title: Is the genetic landscape of the deep subsurface biosphere affected by viruses?
abstract: Viruses are powerful manipulators of microbial diversity, biogeochemistry, and evolution in the marine environment. Viruses can directly influence the genetic capabilities and the fitness of their hosts through the use of fitness factors and through horizontal gene transfer. However, the impact of viruses on microbial ecology and evolution is often overlooked in studies of the deep subsurface biosphere. Subsurface habitats connected to hydrothermal vent systems are characterized by constant fluid flux, dynamic environmental variability, and high microbial diversity. In such conditions, high adaptability would be an evolutionary asset, and the potential for frequent host-virus interactions would be high, increasing the likelihood that cellular hosts could acquire novel functions. Here, we review evidence supporting this hypothesis, including data indicating that microbial communities in subsurface hydrothermal fluids are exposed to a high rate of viral infection, as well as viral metagenomic data suggesting that the vent viral assemblage is particularly enriched in genes that facilitate horizontal gene transfer and host adaptability. Therefore, viruses are likely to play a crucial role in facilitating adaptability to the extreme conditions of these regions of the deep subsurface biosphere. We also discuss how these results might apply to other regions of the deep subsurface, where the nature of virus-host interactions would be altered, but possibly no less important, compared to more energetic hydrothermal systems.
authors.affiliation: School of Oceanography and Astrobiology Program, University of Washington Seattle, WA, USA.
authors.forename: Rika E
authors.initials: RE
authors.lastname: Anderson
authors.forename: William J
authors.initials: WJ
authors.lastname: Brazelton
authors.forename: John A
authors.initials: JA
authors.lastname: Baross
references.citation: Int J Syst Evol Microbiol. 2003 May;53(Pt 3):847-851
references.pmid: 12807211
references.citation: Trends Microbiol. 2005 Sep;13(9):449-56
references.pmid: 16054363
references.citation: Int J Syst Evol Microbiol. 2005 Mar;55(Pt 2):925-933
references.pmid: 15774687
references.citation: Proc Biol Sci. 2004 Mar 22;271(1539):565-74
references.pmid: 15156913
references.citation: Proc Natl Acad Sci U S A. 2004 Dec 28;101(52):18036-41
references.pmid: 15596722
references.citation: ISME J. 2008 Nov;2(11):1112-21
references.pmid: 18719614
references.citation: Environ Microbiol. 2009 Nov;11(11):2935-51
references.pmid: 19840100
references.citation: FEMS Microbiol Lett. 2001 Dec 18;205(2):291-7
references.pmid: 11750818
references.citation: Proc Natl Acad Sci U S A. 2008 Jul 29;105(30):10583-8
references.pmid: 18650394
references.citation: Microbiol Mol Biol Rev. 2011 Jun;75(2):361-422
references.pmid: 21646433
references.citation: ISME J. 2008 Dec;2(12):1194-212
references.pmid: 18670397
references.citation: Microbiology (Reading). 2005 Aug;151(Pt 8):2551-2561
references.pmid: 16079334
references.citation: ISME J. 2007 Dec;1(8):703-13
references.pmid: 18059494
references.citation: Nucleic Acids Res. 2000 Nov 1;28(21):4051-8
references.pmid: 11058099
references.citation: Appl Environ Microbiol. 1981 Feb;41(2):528-38
references.pmid: 16345722
references.citation: Nucleic Acids Res. 2010 Jan;38(Database issue):D211-22
references.pmid: 19920124
references.citation: Biol Direct. 2009 Dec 18;4:51
references.pmid: 20021668
references.citation: Chem Rev. 2007 Oct;107(10):4206-72
references.pmid: 17927159
references.citation: FEMS Microbiol Rev. 2001 Apr;25(2):175-243
references.pmid: 11250035
references.citation: BMC Bioinformatics. 2007 May 23;8:172
references.pmid: 17521438
references.citation: Nature. 2004 Mar 4;428(6978):37-43
references.pmid: 14961025
references.citation: Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14332-7
references.pmid: 16176988
references.citation: Appl Environ Microbiol. 1998 Aug;64(8):2780-7
references.pmid: 9687430
references.citation: Int J Syst Evol Microbiol. 2003 Jan;53(Pt 1):59-65
references.pmid: 12656153
references.citation: Microbiology (Reading). 2005 Mar;151(Pt 3):653-663
references.pmid: 15758212
references.citation: BMC Bioinformatics. 2008 Sep 19;9:386
references.pmid: 18803844
references.citation: Nat Rev Microbiol. 2011 Sep 06;9(10):703-12
references.pmid: 21894169
references.citation: Int J Syst Bacteriol. 1999 Apr;49 Pt 2:351-9
references.pmid: 10319455
references.citation: Anaerobe. 2007 Apr;13(2):43-9
references.pmid: 17513139
references.citation: Proc Natl Acad Sci U S A. 2004 Jul 27;101(30):11013-8
references.pmid: 15256601
references.citation: Nature. 2008 Mar 20;452(7185):340-3
references.pmid: 18311127
references.citation: J Bacteriol. 2005 Sep;187(17):5885-92
references.pmid: 16109929
references.citation: ISME J. 2008 May;2(5):571-4
references.pmid: 18288217
references.citation: Int J Syst Evol Microbiol. 2003 May;53(Pt 3):747-752
references.pmid: 12807196
references.citation: Appl Environ Microbiol. 2003 Jun;69(6):3580-92
references.pmid: 12788766
references.citation: FEMS Microbiol Rev. 2004 May;28(2):127-81
references.pmid: 15109783
references.citation: Biochem Soc Trans. 2004 Apr;32(Pt 2):184-7
references.pmid: 15046568
references.citation: Science. 2008 Dec 19;322(5909):1843-5
references.pmid: 19095942
references.citation: PLoS Biol. 2005 May;3(5):e144
references.pmid: 15828858
references.citation: Nat Rev Microbiol. 2008 Mar;6(3):181-6
references.pmid: 18157154
references.citation: ISME J. 2008 Jun;2(6):579-89
references.pmid: 18521076
references.citation: Appl Environ Microbiol. 2008 May;74(10):2933-9
references.pmid: 18359833
references.citation: Science. 2007 Mar 23;315(5819):1709-12
references.pmid: 17379808
references.citation: Nature. 2002 Jan 31;415(6871):496
references.pmid: 11823851
references.citation: Appl Environ Microbiol. 2007 Jul;73(14):4429-38
references.pmid: 17496133
references.citation: Nucleic Acids Res. 2007 Jul;35(Web Server issue):W52-7
references.pmid: 17537822
references.citation: Science. 2010 Jan 8;327(5962):167-70
references.pmid: 20056882
references.citation: PLoS One. 2008 Apr 09;3(4):e1937
references.pmid: 18398463
references.citation: Mol Microbiol. 1994 Feb;11(3):537-44
references.pmid: 8152377
references.citation: ISME J. 2009 Dec;3(12):1420-4
references.pmid: 19571895
references.citation: Nature. 2009 May 14;459(7244):207-12
references.pmid: 19444207
references.citation: Nat Struct Mol Biol. 2011 May;18(5):529-36
references.pmid: 21460843
references.citation: Science. 1996 Jun 28;272(5270):1910-4
references.pmid: 8658163
references.citation: Science. 2006 Dec 15;314(5806):1783-6
references.pmid: 17170307
references.citation: Trends Microbiol. 2010 Jan;18(1):11-9
references.pmid: 19942437
references.citation: FEMS Microbiol Ecol. 2011 Jul;77(1):120-33
references.pmid: 21410492
references.citation: Appl Environ Microbiol. 2002 Sep;68(9):4307-14
references.pmid: 12200280
references.citation: Int J Syst Evol Microbiol. 2003 Nov;53(Pt 6):1801-5
references.pmid: 14657107
references.citation: Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):859-64
references.pmid: 10639170
references.citation: Science. 2005 Apr 22;308(5721):554-7
references.pmid: 15845853
references.citation: Nature. 2005 Nov 3;438(7064):86-9
references.pmid: 16222247
references.citation: BMC Genomics. 2010 Apr 17;11:247
references.pmid: 20398413
references.citation: Nature. 2007 Jan 25;445(7126):369
references.pmid: 17251963
references.citation: Environ Microbiol. 2009 Jan;11(1):16-34
references.pmid: 18764874
references.citation: In Silico Biol. 2006;6(3):223-7
references.pmid: 16922685
references.citation: J Mol Biol. 1997 Dec 5;274(3):318-24
references.pmid: 9405142
references.citation: Science. 2007 Oct 5;318(5847):97-100
references.pmid: 17916733
references.citation: Infect Immun. 2006 Aug;74(8):4900-9
references.pmid: 16861679
references.citation: Ann Rev Mar Sci. 2010;2:279-304
references.pmid: 21141666
references.citation: Trends Genet. 2003 Apr;19(4):172-6
references.pmid: 12683966
references.citation: Extremophiles. 2005 Oct;9(5):375-83
references.pmid: 15965715
references.citation: Science. 2008 Aug 15;321(5891):960-4
references.pmid: 18703739
references.citation: Appl Environ Microbiol. 2001 Oct;67(10):4566-72
references.pmid: 11571157
references.citation: Chem Rev. 2006 Feb;106(2):687-99
references.pmid: 16464020
references.citation: J Mol Evol. 2005 Feb;60(2):174-82
references.pmid: 15791728
references.citation: PLoS Comput Biol. 2005 Nov;1(6):e60
references.pmid: 16292354
references.citation: Environ Microbiol Rep. 2011 Aug;3(4):459-65
references.pmid: 23761308
references.citation: Proc Natl Acad Sci U S A. 2008 Aug 5;105(31):10949-54
references.pmid: 18664583
references.citation: Nature. 2010 Nov 4;468(7320):67-71
references.pmid: 21048762
references.citation: Int J Syst Evol Microbiol. 2002 Jul;52(Pt 4):1089-1095
references.pmid: 12148612
references.citation: Proc Natl Acad Sci U S A. 2008 Nov 11;105(45):17516-21
references.pmid: 18987310
references.citation: Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10416-21
references.pmid: 11517341
references.citation: Nature. 2008 Apr 3;452(7187):629-32
references.pmid: 18337718
references.citation: Appl Environ Microbiol. 2004 Oct;70(10):5842-6
references.pmid: 15466522
references.citation: J Mol Microbiol Biotechnol. 2002 Jul;4(4):453-61
references.pmid: 12125824
references.citation: Proc Natl Acad Sci U S A. 2004 Jul 27;101(30):11007-12
references.pmid: 15263091
references.citation: Science. 1974 Nov 29;186(4166):790-7
references.pmid: 4377758
references.citation: Nature. 2010 Jan 28;463(7280):568-71
references.pmid: 20072129
references.citation: Science. 2005 Mar 4;307(5714):1459-61
references.pmid: 15746425
references.citation: Microb Ecol. 2008 May;55(4):626-39
references.pmid: 17687593
references.citation: FEMS Microbiol Ecol. 2003 Apr 1;43(3):393-409
references.pmid: 19719671
references.citation: Extremophiles. 1998 Jan;2(1):1-7
references.pmid: 9676237
references.citation: Nat Commun. 2010;1:147
references.pmid: 21266997
references.citation: Nature. 2005 Sep 15;437(7057):356-61
references.pmid: 16163346
references.citation: Cell. 2009 Nov 25;139(5):945-56
references.pmid: 19945378
references.citation: Nature. 2006 Jul 27;442(7101):444-7
references.pmid: 16871216
references.citation: Trends Biochem Sci. 2009 Aug;34(8):401-7
references.pmid: 19646880
references.citation: BMC Genomics. 2005 Sep 14;6:122
references.pmid: 16162277
references.citation: Nat Rev Microbiol. 2010 May;8(5):317-27
references.pmid: 20348932
references.citation: PLoS Biol. 2006 Nov;4(11):e368
references.pmid: 17090214
references.citation: Adv Exp Med Biol. 2010;675:253-64
references.pmid: 20532745
references.citation: Nature. 2008 Aug 28;454(7208):1084-7
references.pmid: 18756250
references.citation: Nature. 1998 Mar 26;392(6674):353-8
references.pmid: 9537320
references.citation: Nature. 2009 Sep 10;461(7261):258-262
references.pmid: 19710652
references.citation: Proc Natl Acad Sci U S A. 2009 Jul 14;106(28):11651-6
references.pmid: 19561304
references.citation: Science. 2010 Oct 1;330(6000):50
references.pmid: 20929803
references.citation: Nature. 2001 Oct 25;413(6858):860-4
references.pmid: 11677611
references.citation: Int J Syst Evol Microbiol. 2003 May;53(Pt 3):839-846
references.pmid: 12807210
references.citation: Nature. 1999 May 27;399(6734):323-9
references.pmid: 10360571
references.citation: ISME J. 2011 Mar;5(3):414-26
references.pmid: 20927138
references.citation: Trends Microbiol. 2005 Jun;13(6):278-84
references.pmid: 15936660
references.citation: J Bacteriol. 2004 Sep;186(18):6133-41
references.pmid: 15342583
references.citation: Virol J. 2011 Jun 09;8:287
references.pmid: 21651822