Seasonal time bombs: Dominant temperate viruses affect Southern Ocean microbial dynamics

ISME Journal

Volumn 10, Issue 2, 2016, Pages 437-449

  Brum, Jennifer R ^a,d   Hurwitz, Bonnie L ^b   Schofield, Oscar ^c   Ducklow, Hugh W ^d   Sullivan, Matthew B ^e  

^a University of Arizona   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c Doherty Earth Observatory of Columbia University   (United States)

^d OHIO STATE UNIVERSITY   (United States)

^e University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOINFORMATICS; COMMUNITY DYNAMICS; ECOSYSTEM FUNCTION; GENETIC ANALYSIS; MICROBIAL COMMUNITY; SEASONALITY; TEMPERATE ENVIRONMENT; VIRUS;

ANTARCTIC PENINSULA; ANTARCTICA; SOUTHERN OCEAN; WEST ANTARCTICA;

BACTERIA (MICROORGANISMS); DNA VIRUSES;

SEA WATER;

ANTARCTICA; CLASSIFICATION; ECOSYSTEM; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METAGENOMICS; SEA; SEASON; VIROLOGY; VIRUS;

ANTARCTIC REGIONS; ECOSYSTEM; METAGENOMICS; OCEANS AND SEAS; SEASONS; SEAWATER; VIRUSES;

EID: 84955204689     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.125     Document Type: Article

References (79)

1. Anesio AM, Bellas CM. (2011). Are low temperature habitats hot spots of microbial evolution driven by viruses? Trends Microbiol 19: 52-57.
2. Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C et al. (2006). The marine viromes of four oceanic regions. PLoS Biol 4: 2121-2131.
3. Billen G, Becquevort S. (1991). Phytoplankton-bacteria relationship in the Antarctic marine ecosystem. Polar Res 10: 245-254.
4. Binder B. (1999). Reconsidering the relationship between virally induced bacterial mortality and the frequency of infected cells. Aquat Microb Ecol 18: 207-215.
5. Bird DF, Karl DM. (1999). Uncoupling of bacteria and phytoplankton during the austral spring bloom in Gerlache Strait, Antarctic Peninsula. Aquat Microb Ecol 19: 13-27.
6. Bird DF, Maranger R, Karl DM. (1993). Palmer LTER: Aquatic virus abundances near the Antarctic Peninsula. Antarct J US 28: 234-235.
7. Boras JA, Sala MM, Vazquez-Dominguez E, Weinbauer MG, Vaque D. (2009). Annual changes of bacterial mortality due to viruses and protists in an oligotrophic coastal environment (NW Mediterranean). Environ Microbiol 11: 1181-1193.
8. Breitbart M. (2012). Marine viruses: Truth or dare. Ann Rev Mar Sci 4: 425-448.
9. Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG, Alberti A et al. (2015). Patterns and ecological drivers of ocean viral communities. Science 348: 1261498.
10. Brum JR, Morris JJ, Decima M, Stukel MR. (2014). Mortality in the oceans: causes and consequences. In: Kemp PF (ed) Eco-DAS IX Symposium Proceedings. ASLO: Waco, TX, USA, pp 16-48.
11. Brum JR, Steward GF, Jiang SC, Jellison R. (2005). Spatial and temporal variability of prokaryotes, viruses, and viral infections of prokaryotes in an alkaline, hypersaline lake. Aquat Microb Ecol 41: 247-260.
12. Brum JR, Sullivan MB. (2015). Rising to the challenge: Accelerated pace of discovery transforms marine virology. Nat Rev Microbiol 13: 147-159.
13. Brussaard CPD, Timmermans KR, Uitz J, Veldhuis MJW. (2008). Virioplankton dynamics and virally induced phytoplankton lysis versus microzooplankton grazing southeast of the Kerguelen (Southern Ocean). Deep Sea Res Part 2 Top Stud Oceanogr 55: 752-765.
14. Chen Y, Golding I, Sawai S, Guo L, Cox EC. (2005). Population fitness and the regulation of Escherichia coli genes by bacterial viruses. PLoS Biol 3: e229.
15. Cottrell MT, Kirchman DL. (2012). Virus genes in Arctic marine bacteria identified by metagenomic analysis. Aquat Microb Ecol 66: 107-116.
16. Doney SC, Ruckelshaus M, Emmett Duffy J, Barry JP, Chan F, English CA et al. (2012). Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4: 11-37.
17. Duarte CM, Agusti S, Vaque D, Agawin NSR, Felipe J, Casamayor EO et al. (2005). Experimental test of bacteria-phytoplankton coupling in the Southern Ocean. Limnol Oceanogr 50: 1844-1854.
18. Ducklow H, Carlson C, Church M, Kirchman D, Smith D, Steward G. (2001). The seasonal development of the bacterioplankton bloom in the Ross Sea, Antarctica, 1994-1997. Deep Sea Res Part 2 Top Stud Oceanogr 48: 4199-4221.
19. Ducklow H, Clarke A, Dickhut R, Doney SC, Geisz H, Huang K et al. (2012a). The marine system of the western Antarctic Peninsula. In: Rogers AD, Johnston NM, Murphy EJ, Clarke A (ed) Antarctic Ecosystems: An Extreme Environment in a Changing World. Blackwell Publishing Ltd. : Hoboken, NJ, USA, pp 121-159.
20. Ducklow HW. (2008). Long-term studies of the marine ecosystem along the west Antarctic Peninsula. Deep Sea Res Part 2 Top Stud Oceanogr 55: 1945-1948.
21. Ducklow HW, Baker K, Martinson DG, Quetin LB, Ross RM, Smith RC et al. (2007). Marine pelagic ecosystems: The West Antarctic Peninsula. Phil Trans R Soc B 362: 67-94.
22. Ducklow HW, Dickson M-L, Kirchman DL, Steward G, Orchardo J, Marra J et al. (2000). Constraining bacterial production, conversion efficiency and respiration in the Ross Sea, Antarctica, January-February, 1997. Deep Sea Res Part 2 Top Stud Oceanogr 47: 3227-3247.
23. Ducklow HW, Schofield O, Vernet M, Stammerjohn S, Erickson M. (2012b). Multiscale control of bacterial production by phytoplankton dynamics and sea ice along the western Antarctic Peninsula: A regional and decadal investigation. J Mar Syst 98-99: 26-39.
24. Duhaime MB, Sullivan MB. (2012). Ocean viruses: rigorously evaluating the metagenomic sample-tosequence pipeline. Virology 434: 181-186.
25. Duhaime MBD, Deng L, Poulos BT, Sullivan MB. (2012). Towards quantitative metagenomics of wild viruses and other ultra-low concentration DNA samples: A rigorous assessment and optimization of the linker amplification method. Environ Microbiol 14: 2526-2537.
26. Evans C, Brussaard CPD. (2012). Regional variation in lytic and lysogenic viral infection in the Southern Ocean and its contribution to biogeochemical cycling. Appl Environ Microbiol 78: 6741-6748.
27. Evans C, Pearce I, Brussaard CPD. (2009). Viral-mediated lysis of microbes and carbon release in the sub-Antarctic and Polar Frontal zones of the Australian Southern Ocean. Environ Microbiol 11: 2924-2934.
28. Fuhrman J. (2000). Impact of viruses on bacterial processes. In: Kirchman DL (ed) Microbial Ecology of the Oceans. Wiley-Liss, Inc. : New York, NY, USA, pp 327-350.
29. Fuhrman JA. (1999). Marine viruses and their biogeochemical and ecological effects. Nature 399: 541-548.
30. Ghiglione JF, Murray AE. (2012). Pronounced summer to winter differences and higher wintertime richness in coastal Antarctic marine bacterioplankton. Environ Microbiol 14: 617-629.
31. Grzymski JJ, Riesenfeld CS, Williams TJ, Dussaq AM, Ducklow H, Erickson M et al. (2012). A metagenomic assessment of winter and summer bacterioplankton from Antarctica Peninsula coastal surface waters. ISME J 6: 2901-2915.
32. Guixa-Boixereu N, Vaque D, Gasol JM, Sanchez-Camara J, Pedro-Alio C. (2002). Viral distribution and activity in Antarctic waters. Deep Sea Res Part 2 Top Stud Oceanogr 49: 827-845.
33. Hewson I, Fuhrman JA. (2007). Characterization of lysogens in bacterioplankton assemblages of the Southern California Borderland. Microb Ecol 53: 631-638.
34. Holm-Hansen O, Lorenzen CJ, Holmes RW, Strickland JDH. (1965). Fluorometric determination of chlorophyll. J Cons Int Explor Mer 30: 3-15.
35. Hurwitz B, Westvald A, Brum J, Sullivan M. (2014). Modeling ecological drivers in marine viral communities using comparative metagenomics and network analyses. Proc Natl Acad Sci USA 111: 10714-10719.
36. Hurwitz BL, Deng L, Poulos BT, Sullivan MB. (2013). Evaluation of methods to concentrate and purify ocean virus communities through comparative, replicated metagenomics. Environ Microbiol 15: 1428-1440.
37. Hurwitz BL, Sullivan MB. (2013). The Pacific ocean virome (POV): A marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS ONE 8: e57355.
38. John SG, Mendez CB, Deng L, Poulos B, Kauffman AKM, Kern S et al. (2011). A simple and efficient method for concentration of ocean viruses by chemical flocculation. Environ Microbiol Rep 3: 195-202.
39. Karl DM, Holm-Hansen O, Taylor GT, Tien G, Bird DF. (1991). Microbial biomass and productivity in the western Bransfield Strait, Antarctica during the 1986-87 austral summer. Deep Sea Res A 38: 1029-1055.
40. Kirchman D. (1993). Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In: Kemp P (ed) Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers: Boca Raton, FL, USA, pp 509-512.
41. Kirchman D, K'nees E, Hodson R. (1985). Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49: 599-607.
42. Kirchman DL, Moran XAG, Ducklow H. (2009). Microbial growth in the polar oceans-role of temperature and potential impact of climate change. Nat Rev Microbiol 7: 451-459.
43. Kunin V, Hugenholtz P. (2010). PyroTagger: A fast, accurate pipeline for analysis of rRNA amplicon pyrosequence data. Open J article 1: 1-8.
44. Lane DJ. (1991). 16S/23S rRNA Sequencing. In: Stackenbrandt E, Goodfellow M (ed) Nucleic Acid Techniques in Bacterial Systematics. John Wiley & Sons: Chichester, NY, USA, pp 115-175.
45. Laybourn-Parry J, Marshall WA, Madan NJ. (2007). Viral dynamics and patterns of lysogeny in saline Antarctic lakes. Polar Biol 30: 351-358.
46. Lochte K, Bjornsen PK, Giesenhagen H. (1997). Bacterial standing stock and production and their relation to phytoplankton in the Southern Ocean. Deep Sea Res Part 2 Top Stud Oceanogr 44: 321-340.
47. Malits A, Christaki U, Obernosterer I, Weinbauer MG. (2014). Enhanced viral production and virus-mediated mortality of bacterioplankton in a natural ironfertilized bloom event above the Kerguelen Plateau. Biogeosciences 11: 6841-6853.
48. Marchant H, Davidson A, Wright S, Glazebrook J. (2000). The distribution and abundance of viruses in the Southern Ocean during spring. Antarct Sci 12: 414-417.
49. Marine R, McCarren C, Vorrasane V, Nasko D, Crowgey E, Polson S et al. (2014). Caught in the middle with multiple displacement amplification: The myth of pooling for avoiding multiple displacement amplification bias in a metagenome. Microbiome 2: 3.
50. McCalley CK, Woodcroft BJ, Hodgkins SB, Wehr RA, Kim E-H, Mondav R et al. (2014). Methane dynamics regulated by microbial community response to permafrost thaw. Nature 514: 478-481.
51. Miller RV, Day MJ. (2008). Contribution of lysogeny, pseudolysogeny, and starvation to phage ecology. In: Abedon ST (ed) Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press: Cambridge, UK, pp 114-143.
52. Mondav R, Woodcroft BJ, Kim E-H, McCalley CK, Hodgkins SB, Crill PM et al. (2014). Discovery of a novel methanogen prevalent in thawing permafrost. Nat Commun 5: 3212.
53. Moran XAG, Estrada M. (2002). Phytoplanktonic DOC and POC production in the Bransfield and Gerlache Straits as derived from kinetic experiments of 14C incorporation. Deep Sea Res Part 2 Top Stud Oceanogr 49: 769-786.
54. Moran XAG, Gasol JM, Pedros-Alio C, Estrada M. (2001). Dissolved and particulate primary production and bacterial production in offshore Antarctic waters during austral summer: coupled or uncoupled? Mar Ecol Prog Ser 222: 25-39.
55. Noble RT, Fuhrman JA. (1998). Use of SYBR green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14: 113-118.
56. Paterson H, Laybourn-Parry J. (2012). Antarctic sea ice viral dynamics over an annual cycle. Polar Biol 35: 491-497.
57. Paul JH. (2008). Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J 2: 579-589.
58. Paul JH, Weinbauer M. (2010). Detection of lysogeny in marine environments. In: Wilhelm SW, Weinbauer MG, Suttle CA (ed) Manual of Aquatic Viral Ecology. ASLO: Waco, TX, USA, pp 30-33.
59. Payet JP, Suttle CA. (2013). To kill or not to kill: The balance between lytic and lysogenic viral infections is driven by trophic status. Limnol Oceanogr 58: 465-474.
60. Pearce I, Davidson AT, Bell EM, Wright S. (2007). Seasonal changes in the concentration and metabolic activity of bacteria and viruses at an Antarctic coastal site. Aquat Microb Ecol 47: 11-23.
61. Pomeroy LR, Wiebe WJ. (2001). Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23: 187-204.
62. Proctor LM, Fuhrman JA. (1990). Viral mortality of marine bacteria and cyanobacteria. Nature 343: 60-62.
63. Rattei T, Arnold R, Tischler P, Lindner D, Stumpflen V, Mewes HW. (2006). SIMAP: The similarity matrix of proteins. Nucleic Acids Res 34: D252-D256.
64. Rich VI, Konstantinidis K, DeLong EF. (2008). Design and testing of 'genome-proxy' microarrays to profile marine microbial communities. Environ Microbiol 10: 506-521.
65. Saba GK, Fraser WR, Saba VS, Iannuzzi RA, Coleman KE, Doney SC et al. (2014). Winter and spring controls on the summer food web of the coastal West Antarctic Peninsula. Nat Commun 5: 4318.
66. Sailley SF, Ducklow HW, Moeller HV, Fraser WR, Schofield OM, Steinberg DK et al. (2013). Carbon fluxes and pelagic ecosystem dynamics near two western Antarctic Peninsula Adelie pengiun colonies: An inverse model approach. Mar Ecol Prog Ser 492: 253-272.
67. Short SM, Suttle CA. (2002). Sequence analysis of marine virus communities reveals that groups of related algal viruses are widely distribution in nature. Appl Environ Microbiol 68: 1290-1296.
68. Smith D, Azam F. (1992). A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6: 107-114.
69. Solonenko SA, Sullivan MB. (2013). Preparation of metagenomic libraries from naturally occurring marine viruses. In: DeLong EF (ed) Methods in Enzymology, Vol 531. Academic Press: Waltham, MA, USA, pp 143-165.
70. Susskind MM, Botstein D. (1978). Molecular genetics of bacteriophage P22. Microbiol Rev 42: 385-413.
71. Suttle CA. (2007). Marine viruses-major players in the global ecosystem. Nat Rev Microbiol 5: 801-812.
72. Takahashi T, Sutherland SC, Sweeney C, Poisson A, Metzl N, Tilbrook B et al. (2002). Global sea-air CO2 flux based on climatological surface ocean pCO2, and seasonal biological and temperature effects. Deep Sea Res Part 2 Top Stud Oceanogr 49: 1601-1622.
73. Thomas R, Berdjeb L, Sime-Ngando T, Jacquet S. (2011). Viral abundance, production, decay rates and life strategies (lysogeny versus lysis) in Lake Bourget (France). Environ Microbiol 13: 616-630.
74. Weinbauer MG. (2004). Ecology of prokaryotic viruses. FEMS Microbiol Rev 28: 127-181.
75. Williams TJ, Long E, Evans F, DeMaere MZ, Lauro FM, Raftery MJ et al. (2012). A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters. ISME J 6: 1883-1900.
76. Williamson SJ, Houchin LA, McDaniel L, Paul JH. (2002). Seasonal variation in lysogeny as depicted by prophage induction in Tampa Bay, Florida. Appl Environ Microbiol 68: 4307-4314.
77. Yang Y, Motegi C, Yokokawa T, Nagata T. (2010). Large-scale distribution patterns of virioplankton in the upper ocean. Aquat Microb Ecol 60: 233-246.
78. Yilmaz S, Allgaier M, Hugenholtz P. (2010). Multiple displacement amplification compromises quantitative analysis of metagenomes. Nat Methods 7: 943-944.
79. Yu Z-C, Chen X-L, Shen Q-T, Zhao D-L, Tang B-L, Su H-N et al. (2015). Filamentous phages prevalent in Pseudoalteromonas spp. confer properties advantageous to host survival in Arctic sea ice. ISME J 9: 871-881.