Virome assembly and annotation: A surprise in the namib desert

Frontiers in Microbiology

Volumn 8, Issue JAN, 2017, Pages

  Hesse, Uljana ^a   Heusden, Peter van ^a   Kirby, Bronwyn M ^a   Olonade, Israel ^a   van Zyl, Leonardo J ^a   Trindade, Marla ^a  

^a UNIVERSITY OF THE WESTERN CAPE   (South Africa)

Author keywords

Annotation; Assembly; Circovirus; Namib Desert; Simulated virtual metagenomes; Virome

Indexed keywords

ATLANTIC OCEAN; CIRCOVIRUS; DATA ANALYSIS SOFTWARE; DESERT; DNA FLANKING REGION; FILTRATION; HABITAT; METAGENOME; NONHUMAN; PHYLOGENY; SIMULATION; VIRUS GENOME;

EID: 85011990330     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.00013     Document Type: Article

References (86)

1. Ackermann, H.-W. (2009). "Basic phage electron microscopy, "in Bacteriophages: Methods and Protocols, eds M. R. J. Clokie and A. M. Kropinski (New York, NY: Humana Press), 113-126.
2. Adriaenssens, E. M., Van Zyl, L. J., Cowan, D. A., and Trindade, M. I. (2016). Metaviromics of Namib desert salt pans: a novel lineage of haloarchaeal salterproviruses and a rich source of ssDNA viruses. Viruses 8:14. doi: 10.3390/v8010014
3. Adriaenssens, E. M., Van Zyl, L., De Maayer, P., Rubagotti, E., Rybicki, E., Tuffin, M., et al. (2015). Metagenomic analysis of the viral community in Namib Desert hypoliths. Environ. Microbiol. 17, 480-495. doi: 10.1111/1462-2920.12528
4. Baker, G. C., Smith, J. J., and Cowan, D. A. (2003). Review and re-analysis of domain-specific 16S primers. J. Microbiol. Methods 55, 541-555. doi: 10.1016/j.mimet.2003.08.009
5. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-477. doi: 10.1089/cmb.2012.0021
6. Boisvert, S., Raymond, F., Godzaridis, é., Laviolette, F., and Corbeil, J. (2012). RayMeta: scalable de novo metagenome assembly and profiling. Genome Biol. 13:R122. doi: 10.1186/gb-2012-13-12-r122
7. Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., et al. (2009). BLAST+: architecture and applications. BMC Bioinformatics 10:421. doi: 10.1186/1471-2105-10-421
8. Carlos, C., Castro, D. B. A., and Ottoboni, L. M. M. (2014). Comparative metagenomic analysis of coral microbial communities using a reference-independent approach. PLoS ONE 9:e111626. doi: 10.1371/journal.pone.0111626
9. Carvalhais, L. C., Dennis, P. G., Tyson, G. W., and Schenk, P. M. (2012). Application of metatranscriptomics to soil environments. J. Microbiol. Methods 91, 246-251. doi: 10.1016/j.mimet.2012.08.011
10. Clark, S. C., Egan, R., Frazier, P. I., and Wang, Z. (2013). ALE: a generic assembly likelihood evaluation framework for assessing the accuracy of genome and metagenome assemblies. Bioinformatics 29, 435-443. doi: 10.1093/bioinformatics/bts723
11. Crecchio, C., and Stotzky, G. (1998). Binding of DNA on humic acids: effect on transformation of Bacillus subtilis and resistance to DNase. Soil Biol. Biochem. 30, 1061-1067. doi: 10.1016/S0038-0717(97)00248-4
12. Dayaram, A., Goldstien, S., Argüello-Astorga, G. R., Zawar-Reza, P., Gomez, C., Harding, J. S., et al. (2015). Diverse small circular DNA viruses circulating amongst estuarine molluscs. Infect. Genet. Evol. 31, 284-295. doi: 10.1016/j.meegid.2015.02.010
13. de Cárcer, D. A., Angly, F. E., and Alcamí, A. (2014). Evaluation of viral genome assembly and diversity estimation in deep metagenomes. BMC Genomics 15:989. doi: 10.1186/1471-2164-15-989
14. Dopson, M., Baker-Austin, C., Koppineedi, P. R., and Bond, P. L. (2003). Growth in sulphidic mineral environments: metal resistance mechanisms in acidophilic micro-organisms. Microbiology 149, 1959-1970. doi: 10.1099/mic.0.26296-0
15. Džunková, M., D'Auria, G., and Moya, A. (2015). Direct sequencing of human gut virome fractions obtained by flow cytometry. Front. Microbiol. 6:955. doi: 10.3389/fmicb.2015.00955
16. Eckardt, F. D., Livingstone, I., Seely, M., and von Holdt, J. (2013b). The surface geology and geomorphology around Gobabeb, Namib Desert, Namibia. Geogr. Ann. Ser. A 95, 271-284. doi: 10.1111/geoa.12028
17. Eckardt, F. D., Soderberg, K., Coop, L. J., Muller, A. A., Vickery, K. J., Grandin, R. D., et al. (2013a). The nature of moisture at Gobabeb, in the central Namib Desert. J. Arid Environ. 93, 7-19. doi: 10.1016/j.jaridenv.2012.01.011
18. Efrony, R., Atad, I., and Rosenberg, E. (2009). Phage therapy of coral white plague disease: properties of phage BA3. Curr. Microbiol. 58, 139-145. doi: 10.1007/s00284-008-9290-x
19. Enault, F., Briet, A., Bouteille, L., Roux, S., Sullivan, M. B., and Petit, M. A. (2017). Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analysis. ISME J. 11, 237-247. doi: 10.1038/ismej.2016.90
20. Fenner, N., and Freeman, C. (2011). Drought-induced carbon loss in peatlands. Nat. Geosci. 4, 895-900. doi: 10.1038/ngeo1323
21. Fierer, N., Breitbart, M., Nulton, J., Salamon, P., Lozupone, C., Jones, R., et al. (2007). Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl. Environ. Microbiol. 73, 7059-7066. doi: 10.1128/AEM.00358-07
22. Fuhrman, J. A. (1999). Marine viruses and their biogeochemical and ecological effects. Nature 399, 541-548. doi: 10.1038/21119
23. García-López, R., Vázquez-Castellanos, J. F., and Moya, A. (2015). Fragmentation and coverage variation in viral metagenome assemblies, and their effect in diversity calculations. Front. Bioeng. Biotechnol. 3:141. doi: 10.3389/fbioe.2015.00141
24. Ge, X., Li, J., Peng, C., Wu, L., Yang, X., Wu, Y., et al. (2011). Genetic diversity of novel circular ssDNA viruses in bats in China. J. Gen. Virol. 92, 2646-2653. doi: 10.1099/vir.0.034108-0
25. Goudie, A. (2010). "Namib Sand Sea: large dunes in an ancient desert, "in Geomorphological Landscapes of the World, ed P. Migon (New York, NY: Springer), 163-169.
26. Grande, R., Di Giulio, M., Bessa, L. J., Di Campli, E., Baffoni, M., Guarnieri, S., et al. (2011). Extracellular DNA in Helicobacter pylori biofilm: a backstairs rumour. J. Appl. Microbiol. 110, 490-498. doi: 10.1111/j.1365-2672.2010.04911.x
27. Grande, R., Nistico, L., Sambanthamoorthy, K., Longwell, M., Iannitelli, A., Cellini, L., et al. (2014). Temporal expression of agrB, cidA, and alsS in the early development of Staphylococcus aureus UAMS-1 biofilm formation and structural role of extracellular DNA and carbohydrates. Pathog. Dis. 70, 414-422. doi: 10.1111/2049-632X.12158
28. Hannigan, G. D., Meisel, J. S., Tyldsley, A. S., Zheng, Q., Hodkinson, B. P., SanMiguel, A. J., et al. (2015). The human skin double-stranded DNA virome: topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome. MBio 6:e01578-15. doi: 10.1128/mBio.01578-15
29. Hansen, M. C., Tolker-Nelson, T., Givskov, M., and Molin, S. (1998). Biased 16S rDNA PCR amplification caused by interference from DNA flanking template region. FEMS Microbiol. Ecol. 15, 25-36. doi: 10.1111/j.1574-6941.1998.tb00500.x
30. Hatfull, G. F. (2008). Bacteriophage genomics. Curr. Opin. Microbiol. 11, 447-453. doi: 10.1016/j.mib.2008.09.004
31. Hosoya, S., Adachi, K., and Kasai, H. (2009). Thalassomonas actiniarum sp. nov. and Thalassomonas haliotis sp. nov., isolated from marine animals. Int. J. Syst. Evol. Microbiol. 59, 686-690. doi: 10.1099/ijs.0.000539-0
32. Hurwitz, B. L., U'Ren, L. M., and Youens-Clark, K. (2016). Computational prospecting the great viral unknown. FEMS Microbiol. Lett. 363, 1-12. doi: 10.1093/femsle/fnw077
33. Huson, D. H., Auch, A. F., Qi, J., and Schuster, S. C. (2007). MEGAN analysis of metagenomic data. Genome Res. 17, 377-386. doi: 10.1101/gr.5969107
34. Jean, W. D., Shieh, W. Y., and Liu, T. Y. (2006). Thalassomonas agarivorans sp. nov., a marine agarolytic bacterium isolated from shallow coastal water of An-Ping Harbour, Taiwan, and emended description of the genus Thalassomonas. Int. J. Syst. Evol. Microbiol. 56, 1245-1250. doi: 10.1099/ijs.0.64130-0
35. Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. doi: 10.1093/molbev/mst010
36. Kim, K. H., and Bae, J. W. (2011). Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl. Environ. Microbiol. 77, 7663-7668. doi: 10.1128/AEM.00289-11
37. Kimura, M., Jia, Z., Nakayama, N., and Asakawa, S. (2008). Ecology of viruses in soils: past, present and future perspectives. Soil Sci. Plant Nutr. 54, 1-32. doi: 10.1111/j.1747-0765.2007.00197.x
38. Kraberger, S., Argüello-Astorga, G. R., Greenfield, L. G., Galilee, C., Law, D., Martin, D. P., et al. (2015). Characterisation of a diverse range of circular replication-associated protein encoding DNA viruses recovered from a sewage treatment oxidation pond. Infect. Genet. Evol. 31, 73-86. doi: 10.1016/j.meegid.2015.01.001
39. Kurtz, S., Phillippy, A., Delcher, A. L., Smoot, M., Shumway, M., Antonescu, C., et al. (2004). Versatile and open software for comparing large genomes. Genome Biol. 5:R12. doi: 10.1186/gb-2004-5-2-r12
40. Krupovic, M. (2013). Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr. Opin. Virol. 3, 578-586. doi: 10.1016/j.coviro.2013.06.010
41. Labonté, J. M., and Suttle, C. A. (2013). Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J. 7, 2169-2177. doi: 10.1038/ismej.2013.110
42. Laffy, P. W., Wood-Charlson, E. M., Turaev, D., Weynberg, K. D., Botté, E. S., van Oppen, M. J. H., et al. (2016). HoloVir: a workflow for investigating the diversity and function of viruses in invertebrate holobionts. Front. Microbiol. 7:822. doi: 10.3389/fmicb.2016.00822
43. Langmead, B., and Salzberg, S. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359. doi: 10.1038/nmeth.1923
44. Letunic, I., and Bork, P. (2007). Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127-128. doi: 10.1093/bioinformatics/btl529
45. Lorenzi, H. A., Hoover, J., Inman, J., Safford, T., Murphy, S., Kagan, L., et al. (2011). The Viral MetaGenome Annotation Pipeline (VMGAP): an automated tool for the functional annotation of viral Metagenomic shotgun sequencing data. Stand. Genomic. Sci. 4, 418-429. doi: 10.4056/sigs.1694706
46. Lusk, R. W. (2014). Diverse and widespread contamination evident in the unmapped depths of high throughput sequencing data. PLoS ONE 9:e110808. doi: 10.1371/journal.pone.0110808
47. Makhalanyane, T. P. (2015). Microbial ecology of hot desert edaphic systems. FEMS Microbiol. Rev. 39, 203-221. doi: 10.1093/femsre/fuu011
48. Mao, D. Q., Luo, Y., Mathieu, J., Wang, Q., Feng, L., Mu, Q. H., et al. (2014). Persistence of extracellular DNA in river sediment facilitates antibiotic resistance gene propagation. Environ. Sci. Technol. 48, 71-78. doi: 10.1021/es404280v
49. Meyer, F., Paarmann, D., D'Souza, M., Olson, R., Glass, E. M., Kubal, M., et al. (2008). The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. doi: 10.1186/1471-2105-9-386
50. McDaniel, L. D., Rosario, K., Breitbart, M., and Paul, J. H. (2014). Comparative metagenomics: natural populations of induced prophages demonstrate highly unique, lower diversity viral sequences. Environ. Microbiol. 16, 570-585. doi: 10.1111/1462-2920.12184
51. Minot, S., Bryson, A., Chehoud, C., Wu, G. D., Lewis, J. D., and Bushman, F. D. (2013). Rapid evolution of the human gut virome. Proc. Natl. Acad. Sci. U.S.A. 110, 12450-12455. doi: 10.1073/pnas.1300833110
52. Mohiuddin, M., and Schellhorn, H. E. (2015). Spatial and temporal dynamics of virus occurrence in two freshwater lakes captured through metagenomic analysis. Front. Microbiol. 6:960. doi: 10.3389/fmicb.2015.00960
53. Nguyen, T. H., Chen, K. L., and Elimelech, M. (2010). Adsorption kinetics and reversibility of linear plasmid DNA on silica surfaces: influence of alkaline earth and transition metal ions. Biomacromolecules 11, 1225-1230. doi: 10.1021/bm901427n
54. Nicholson, S. (2011). Dryland Climatology. New York, NY: Cambridge University Press.
55. Peng, Y., Leung, H. C., Yiu, S. M., and Chin, F. Y. (2011). Meta-IDBA: a de novo assembler for metagenomic data. Bioinformatics 27, 94-101. doi: 10.1093/bioinformatics/btr216
56. Peng, Y., Leung, H. C., Yiu, S. M., and Chin, F. Y. (2012). IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28, 1420-1428. doi: 10.1093/bioinformatics/bts174
57. Pointing, S. B., and Belnap, J. (2012). Microbial colonization and controls in dryland systems. Nat. Rev. Microbiol. 10, 551-562. doi: 10.1038/nrmicro2831
58. Prestel, E., Regeard, C., Andrews, J., Oger, P., and DuBow, M. S. (2012). A novel bacteriophage morphotype with a ribbon-like structure at the tail extremity. Res. J. Microbiol. 7, 75-81. doi: 10.3923/jm.2012.75.81
59. Prestel, E., Salamitou, S., and DuBow, M. S. (2008). An examination of the bacteriophages and bacteria of the Namib Desert. J. Microbiol. 46, 364-372. doi: 10.1007/s12275-008-0007-4
60. Prigent, M., Leroy, M., Confalonieri, F., Dutertre, M., and DuBow, M. S. (2005). A diversity of bacteriophage forms and genomes can be isolated from the surface sands of the Sahara Desert. Extremophiles 9, 289-296. doi: 10.1007/s00792-005-0444-5
61. Rambaut, A. (2008). FigTree v1.1.1: Tree Figure Drawing Tool. Available online at: http://tree.bio.ed.ac.uk/software/figtree/
62. Rawlings, D. E. (2005). Characteristics and adaptability of iron-and sulphur-oxidizing microorganisms used for the recovery of metals from minerals and their concentrates. Microb. Cell Fact. 4:13. doi: 10.1186/1475-2859-4-13
63. Richter, D. C., Ott, F., Auch, A. F., Schmid, R., and Huson, D. H. (2008). MetaSim: a sequencing simulator for genomics and metagenomics. PLoS ONE 3:e3373. doi: 10.1371/journal.pone.0003373
64. Rosario, K., Schenck, R. O., Harbeitner, R. C., Lawler, S. N., and Breitbart, M. (2015). Novel circular single-stranded DNA viruses identified in marine invertebrates reveal high sequence diversity and consistent predicted intrinsic disorder patterns within putative structural proteins. Front. Microbiol. 6:696. doi: 10.3389/fmicb.2015.00696
65. Roux, S., Enault, F., Hurwitz, B. L., and Sullivan, M. B. (2015). VirSorter: mining viral signal from microbial genomic data. PeerJ 3:e985. doi: 10.7717/peerj.985
66. Roux, S., Faubladier, M., Mahul, A., Paulhe, N., Bernard, A., Debroas, D., et al. (2011). MetaVir: a web server dedicated to virome analysis. Bioinformatics 27, 3074-3075. doi: 10.1093/bioinformatics/btr519
67. Roux, S., Krupovic, M., Debroas, D., Forterre, P., and Enault, F. (2013). Assessment of viral community functional potential from viral metagenomes may be hampered by contamination with cellular sequences. Open Biol. 3:130160. doi: 10.1098/rsob.130160
68. Schmieder, R., and Edwards, R. (2011). Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS ONE 6:e17288. doi: 10.1371/journal.pone.0017288
69. Simpson, J. T., Wong, K., Jackman, S. D., Schein, J. E., Jones, S. J., and Birol, I. (2009). ABySS: a parallel assembler for short read sequence data. Genome Res. 19, 1117-1123. doi: 10.1101/gr.089532.108
70. Solonenko, S. A., and Sullivan, M. B. (2013). Preparation of metagenomic libraries from naturally occurring marine viruses. Methods Enzymol. 531, 143-165. doi: 10.1016/B978-0-12-407863-5.00008-3
71. Stadelmann, B., Herrera, L. G., Arroyo-Cabrales, J., Flores-Martinez, J. J., May, B. P., and Ruedi, M. (2004). Molecular systematics of the fishing bat Myotis (Pizonyx) vivesi. J. Mammal. 85, 133-139. doi: 10.1644/1545-1542(2004)085<0133:MSOTFB>2.0.CO;2
72. Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57, 758-771. doi: 10.1080/10635150802429642
73. Sullivan, M. J., Petty, N. K., and Beatson, S. A. (2011). Easyfig: a genome comparison visualizer. Bioinformatics 27, 1009-1010. doi: 10.1093/bioinformatics/btr039
74. Tangherlini, M., Dell'Anno, A., Allen, L. Z., Riccioni, G., and Corinaldesi, C. (2016). Assessing viral taxonomic composition in benthic marine ecosystems: reliability and efficiency of different bioinformatic tools for viral metagenomic analyses. Sci. Rep. 6:28428. doi: 10.1038/srep28428
75. Thompson, F. L., Barash, Y., Sawabe, T., Sharon, G., Swings, J., and Rosenberg, E. (2006). Thalassomonas loyana sp. nov., a causative agent of the white plague-like disease of corals on the Eilat coral reef. Int. J. Syst. Evol. Microbiol. 56, 365-368. doi: 10.1099/ijs.0.63800-0
76. Tveit, A. T., Urich, T., and Svenning, M. M. (2014). Metatranscriptomic analysis of artic peat soil microbiota. Appl. Environ. Microbiol. 80, 5761-5772. doi: 10.1128/AEM.01030-14
77. van Dijk, E. L., Jaszczyszyn, Y., and Thermes, C. (2014). Library preparation methods for next-generation sequencing: tone down the bias. Exp. Cell Res. 322, 12-20. doi: 10.1016/j.yexcr.2014.01.008
78. Vázquez-Castellanos, J. F., García-López, R., Pérez-Brocal, V., Pignatelli, M., and Moya, A. (2014). Comparison of different assembly and annotation tools on analysis of simulated viral metagenomic communities in the gut. BMC Genomics 15:37. doi: 10.1186/1471-2164-15-37
79. Vikram, S., Guerrero, L. D., Makhalanyane, T. P., Le, P. T., Seely, M., and Cowan, D. A. (2015). Metagenomic analysis provides insights into functional capacity in a hyperarid desert soil niche community. Environ. Microbiol. 18, 1875-1888. doi: 10.1111/1462-2920.13088
80. Weynberg, K. D., Wood-Charlson, E. M., Suttle, C. A., and van Oppen, M. J. (2014). Generating viral metagenomes from the coral holobiont. Front. Microbiol. 5:206. doi: 10.3389/fmicb.2014.00206
81. Wright, I. A., and Travers, S. A. (2014). RAMICS: trainable, high-speed and biologically relevant alignment of high-throughput sequencing reads to coding DNA. Nucl Acids Res. 42:e106. doi: 10.1093/nar/gku473
82. Wommack, K. E., Bhavsar, J., Polson, S. W., Chen, J., Dumas, M., Srinivasiah, S., et al. (2012). VIROME: a standard operating procedure for analysis of viral metagenome sequences. Stand. Genomic. Sci. 6, 427-439. doi: 10.4056/sigs.2945050
83. Yi, H., Bae, K. S., and Chun, J. (2004). Thalassomonas ganghwensis sp. nov., isolated from tidal flat sediment. Int. J. Syst. Evol. Microbiol. 54, 377-380. doi: 10.1099/ijs.0.02748-0
84. Yuan, S., Cohen, D. B., Ravel, J., Abdo, Z., and Forney, L. J. (2012). Evaluation of methods for the extraction and purification of DNA from the human microbiome. PLoS ONE 7:e33865. doi: 10.1371/journal.pone.0033865
85. Zablocki, O., Adriaenssens, E. M., and Cowan, D. (2016). Diversity and ecology of viruses in hyperarid desert soils. Appl. Environ. Microbiol. 82, 770-777. doi: 10.1128/AEM.02651-15
86. Zablocki, O., van Zyl, L., Adriaenssens, E. M., Rubagotti, E., Tuffin, M., Cary, S. C., et al. (2014). High-level diversity of tailed Phages, eukaryote-associated viruses, and virophage-like elements in the metaviromes of Antarctic soils. Appl. Environ. Microbiol. 80, 6888-6897. doi: 10.1128/AEM.01525-14