Metaviromics of Namib desert salt pans: A novel lineage of haloarchaeal salterproviruses and a rich source of ssDNA viruses

Viruses

Volumn 8, Issue 1, 2016, Pages

  Adriaenssens, Evelien M ^a   van Zyl, Leonardo Joaquim ^b   Cowan, Don A ^a   Trindade, Marla I ^b  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b UNIVERSITY OF THE WESTERN CAPE   (South Africa)

Author keywords

Environmental viromics; Gokushovirinae; Haloarchaeal viruses; Hypersaline; Metaviromics; Microviridae; Namib desert playa; SsDNA viruses

Indexed keywords

CONTIG; DOUBLE STRANDED DNA; SINGLE STRANDED DNA; DNA VIRUS; SODIUM CHLORIDE; VIRUS DNA;

ACIDIANUS; ANALYTICAL PARAMETERS; ARTICLE; CIRCOVIRIDAE; DESERT; DNA LIBRARY; DNA PURIFICATION; DNA SEQUENCE; ELECTRIC CONDUCTIVITY; FUSELLOVIRIDAE; GENE AMPLIFICATION; GENE MAPPING; GENETIC ANALYSIS; GOKUSHOVIRINAE; HALOARCHAEAL SALTERPROVIRUS; INOVIRIDAE; LYSOGENIZATION; MICROVIRIDAE; MIMIVIRIDAE; NONHUMAN; NUDIVIRIDAE; POLYMERASE CHAIN REACTION; PROVIRUS; RUDIVIRIDAE; SALINITY; SINGLE-STRANDED DNA VIRUS; SULFOLOBUS; TOTAL DISSOLVED SOLID; VIRUS CAPSID; VIRUS GENOME; ARCHAEAL VIRUS; CLASSIFICATION; DESERT CLIMATE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; NAMIBIA; PHYLOGENY;

ARCHAEAL VIRUSES; DESERT CLIMATE; DNA VIRUSES; DNA, SINGLE-STRANDED; DNA, VIRAL; GENOME, VIRAL; MOLECULAR SEQUENCE DATA; NAMIBIA; PHYLOGENY; SODIUM CHLORIDE;

EID: 84954416338     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v8010014     Document Type: Article

References (80)

1. Rodriguez-Brito, B.; Li, L.; Wegley, L.; Furlan, M.; Angly, F.; Breitbart, M.; Buchanan, J.; Desnues, C.; Dinsdale, E.; Edwards, R.; et al. Viral and microbial community dynamics in four aquatic environments. ISME J. 2010, 4, 739-751. [CrossRef] [PubMed]
2. Baxter, B.K.; Mangalea, M.R.; Willcox, S.; Sabet, S.; Nagoulat, M.-N.; Griffith, J.D. Haloviruses of Great Salt Lake: A model for understanding viral diversity. In Halophiles and Hypersaline Environments; Ventosa, A., Oren, A., Ma, Y., Eds.; Springer: Berlin, Germany, 2011; pp. 173-190.
3. Boujelben, I.; Yarza, P.; Almansa, C.; Villamor, J.; Maalej, S.; Antón, J.; Santos, F. Virioplankton community structure in Tunisian solar salterns. Appl. Environ. Microbiol. 2012, 78, 7429-7437. [CrossRef] [PubMed]
4. Santos, F.; Yarza, P.; Parro, V.; Briones, C.; Anton, J. The metavirome of a hypersaline environment. Environ. Microbiol. 2010, 12, 2965-2976. [CrossRef] [PubMed]
5. Emerson, J.B.; Thomas, B.C.; Andrade, K.; Allen, E.E.; Heidelberg, K.B.; Banfield, J.F. Dynamic viral populations in hypersaline systems as revealed by metagenomic assembly. Appl. Environ. Microbiol. 2012, 78, 6309-6320. [CrossRef] [PubMed]
6. Emerson, J.B.; Thomas, B.C.; Andrade, K.; Heidelberg, K.B.; Banfield, J.F. New approaches indicate constant viral diversity despite shifts in assemblage structure in an Australian hypersaline lake. Appl. Environ. Microbiol. 2013, 79, 6754-6764. [CrossRef] [PubMed]
7. Breitbart, M. Marine Viruses: Truth or Dare. Ann. Rev. Mar. Sci. 2012, 4, 425-448. [CrossRef] [PubMed]
8. Arnold, H.P.; Zillig, W.; Ziese, U.; Holz, I.; Crosby, M.; Utterback, T.; Weidmann, J.F.; Kristjanson, J.K.; Klenk, H.P.; Nelson, K.E.; et al. A novel lipothrixvirus, SIFV, of the extremely thermophilic crenarchaeon Sulfolobus. Virology 2000, 267, 252-266. [CrossRef] [PubMed]
9. Chen, Y.; Wei, D.; Wang, Y.; Zhang, X. The role of interactions between bacterial chaperone, aspartate aminotransferase, and viral protein during virus infection in high temperature environment: The interactions between bacterium and virus proteins. BMC Microbiol. 2013, 13, 48. [CrossRef] [PubMed]
10. Jin, M.; Ye, T.; Zhang, X. Roles of bacteriophage GVE2 endolysin in host lysis at high temperatures. Microbiology 2013, 159, 1597-1605. [CrossRef] [PubMed]
11. Moser, M.J.; DiFrancesco, R.A.; Gowda, K.; Klingele, A.J.; Sugar, D.R.; Stocki, S.; Mead, D.A.; Schoenfeld, T.W. Thermostable DNA polymerase from a viral metagenome is a potent RT-PCR enzyme. PLoS ONE 2012, 7, e38371. [CrossRef] [PubMed]
12. Plotka, M.; Kaczorowska, A.K.; Stefanska, A.; Morzywolek, A.; Fridjonsson, O.H.; Dunin-Horkawicz, S.; Kozlowski, L.; Hreggvidsson, G.O.; Kristjansson, J.K.; Dabrowski, S.; et al. Novel highly thermostable endolysin from Thermus scotoductus MAT2119 bacteriophage Ph2119 with amino acid sequence similarity to eukaryotic peptidoglycan recognition proteins. Appl. Environ. Microbiol. 2014, 80, 886-895. [CrossRef] [PubMed]
13. Sevostyanova, A.; Djordjevic, M.; Kuznedelov, K.; Naryshkina, T.; Gelfand, M.S.; Severinov, K.; Minakhin, L. Temporal regulation of viral transcription during development of Thermus thermophilus bacteriophage 'YS40. J. Mol. Biol. 2007, 366, 420-435. [CrossRef] [PubMed]
14. Liu, B.; Zhang, X. Deep-sea thermophilic Geobacillus bacteriophage GVE2 transcriptional profile and proteomic characterization of virions. Appl. Microbiol. Biotechnol. 2008, 80, 697-707. [CrossRef] [PubMed]
15. Payet, J.; Suttle, C.A. To kill or not to kill: The balance between lytic and lysogenic viral infection is driven by trophic status. Limnol. Oceanogr. 2013, 58, 465-474.
16. Rice, G.; Stedman, K.; Snyder, J.;Wiedenheft, B.;Willits, D.; Brumfield, S.; McDermott, T.; Young, M.J. Viruses from extreme thermal environments. Proc. Natl. Acad. Sci. USA 2001, 98, 13341-13345. [CrossRef] [PubMed]
17. Roine, E.; Oksanen, H.M. Viruses from the hypersaline environment. In Halophiles and Hypersaline Environments; Ventosa, A., Al, E., Eds.; Springer: Berlin, Germany, 2011; pp. 153-172.
18. Sime-Ngando, T.; Lucas, S.; Robin, A.; Tucker, K.P.; Colombet, J.; Bettarel, Y.; Desmond, E.; Gribaldo, S.; Forterre, P.; Breitbart, M.; et al. Diversity of virus-host systems in hypersaline Lake Retba, Senegal. Environ. Microbiol. 2011, 13, 1956-1972. [CrossRef] [PubMed]
19. Atanasova, N.S.; Roine, E.; Oren, A.; Bamford, D.H.; Oksanen, H.M. Global network of specific virus-host interactions in hypersaline environments. Environ. Microbiol. 2012, 14, 426-440. [CrossRef] [PubMed]
20. Brum, J.R.; Steward, G.F. Morphological characterization of viruses in the stratified water column of alkaline, hypersaline Mono Lake. Microb. Ecol. 2010, 60, 636-643. [CrossRef] [PubMed]
21. Senčilo, A.; Roine, E. A glimpse of the genomic diversity of haloarchaeal tailed viruses. Front. Microbiol. 2014, 5, 1-6.
22. Pietilä, M.K.; Roine, E.; Paulin, L.; Kalkkinen, N.; Bamford, D.H. An ssDNA virus infecting archaea: A new lineage of viruses with a membrane envelope. Mol. Microbiol. 2009, 72, 307-319. [CrossRef] [PubMed]
23. Roine, E.; Kukkaro, P.; Paulin, L.; Laurinavicius, S.; Domanska, A.; Somerharju, P.; Bamford, D.H. New, closely related haloarchaeal viral elements with different nucleic acid types. J. Virol. 2010, 84, 3682-3689. [CrossRef] [PubMed]
24. Senčilo, A.; Paulin, L.; Kellner, S.; Helm, M.; Roine, E. Related haloarchaeal pleomorphic viruses contain different genome types. Nucleic Acids Res. 2012, 40, 5523-5534. [CrossRef] [PubMed]
25. Santos, F.; Meyerdierks, A.; Peña, A.; Rosselló-Mora, R.; Amann, R.; Antón, J. Metagenomic approach to the study of halophages: The environmental halophage 1. Environ. Microbiol. 2007, 9, 1711-1723. [CrossRef] [PubMed]
26. Garcia-Heredia, I.; Martin-Cuadrado, A.B.; Mojica, F.J.M.; Santos, F.; Mira, A.; Antón, J.; Rodriguez-Valera, F. Reconstructing viral genomes from the environment using fosmid clones: The case of haloviruses. PLoS ONE 2012, 7, e33802. [CrossRef] [PubMed]
27. Prestel, E.; Regeard, C.; Andrews, J.; Oger, P.; DuBow, M.S. A novel bacteriophage morphotype with a ribbon-like structure at the tail extremity. Res. J. Microbiol. 2012, 7, 75-81.
28. Prestel, E.; Salamitou, S.; DuBow, M.S. An examination of the bacteriophages and bacteria of the Namib Desert. J. Microbiol. 2008, 46, 364-372. [CrossRef] [PubMed]
29. Adriaenssens, E.M.; van Zyl, L.; de Maayer, P.; Rubagotti, E.; Rybicki, E.; Tuffin, M.; Cowan, D.A. Metagenomic analysis of the viral community in Namib Desert hypoliths. Environ. Microbiol. 2015, 17, 480-495. [CrossRef] [PubMed]
30. Eckardt, F.D.; Drake, N.; Goudie, A.S.; White, K.; Viles, H. The role of playas in pedogenic gypsum crust formation in the Central Namib Desert: A theoretical model. Earth Surf. Process. Landf. 2001, 26, 1177-1193. [CrossRef]
31. Day, J.A.; Seely, M.K. Physical and chemical conditions in an hypersaline spring in the Namib Desert. Hydrobiologia 1988, 160, 141-153. [CrossRef]
32. Day, J.A. The major ion chemistry of some southern African saline systems. Hydrobiologia 1993, 267, 37-59. [CrossRef]
33. Eckardt, F.D.; Drake, N. Introducing the Namib Desert playas. In Sabkha Ecosystems; Öztürk, M., Böer, B., Barth, H.-J., Clüsener-Godt, M., Khan, M.A., Breckle, S.-W., Eds.; Springer Netherlands: Dordrecht, The Netherlands, 2011; Volume 46, pp. 19-25.
34. Eckardt, F.D.; Soderberg, K.; Coop, L.J.; Muller, A.A.; Vickery, K.J.; Grandin, R.D.; Jack, C.; Kapalanga, T.S.; Henschel, J. The nature of moisture at Gobabeb, in the central Namib Desert. J. Arid Environ. 2013, 93, 7-19. [CrossRef]
35. Capece, M.C.; Clark, E.; Saleh, J.K.; Halford, D.; Heinl, N.; Hoskins, S.; Rothschild, L.J. Polyextremophiles and the constraints for terrestrial habitability. In Polyextremophiles: Life under Multiple Forms of Stress; Seckbach, J., Oren, A., Stan-Lotter, H., Eds.; Springer Science + Business Media: Dordrecht, The Netherlands, 2013; pp. 7-59.
36. Schoenfeld, T.; Liles, M.;Wommack, K.E.; Polson, S.W.; Godiska, R.; Mead, D. Functional viral metagenomics and the next generation of molecular tools. Trends Microbiol. 2010, 18, 20-29. [CrossRef] [PubMed]
37. Schoenfeld, T.; Patterson, M.; Richardson, P.M.; Wommack, K.E.; Young, M.; Mead, D. Assembly of viral metagenomes from yellowstone hot springs. Appl. Environ. Microbiol. 2008, 74, 4164-4174. [CrossRef] [PubMed]
38. Andrews, S. FastQC: A quality control tool for high throughput sequence data. Available online: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (accessed on 9 March 2015).
39. Roux, S.; Faubladier, M.; Mahul, A.; Paulhe, N.; Bernard, A.; Debroas, D.; Enault, F. Metavir: A web server dedicated to virome analysis. Bioinformatics 2011, 27, 3074-3075. [CrossRef] [PubMed]
40. Roux, S.; Tournayre, J.; Mahul, A.; Debroas, D.; Enault, F. Metavir 2: New tools for viral metagenome comparison and assembled virome analysis. BMC Bioinform. 2014, 15, 76. [CrossRef] [PubMed]
41. Wommack, K.E.; Bhavsar, J.; Polson, S.W.; Chen, J.; Dumas, M.; Srinivasiah, S.; Furman, M.; Jamindar, S.; Nasko, D.J. VIROME: A standard operating procedure for analysis of viral metagenome sequences. Stand. Genomic Sci. 2012, 6, 427-439. [CrossRef] [PubMed]
42. Langmead, B.; Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 2012, 9, 357-359. [CrossRef] [PubMed]
43. Albertsen, M. Cytoscapeviz. Available online: http://www.github.com/MadsAlbertsen/multi-metagenome/ tree/master/cytoscapeviz (accessed on 15 August 2014).
44. Albertsen, M.; Hugenholtz, P.; Skarshewski, A.; Nielsen, K.L.; Tyson, G.W.; Nielsen, P.H. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 2013, 31, 533-538. [CrossRef] [PubMed]
45. Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.;Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13, 2498-2504. [CrossRef] [PubMed]
46. Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30, 2725-2729. [CrossRef] [PubMed]
47. Larkin, M.A.; Blackshields, G.; Brown, N.P.; Chenna, R.; McGettigan, P.A.; McWilliam, H.; Valentin, F.; Wallace, I.M.; Wilm, A.; Lopez, R.; et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23, 2947-2948. [CrossRef] [PubMed]
48. Jones, D.T.; Taylor, W.R.; Thornton, J.M. The rapid generation of mutation data matrices from protein sequences. Bioinformatics 1992, 8, 275-282. [CrossRef]
49. 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 2009, 25, 2078-2079. [CrossRef] [PubMed]
50. Noguchi, H.; Taniguchi, T.; Itoh, T. MetaGeneAnnotator: Detecting species-specific patterns of ribosomal binding site for precise gene prediction in anonymous prokaryotic and phage genomes. DNA Res. 2008, 15, 387-396. [CrossRef] [PubMed]
51. Noguchi, H.; Park, J.; Takagi, T. MetaGene: Prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res. 2006, 34, 5623-5630. [CrossRef] [PubMed]
52. The UniProt Consortium. The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Res. 2010, 38, D142-D148.
53. Metagenomes Online. Available online: http://www.metagenomesonline.org (accessed on 6 April 2015).
54. Marchler-Bauer, A.; Derbyshire, M.K.; Gonzales, N.R.; Lu, S.; Chitsaz, F.; Geer, L.Y.; Geer, R.C.; He, J.; Gwadz, M.; Hurwitz, D.I.; et al. CDD: NCBI's conserved domain database. Nucleic Acids Res. 2014, 43, D222-D226. [CrossRef] [PubMed]
55. Sullivan, M.J.; Petty, N.K.; Beatson, S.A. Easyfig: A genome comparison visualizer. Bioinformatics 2011, 27, 1009-1010. [CrossRef] [PubMed]
56. Swan, B.K.; Ehrhardt, C.J.; Reifel, K.M.; Moreno, L.I.; Valentine, D.L. Archaeal and bacterial communities respond differently to environmental gradients in anoxic sediments of a California hypersaline lake, the Salton Sea. Appl. Environ. Microbiol. 2010, 76, 757-768. [CrossRef] [PubMed]
57. Martínez-García, M.; Santos, F.; Moreno-Paz, M.; Parro, V.; Antón, J. Unveiling viral-host interactions within the "microbial dark matter". Nat. Commun. 2014, 5, 1-8. [CrossRef] [PubMed]
58. 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 2006, 7, 8. [CrossRef] [PubMed]
59. King, A.M.Q., Adams, M.J., Carstens, E.B., Lefkowitz, E.J., Eds.; Virus Taxonomy, 9th ed.; Elsevier Inc.: London, UK, 2012.
60. Labonté, J.M.; Suttle, C.A. Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J. 2013, 7, 2169-2177. [CrossRef] [PubMed]
61. Wearne, K.; Bridgeford, P. Coastal birds of the Namib-Naukluft Park. In Namib: Secrets of a Desert Uncovered; Seely, M., Pallett, J., Eds.; Venture Publications: Windhoek, Namibia, 2012; pp. 37-39.
62. Roberts, J.W.; Devoret, R. Lysogenic Induction. Cold Spring Harb. Monogr. Arch. 1983, 13, 123-144.
63. Kim, K.-H.; Bae, J.-W. Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl. Environ. Microbiol. 2011, 77, 7663-7668. [CrossRef] [PubMed]
64. Marine, R.; McCarren, C.; Vorrasane, V.; Nasko, D.; Crowgey, E.; Polson, S.W.; Wommack, K.E. Caught in the middle with multiple displacement amplification: The myth of pooling for avoiding multiple displacement amplification bias in a metagenome. Microbiome 2014, 2. [CrossRef] [PubMed]
65. Polson, S.W.; Wilhelm, S.W.; Wommack, K.E. Unraveling the viral tapestry (from inside the capsid out). ISME J. 2011, 5, 165-168. [CrossRef] [PubMed]
66. 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 2012, 7, e40418. [CrossRef] [PubMed]
67. Hopkins, M.; Kailasan, S.; Cohen, A.; Roux, S.; Tucker, K.P.; Shevenell, A.; Agbandje-McKenna, M.; Breitbart, M. Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein. ISME J. 2014, 8, 2093-2103. [CrossRef] [PubMed]
68. Reavy, B.; Swanson, M.M.; Cock, P.; Dawson, L.; Freitag, T.E.; Singh, B.K.; Torrance, L.; Mushegian, A.R.; Taliansky, M. Distinct circular single-stranded DNA viruses exist in different soil types. Appl. Environ. Microbiol. 2015, 81, 3934-3945. [CrossRef] [PubMed]
69. Labonté, J.M.; Hallam, S.; Suttle, C.A. Previously unknown evolutionary groups dominate the ssDNA gokushoviruses in oxic and anoxic waters of a coastal marine environment. Front. Microbiol. 2015, 6. [CrossRef] [PubMed]
70. Bryson, S.; Thurber, A.R.; Correa, A.M.S.; Orphan, V.J.; Thurber, R.V. A novel sister clade to the Enterobacteria microviruses (family Microviridae) identified in methane seep sediments. Environ. Microbiol. 2015, 17, 3708-3721. [CrossRef] [PubMed]
71. Krupovic, M.; Forterre, P. Microviridae goes temperate: Microvirus-related proviruses reside in the genomes of Bacteroidetes. PLoS ONE 2011, 6, e19893. [CrossRef] [PubMed]
72. Bath, C.; Dyall-Smith, M.L. His1, an archaeal virus of the Fuselloviridae family that infects Haloarcula Hispanica. J. Virol. 1998, 72, 9392-9395. [PubMed]
73. Bath, C.; Cukalac, T.; Porter, K.; Dyall-Smith, M.L. His1 and His2 are distantly related, spindle-shaped haloviruses belonging to the novel virus group, Salterprovirus. Virology 2006, 350, 228-239. [CrossRef] [PubMed]
74. Pietilä, M.K.; Atanasova, N.S.; Oksanen, H.M.; Bamford, D.H. Modified coat protein forms the flexible spindle-shaped virion of haloarchaeal virus His1. Environ. Microbiol. 2013, 15, 1674-1686. [CrossRef] [PubMed]
75. Krupovic, M.; Quemin, E.R.J.; Bamford, D.H.; Forterre, P.; Prangishvili, D. Unification of the globally distributed spindle-shaped viruses of the Archaea. J. Virol. 2014, 88, 2354-2358. [CrossRef] [PubMed]
76. Williamson, S.J.; Allen, L.Z.; Lorenzi, H.A.; Fadrosh, D.W.; Brami, D.; Thiagarajan, M.; McCrow, J.P.; Tovchigrechko, A.; Yooseph, S.; Venter, J.C. Metagenomic exploration of viruses throughout the Indian Ocean. PLoS ONE 2012, 7, e42047. [CrossRef] [PubMed]
77. Zablocki, O.; van Zyl, L.; Adriaenssens, E.M.; Rubagotti, E.; Tuffin, M.; Cary, S.C.; Cowan, D. High-level diversity of tailed phages, eukaryote-associated viruses and virophage-like elements in the metaviroms of Antarctic soils. Appl. Environ. Microbiol. 2014, 80, 6888-6897. [CrossRef] [PubMed]
78. Holmfeldt, K.; Solonenko, N.; Shah, M.; Corrier, K.; Riemann, L.; Verberkmoes, N.C.; Sullivan, M.B. Twelve previously unknown phage genera are ubiquitous in global oceans. Proc. Natl. Acad. Sci. USA 2013, 110, 12798-12803. [CrossRef] [PubMed]
79. 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. 2014, 5. [CrossRef] [PubMed]
80. Stachler, E.; Bibby, K. Metagenomic evaluation of the highly abundant human gut bacteriophage CrAssphage for source tracking of human fecal pollution. Environ. Sci. Technol. Lett. 2014, 1, 405-409. [CrossRef]