, W. Nelson, D. E. Fouts, S. Levy, A. H. Knap, M. W. Lomas, K. Nealson, O. White, J. Peterson, J. Hoffman, R. Parsons, H. Baden-Tillson, C. Pfannkoch, Y.-H. Rogers, H. O. Smith, Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004).
5. N. R. Pace, A molecular view of microbial diversity and the biosphere. Science 276, 734–740 (1997).
6. F. Partensky, W. R. Hess, D. Vaulot, Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63, 106–127 (1999).
7. A. L. Kau, P. P. Ahern, N. W. Griffin, A. L. Goodman, J. I. Gordon, Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336 (2011).
8. J. F. Cryan, T. G. Dinan, Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701–712 (2012).
9. L. Philippot, J. M. Raaijmakers, P. Lemanceau, W. H. van der Putten, Going back to the roots: The microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799 (2013).
10. J. Yang, J. W. Kloepper, C.-M. Ryu, Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14, 1–4 (2009).
11. L. A. Hug, B. J. Baker, K. Anantharaman, C. T. Brown, A. J. Probst, C. J. Castelle, C. N. Butterfield, A. W. Hernsdorf, Y. Amano, K. Ise, Y. Suzuki, N. Dudek, D. A. Relman, K. M. Finstad, R. Amundson, B. C. Thomas, J. F. Banfield, A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).
12. S. Guermazi, P. Daegelen, C. Dauga, D. Rivière, T. Bouchez, J. J. Godon, G. Gyapay, A. Sghir, E. Pelletier, J. Weissenbach, D. Le Paslier, Discovery and characterization of a new bacterial candidate division by an anaerobic sludge digester metagenomic approach. Environ. Microbiol. 10, 2111–2123 (2008).
13. P. Bork, C. Bowler, C. de Vargas, G. Gorsky, E. Karsenti, P. Wincker, Tara Oceans studies plankton at planetary scale. Science 348, 873 (2015).
14. H. B. Nielsen, M. Almeida, A. S. Juncker, S. Rasmussen, J. Li, S. Sunagawa, D. R. Plichta, L. Gautier, A. G. Pedersen, E. L. Chatelier, E. Pelletier, I. Bonde, T. Nielsen, C. Manichanh, M. Arumugam, J.-M. Batto, M. B. Quintanilha dos Santos, N. Blom, N. Borruel, K. S. Burgdorf, F. Boumezbeur, F. Casellas, J. Doré, P. Dworzynski, F. Guarner, T. Hansen, F. Hildebrand, R. S. Kaas, S. Kennedy, K. Kristiansen, J. R. Kultima, P. Léonard, F. Levenez, O. Lund, B. Moumen, D. Le Paslier, N. Pons, O. Pedersen, E. Prifti, J. Qin, J. Raes, S. Sørensen, J. Tap, S. Tims, D. W. Ussery, T. Yamada; MetaHIT Consortium, P. Renault, T. Sicheritz-Ponten, P. Bork, J. Wang, S. Brunak, S. D. Ehrlich, Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat. Biotechnol. 32, 822–828 (2014).
15. A. Schlüter, L. Krause, R. Szczepanowski, A. Goesmann, A. Pühler, Genetic diversity and composition of a plasmid metagenome from a wastewater treatment plant. J. Biotechnol. 136, 65–76 (2008).
16. V. Sentchilo, A. P. Mayer, L. Guy, R. Miyazaki, S. G. Tringe, K. Barry, Community-wide plasmid gene mobilization and selection. ISME J. 7, 1173–1186 (2013).
17. L. A. Ogilvie, B. V. Jones, The human gut virome: A multifaceted majority. Front. Microbiol. 6, 918 (2015).
18. E. S. Lim, Y. Zhou, G. Zhao, I. K. Bauer, L. Droit, I. M. Ndao, B. B. Warner, P. I. Tarr, D. Wang, L. R. Holtz, Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat. Med. 21, 1228–1234 (2015).
19. M. Breitbart, P. Salamon, B. Andresen, J. M. Mahaffy, A. M. Segall, D. Mead, F. Azam, F. Rohwer, Genomic analysis of uncultured marine viral communities. Proc. Natl. Acad. Sci. U.S.A. 99, 14250–14255 (2002).
20. D. M. Kristensen, A. R. Mushegian, V. V. Dolja, E. V. Koonin, New dimensions of the virus world discovered through metagenomics. Trends Microbiol. 18, 11–19 (2010).
21. J.-F. Flot, H. Marie-Nelly, R. Koszul, Contact genomics: Scaffolding and phasing (meta) genomes using chromosome 3D physical signatures. FEBS Lett. 589 (20 Pt. A), 2966–2974 (2015).
22. C. Canchaya, G. Fournous, S. Chibani-Chennoufi, M. L. Dillmann, H. Brüssow, Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 6, 417–424 (2003).
23. A. Stern, E. Mick, I. Tirosh, O. Sagy, R. Sorek, CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome Res. 22, 1985–1994 (2012).
24. C. A. Suttle, Viruses in the sea. Nature 437, 356–361 (2005).
25. K. D. Seed, M. Yen, B. J. Shapiro, I. J. Hilaire, R. C. Charles, J. E. Teng, Evolutionary consequences of intra-patient phage predation on microbial populations. eLife 3, e03497 (2014)
26. B. M. Davis, M. K. Waldor, Filamentous phages linked to virulence of Vibrio cholerae. Curr. Opin. Microbiol. 6, 35–42 (2003).
27. S. L. Welkos, R. K. Holmes, Regulation of toxinogenesis in Corynebacterium diphtheriae. I. Mutations in bacteriophage b that alter the effects of iron on toxin production. J. Virol. 37, 936–945 (1981).
28. B. E. Dutilh, N. Cassman, K. McNair, S. E. Sanchez, G. G. Z. Silva, L. Boling, J. J. Barr, D. R. Speth, V. Seguritan, R. K. Aziz, B. Felts, E. A. Dinsdale, J. L. Mokili, R. A. Edwards, A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes. Nat. Commun. 5, 4498 (2014).
29. R. A. Edwards, K. McNair, K. Faust, J. Raes, B. E. Dutilh, Computational approaches to predict bacteriophage–host relationships. FEMS Microbiol. Rev. 40, 258–272 (2015).
30. H. Marie-Nelly, M. Marbouty, A. Cournac, J.-F. Flot, G. Liti, D. P. Parodi, S. Syan, N. Guillén, A. Margeot, C. Zimmer, R. Koszul, High-quality genome (re)assembly using chromosomal contact data. Nat. Commun. 5, 5695 (2014).
31. N. Kaplan, J. Dekker, High-throughput genome scaffolding from in vivo DNA interaction frequency. Nat. Biotechnol. 31, 1143–1147 (2013).
32. C. W. Beitel, L. Froenicke, J. M. Lang, I. F. Korf, R. W. Michelmore, J. A. Eisen, A. E. Darling, Strain- and plasmid-level deconvolution of a synthetic metagenome by sequencing proximity ligation products. PeerJ 2, e415 (2014).
33. J. N. Burton, I. Liachko, M. J. Dunham, J. Shendure, Species-level deconvolution of metagenome assemblies with Hi-C–based contact probability maps. G3 4, 1339–1346 (2014).
34. M. Marbouty, A. Cournac, J.-F. Flot, H. Marie-Nelly, J. Mozziconacci, R. Koszul, Metagenomic chromosome conformation capture (meta3C) unveils the diversity of chromosome organization in microorganisms. eLife 3, e03318 (2014).
35. M. Marbouty, R. Koszul, Metagenome analysis exploiting high-throughput chromosome conformation capture (3C) data. Trends Genet. 31, 673–682 (2015).
36. J. Dekker, K. Rippe, M. Dekker, N. Kleckner, Capturing chromosome conformation. Science 295, 1306–1311 (2002).
37. V. V. Mesyanzhinov, J. Robben, B. Grymonprez, V. A. Kostyuchenko, M. V. Bourkaltseva, N. N. Sykilinda, V. N. Krylov, G. Volckaert, The genome of bacteriophage ϕKZ of Pseudomonas aeruginosa. J. Mol. Biol. 317, 1–19 (2002).
38. A. Cornelissen, S. C. Hardies, O. V. Shaburova, V. N. Krylov, W. Mattheus, A. M. Kropinski, Complete genome sequence of the giant virus OBP and comparative genome analysis of the diverse fKZ-related phages. J. Virol. 86, 1844–1852 (2012).
39. A. S. Waller, T. Yamada, D. M. Kristensen, J. R. Kultima, S. Sunagawa, E. V. Koonin, P. Bork, Classification and quantification of bacteriophage taxa in human gut metagenomes. ISME J. 8, 1391–1402 (2014).
40. Y. Peng, H. C. M. Leung, S. M. Yiu, F. Y. L. Chin, IDBA-UD: A de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420–1428 (2012).
41. W. Zhu, A. Lomsadze, M. Borodovsky, Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 38, e132 (2010).
42. F. Meyer, D. Paarmann, M. D’Souza, R. Olson, E. M. Glass, M. Kubal, T. Paczian, A. Rodriguez, R. Stevens, A. Wilke, J. Wilkening, R. A. Edwards, The metagenomics RAST server—A public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9, 386 (2008).
43. L. Xiao, Q. Feng, S. Liang, S. B. Sonne, Z. Xia, X. Qiu, X. Li, H. Long, J. Zhang, D. Zhang, C. Liu, Z. Fang, J. Chou, J. Glanville, Q. Hao, D. Kotowska, C. Colding, T. R. Licht, D. Wu, J. Yu, J. J. Y. Sung, Q. Liang, J. Li, H. Jia, Z. Lan, V. Tremaroli, P. Dworzynski, H. B. Nielsen, F. Bäckhed, J. Doré, E. Le Chatelier, S. D. Ehrlich, J. C. Lin, M. Arumugam, J. Wang, L. Madsen, K. Kristiansen, A catalog of the mouse gut metagenome. Nat. Biotechnol. 33, 1103–1108 (2015).
44. D. E. Wood, S. L. Salzberg, Kraken: Ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 15, R46 (2014).
45. S. Roux, F. Enault, B. L. Hurwitz, M. B. Sullivan, VirSorter: Mining viral signal from microbial genomic data. PeerJ 3, e985 (2015).
46. J. Guglielmini, B. Néron, S. S. Abby, M. P. Garcillán-Barcia, F. de la Cruz, E. P. C. Rocha, Key components of the eight classes of type IV secretion systems involved in bacterial conjugation or protein secretion. Nucleic Acids Res. 42, 5715–5727 (2014).
47. V. D. Blondel, J.-L. Guillaume, R. Lambiotte, E. Lefebvre, Fast unfolding of communities in large networks. J. Stat. Mech. Theory Exp. 2008, P10008 (2008).
48. M. Albertsen, P. Hugenholtz, A. Skarshewski, K. L. Nielsen, G. W. Tyson, P. H. Nielsen, Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31, 533–538 (2013).
49. D. H. Parks, M. Imelfort, C. T. Skennerton, P. Hugenholtz, G. W. Tyson, CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).
50. J. Guglielmini, L. Quintais, M. P. Garcillán-Barcia, F. de la Cruz, E. P. C. Rocha, The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLOS Genet. 7, e1002222 (2011).
51. J. M. Lang, A. E. Darling, J. A. Eisen, Phylogeny of bacterial and archaeal genomes using conserved genes: Supertrees and supermatrices. PLOS ONE 8, e62510 (2013).
52. M. A. Umbarger, E. Toro, M. A. Wright, G. J. Porreca, D. Baù, S.-H. Hong, M. J. Fero, L. J. Zhu, M. A. Marti-Renom, H. H. McAdams, L. Shapiro, J. Dekker, G. M. Church, The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol. Cell 44, 252–264 (2011).
53. M. Marbouty, A. Le Gall, D. I. Cattoni, A. Cournac, A. Koh, J.-B. Fiche, J. Mozziconacci, H. Murray, R. Koszul, M. Nollmann, Condensin- and replication-mediated bacterial chromosome folding and origin condensation revealed by Hi-C and super-resolution imaging. Mol. Cell 59, 588–602 (2015).
54. M.-E. Val, M. Marbouty, F. de Lemos Martins, S. P. Kennedy, H. Kemble, M. J. Bland, C. Possoz, R. Koszul, O. Skovgaard, D. Mazel, A checkpoint control orchestrates the replication of the two chromosomes of Vibrio cholerae. Sci. Adv. 2, e1501914 (2016).
55. X. Wang, T. B. K. Le, B. R. Lajoie, J. Dekker, M. T. Laub, D. Z. Rudner, Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis. Genes Dev. 29, 1661–1675 (2015).
56. D. Arndt, J. R. Grant, A. Marcu, T. Sajed, A. Pon, Y. Liang, D. S. Wishart, PHASTER: A better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44, W16–W21 (2016).
57. D. M. Kristensen, X. Cai, A. Mushegian, Evolutionarily conserved orthologous families in phages are relatively rare in their prokaryotic hosts. J. Bacteriol. 193, 1806–1814 (2011).
58. D. M. Kristensen, A. S. Waller, T. Yamada, P. Bork, A. R. Mushegian, E. V. Koonin, Orthologous gene clusters and taxon signature genes for viruses of prokaryotes. J. Bacteriol. 195, 941–950 (2013).
59. S. Akhter, R. K. Aziz, R. A. Edwards, PhiSpy: A novel algorithm for finding prophages in bacterial genomes that combines similarity- and composition-based strategies. Nucleic Acids Res. 40, e126 (2012).
60. C. O. Flores, J. R. Meyer, S. Valverde, L. Farr, J. S. Weitz, Statistical structure of host–phage interactions. Proc. Natl. Acad. Sci. U.S.A. 108, E288–E297 (2011).
61. N. A. Bokulich, S. Subramanian, J. J. Faith, D. Gevers, J. I. Gordon, R. Knight, D. A. Mills, J. G. Caporaso, Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57–59 (2013).
62. S. R. Eddy, A new generation of homology search tools based on probabilistic inference. Genome Inform. 23, 205–211 (2009).
63. K. Rippe, Making contacts on a nucleic acid polymer. Trends Biochem. Sci. 26, 733–740 (2001).
64. R. Overbeek, R. Olson, G. D. Pusch, G. J. Olsen, J. J. Davis, T. Disz, R. A. Edwards, S. Gerdes, B. Parrello, M. Shukla, V. Vonstein, A. R. Wattam, F. Xia, R. Stevens, The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42, D206–D214 (2014).