High-level diversity of tailed phages, eukaryote-associated viruses, and virophage-like elements in the metaviromes of antarctic soils

Applied and Environmental Microbiology

Volumn 80, Issue 22, 2014, Pages 6879-6887

  Zablocki, Olivier ^a   van Zyl, Lonnie ^b   Adriaenssens, Evelien M ^a   Rubagotti, Enrico ^a   Tuffin, Marla ^b   Cary, Stephen Craig ^c   Cowan, Don ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b UNIVERSITY OF THE WESTERN CAPE   (South Africa)

^c UNIVERSITY OF WAIKATO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; GENES; SOILS;

ANTARCTIC SOILS; ARCHAEAL; BACTERIAL COMMUNITY; CYANOBACTERIUM; CYANOPHAGES; DESERT SOILS; HIERARCHICAL SEQUENCES; SURFACE SOIL;

VIRUSES;

ABUNDANCE; ANTARCTIC ECOZONE; BACTERIUM; DESERT SOIL; EUKARYOTE; GENOME; HIERARCHICAL SYSTEM; MICROBIAL COMMUNITY; SOIL MICROORGANISM; SPECIES DIVERSITY; VIRUS;

CAUDOVIRALES; EUKARYOTA;

ANTARCTICA; BACTERIOPHAGE; BIODIVERSITY; CLASSIFICATION; ECOSYSTEM; EUKARYOTE; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; SATELLITE VIRUS; VIROLOGY;

ANTARCTIC REGIONS; BACTERIOPHAGES; BIODIVERSITY; ECOSYSTEM; EUKARYOTA; MOLECULAR SEQUENCE DATA; PHYLOGENY; SATELLITE VIRUSES; SOIL MICROBIOLOGY;

EID: 84908307840     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01525-14     Document Type: Article

References (50)

1. Oerlemans J, Fortuin JPF. 1990. Parameterization of the annual surface temperature and mass balance of Antarctica. Ann. Glaciol. 14:78-84.
2. Bockheim JG, McLeod M. 2008. Soil distribution in the McMurdo Dry Valleys, Antarctica. Geoderma 144:43-49. http://dx.doi.org/10.1016/j.geoderma.2007.10.015.
3. Cary SC, McDonald IR, Barrett JE, Cowan DA. 2010. On the rocks: the microbiology of Antarctic Dry Valley soils. Nat. Rev. Microbiol. 8:129- 138. http://dx.doi.org/10.1038/nrmicro2281.
4. Wierzchos J, de Los Ríos A, Ascas C. 2013. Microorganisms in desert rocks: the edge of life on Earth. Int. Microbiol. 15:172-182. http://dx.doi.org/10.2436/20.1501.01.170.
5. Wood SA, Rueckert A, Cowan DA, Cary SC. 2008. Sources of edaphic cyanobacterial diversity in the Dry Valleys of Eastern Antarctica. ISME J. 2:308-320. http://dx.doi.org/10.1038/ismej.2007.104.
6. Tracy CR, Streten-Joyce C, Dalton R, Nussear KE, Gibb KS, Christian KA. 2010. Microclimate and limits to photosynthesis in a diverse community of hypolithic cyanobacteria in northern Australia. Appl. Environ. Microbiol. 12: 592-607. http://dx.doi.org/10.1111/j.1462-2920.2009.02098.x.
7. Cowan DA, Sohm JA, Makhalanyane TP, Capone DG, Green TGA, Cary SC, Tuffin IM. 2011. Hypolithic communities: important nitrogen sources in Antarctic desert soils. Environ. Microbiol. Rep. 3:581-586. http://dx.doi.org/10.1111/j.1758-2229.2011.00266.x.
8. Smith MC, Bowman JP, Scott FJ, Line ME. 2000. Sublithic bacteria associated with Antarctic quartz stones. Antarct. Sci. 12:177-184. http://dx.doi.org/10.1017/S0954102000000237.
9. Pointing SB, Chan Y, Lacap DC, Lau MC, Jurgens JA, Farrell RL. 2009. Highly specialized microbial diversity in hyper-arid polar desert. Proc. Natl. Acad. Sci. U. S. A. 106:19964-19969. http://dx.doi.org/10.1073/pnas.0908274106.
10. Cowan DA, Khan N, Pointing S, Cary SC. 2010. Diverse hypolithic refuge communities in Antarctic Dry Valleys. Antarct. Sci. 22:714-720. http://dx.doi.org/10.1017/S0954102010000507.
11. Cowan DA, Pointing SB, Stevens MI, Cary SC, Stomeo F, Tuffin IM. 2011. Distribution and abiotic influences on hypolithic microbial communities in an Antarctic Dry Valley. Polar Biol. 34:307-311. http://dx.doi.org/10.1007/s00300-010-0872-2.
12. Khan N, Tuffin M, Stafford W, Cary C, Lacap DC, Pointing SB, Cowan DA. 2011. Hypolithic microbial communities of quartz rocks from Miers Valley, McMurdo Dry Valleys, Antarctica. Polar. Biol. 34:1657-1668. http://dx.doi.org/10.1007/s00300-011-1061-7.
13. Laybourn-Parry J. 2009. No place too cold. Science 324:1521-1522. http://dx.doi.org/10.1126/science.1173645.
14. Säwström C, Lisle J, Anesio AM, Priscu JC, Laybourn-Parry J. 2008. Bacteriophage in polar inland waters. Extremophiles 12:167-175. http://dx.doi.org/10.1007/s00792-007-0134-6.
15. López-Bueno A, Tamames J, Velázquez D, Moya A, Quesada A, Alcamí A. 2009. High diversity of the viral community from an Antarctic lake. Science 326:858-861. http://dx.doi.org/10.1126/science.1179287.
16. Yau S, Lauro FM, DeMaere MZ, Brown MV, Raftery MJ, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Gibson JA, Cavicchioli R. 2011. Virophage control of Antarctic algal host-virus dynamics. Proc. Natl. Acad. Sci. U. S. A. 108:6163-6168. http://dx.doi.org/10.1073/pnas.1018221108.
17. Kennedy S, Kuiken T, Jepson PD, Deaville R, Forsyth M, Barrett T, Wilson S. 2000. Mass die-off of Caspian seals caused by canine distemper virus. Emerg. Infect. Dis. 6:637-639. http://dx.doi.org/10.3201/eid0606.000613.
18. Wallensten A, Munster VJ, Osterhaus ADME, Waldenström J, Bonnedahl J, Broman T, Fouchier RAM, Olsen B. 2006. Mounting evidence for the presence of influenza A virus in the avifauna of the Antarctic region. Antarct. Sci. 18:353-356. http://dx.doi.org/10.1017/S095410200600040X.
19. Williamson KE, Radosevich M, Smith DW, Wommack KE. 2007. Incidence of lysogeny within temperate and extreme soil environments. Environ. Microbiol. 9:2563-2574. http://dx.doi.org/10.1111/j.1462-2920.2007.01374.x.
20. Meiring TL, Tuffin IM, Cary C, Cowan DA. 2012. Genome sequence of temperate bacteriophage Psymv2 from Antarctic Dry Valley soil isolate Psychrobacter sp. MV2. Extremophiles 16:715-726. http://dx.doi.org/10.1007/s00792-012-0467-7.
21. Swanson MM, Reavy B, Makarova KS, Cock PJ, Hopkins DW, Torrance L, Taliansky M. 2012. Novel bacteriophages containing a genome of another bacteriophage within their genomes. PLoS One 7:e40683. http://dx.doi.org/10.1371/journal.pone.0040683.
22. Adriaenssens EM, Van Zyl L, De Maayer P, Rubagotti E, Rybicki E, Tuffin M, Cowan DA. 9 June 2014. Metagenomic analysis of the viral community in Namib Desert hypoliths. Environ. Microbiol. http://dx.doi.org/10.1111/1462-2920.12528.
23. Hansen MC, Tolker-Nielsen T, Givskov M, Molin S. 1998. Biased 16S rDNA PCR amplification caused by interference from DNA flanking the template region. FEMS Microbiol. Ecol. 26:141-149. http://dx.doi.org/10.1111/j.1574-6941.1998.tb00500.x.
24. Reysenbach AL, Pace NR, Robb FT, Place AR. 1995. Archaea: a laboratory manual-thermophiles. Cold Spring Harb. Protoc. 16:101-107.
25. Illumina, Inc. 2012. Nextera XT DNA sample preparation guide. Part 15031942. Revision B. Illumina, Inc, San Diego, CA.
26. Roux S, Faubladier M, Mahul A, Paulhe N, Bernard A, Debroas D, Enault F. 2011. Metavir: a web server dedicated to virome analysis. Bioinformatics 27:3074-3075. http://dx.doi.org/10.1093/bioinformatics/btr519.
27. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodrigez A, Stevens R, Wilke A, Wilkening J, Edwards RA. 2008. The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. http://dx.doi.org/10.1186/1471-2105-9-386.
28. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
29. Schattner P, Brooks AN, Lowe TM. 2005. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 33:W686-W689. http://dx.doi.org/10.1093/nar/gki366.
30. McNair K, Bailey BA, Edwards RA. 2012. PHACTS, a computational approach to classifying the lifestyle of phages. Bioinformatics 28:614-618. http://dx.doi.org/10.1093/bioinformatics/bts014.
31. Zhou J, Zhang W, Yan S, Xiao J, Zhang Y, Li B, Pan Y, Wang Y. 2013. Diversity of virophages in metagenomic data sets. J. Virol. 87:4225-4236. http://dx.doi.org/10.1128/JVI.03398-12.
32. La Scola B, Desnues C, Pagnier I, Robert C, Barrassi L, Fournous G, Raoult D. 2008. The virophage as a unique parasite of the giant mimivirus. Nature 455:100-104. http://dx.doi.org/10.1038/nature07218.
33. Black LW. 1995. DNA packaging and cutting by phage terminases: control in phage T4 by a synaptic mechanism. Bioessays 17:1025-1030. http://dx.doi.org/10.1002/bies.950171206.
34. Gaia M, Benamar S, Boughalmi M, Pagnier I, Croce O, Colson P, Raoult D, La Scola B. 2014. Zamilon, a novel virophage with Mimiviridae host specificity. PLoS One 9:e94923. http://dx.doi.org/10.1371/journal.pone.0094923.
35. Makhalanyane TP, Valverde A, Birkeland NK, Cary SC, Tuffin IM, Cowan DA. 2013. Evidence for successional development in Antarctic hypolithic bacterial communities. ISME J. 7:2080-2090. http://dx.doi.org/10.1038/ismej.2013.94.
36. Iyer LM, Aravind L, Koonin EV. 2001. Common origin of four diverse families of large eukaryotic DNA viruses. J. Virol. 75:11720-11734. http://dx.doi.org/10.1128/JVI.75.23.11720-11734.2001.
37. Van Etten JL, Graves MV, Müller DG, Boland W, Delaroque N. 2002. Phycodnaviridae-large DNA algal viruses. Arch. Virol. 147:1479-1516. http://dx.doi.org/10.1007/s00705-002-0822-6.
38. Pearce DA, Newsham KK, Thorne MA, Calvo-Bado L, Krsek M, Laskaris P, Hodson A, Wellington EM. 2012. Metagenomic analysis of a southern maritime Antarctic soil. Front. Microbiol. 3:403. http://dx.doi.org/10.3389/fmicb.2012.00403.
39. Srinivasiah S, Bhavsar J, Thapar K, Liles M, Schoenfeld T, Wommack KE. 2008. Phages across the biosphere: contrasts of viruses in soil and aquatic environments. Res. Microbiol. 159:349-357. http://dx.doi.org/10.1016/j.resmic.2008.04.010.
40. Fierer N, Breitbart M, Nulton J, Salamon P, Loozupone C, Jones R, Robeson M, Edwards RA, Felts B, Rayhawk S, Knight R, Rohwer F, Jackson RB. 2007. Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, fungi, and viruses in soil. Appl. Environ. Microbiol. 73:7059-7066. http://dx.doi.org/10.1128/AEM.00358-07.
41. Breitbart M, Rohwer F. 2005. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13:278-284. http://dx.doi.org/10.1016/j.tim.2005.04.003.
42. Hurst CJ (ed). 2011. Studies in viral ecology: microbial and botanical host systems, vol 1. Wiley-Blackwell, Hoboken, NJ.
43. Wang G, Asakawa S, Kimura M. 2011. Spatial and temporal changes of cyanophage communities in paddy field soils as revealed by the capsid assembly protein gene g20. FEMS Microbiol. Ecol. 76:352-359. http://dx.doi.org/10.1111/j.1574-6941.2011.01052.x.
44. Claverie JM, Grzela R, Lartigue A, Bernadac A, Nitsche S, Vacelet J, Abergel C. 2009. Mimivirus and Mimiviridae: giant viruses with an increasing number of potential hosts, including corals and sponges. J. Invertebr. Pathol. 101:172-180. http://dx.doi.org/10.1016/j.jip.2009.03.011.
45. Dunigan DD, Fitzgerald LA, Van Etten JL. 2006. Phycodnaviruses: a peek at genetic diversity. Virus Res. 117:119-132. http://dx.doi.org/10.1016/j.virusres.2006.01.024.
46. La Scola B, Campocasso A, N'Dong R, Fournous G, Barrassi L, Flaudrops C, Raoult D. 2010. Tentative characterization of new environmental giant viruses by MALDI-TOF mass spectrometry. Intervirology 53: 344-353. http://dx.doi.org/10.1159/000312919.
47. Convey P, Gibson JA, Hillenbrand CD, Hodgson DA, Pugh PJ, Smellie JL, Stevens MI. 2008. Antarctic terrestrial life- challenging the history of the frozen continent? Biol. Rev. Camb. Philos. Soc. 83:103-117. http://dx.doi.org/10.1111/j.1469-185X.2008.00034.x.
48. Treonis AM, Wall DH, Virginia RA. 1999. Invertebrate biodiversity in Antarctic Dry Valley soils and sediments. Ecosystems 2:482-492. http://dx.doi.org/10.1007/s100219900096.
49. Friedmann EI (ed). 1993. Antarctic microbiology, p 634. Wiley-Liss, New York, NY.
50. Smith JJ, Tow LA, Stafford W, Cary C, Cowan DA. 2006. Bacterial diversity in three different Antarctic cold desert mineral soils. Microb. Ecol. 51:413-421. http://dx.doi.org/10.1007/s00248-006-9022-3.