Water column stratification structures viral community composition in the Sargasso Sea

Aquatic Microbial Ecology

Volumn 76, Issue 2, 2015, Pages 85-94

  Goldsmith, Dawn B ^a   Brum, Jennifer R ^b,d   Hopkins, Max ^a   Carlson, Craig A ^c   Breitbart, Mya ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b The University of Arizona   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

Bermuda Atlantic Time series Study; Diversity; Marine; Phage; Season; Signature gene; Stratification; Virus

Indexed keywords

EID: 84946561737     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01768     Document Type: Article

References (71)

1. Abascal F, Zardoya R, Telford M (2010) TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 38: W7-W13
2. Allers E, Moraru C, Duhaime MB, Beneze E and others (2013) Single-cell and population level viral infection dynamics revealed by phageFISH, a method to visualize intracellular and free viruses. Environ Microbiol 15: 2306-2318
3. Angly F, Felts B, Breitbart M, Salamon P and others (2006) The marine viromes of four oceanic regions. PLoS Biol 4: e368
4. Araújo MFF, Godinho MJL (2009) Short-term variations of virus-like particles in a tropical lake: relationship with microbial communities (bacteria, ciliates and flagellates). Microbiol Res 164: 411-419
5. Breitbart M (2012) Marine viruses: truth or dare. Annu Rev Mar Sci 4: 425-448
6. Breitbart M, Salamon P, Andresen B, Mahaffy JM and others (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99: 14250-14255
7. Brum JR, Sullivan MB (2015) Rising to the challenge: accelerated pace of discovery transforms marine virology. Nat Rev Microbiol 13: 147-159
8. Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G and others (2015) Patterns and ecological drivers of ocean viral communities. Science 348: 1261498
9. Carlson CA, Ducklow HW, Sleeter TD (1996) Stocks and dynamics of bacterioplankton in the northwestern Sargasso Sea. Deep-Sea Res II 43: 491-515
10. Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, Vergin K (2009) Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J 3: 283-295
11. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552
12. Chow CET, Fuhrman JA (2012) Seasonality and monthly dynamics of marine myovirus communities. Environ Microbiol 14: 2171-2183
13. Chow CET, Kim DY, Sachdeva R, Caron DA, Fuhrman JA (2014) Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J 8: 816-829
14. Comeau AM, Krisch HM (2008) The capsid of the T4 phage superfamily: the evolution, diversity, and structure of some of the most prevalent proteins in the biosphere. Mol Biol Evol 25: 1321-1332
15. Dang VT, Sullivan MB (2014) Emerging methods to study bacteriophage infection at the single-cell level. Front Microbiol 5: 724
16. Deng L, Gregory A, Yilmaz S, Poulos BT, Hugenholtz P, Sullivan MB (2012) Contrasting life strategies of viruses that infect photo-and heterotrophic bacteria, as revealed by viral tagging. MBio 3: e00373-12
17. DuRand M, Olson R, Chisholm S (2001) Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea. Deep-Sea Res II 48: 1983-2003
18. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797
19. Filée J, Tétart F, Suttle C, Krisch H (2005) Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc Natl Acad Sci USA 102: 12471-12476
20. Goldsmith DB, Crosti G, Dwivedi B, McDaniel LD and others (2011) Development of phoH as a novel signature gene for assessing marine phage diversity. Appl Environ Microbiol 77: 7730-7739
21. Hodcroft E (2013) TreeCollapserCL 4. http://emmahodcroft.com/TreeCollapseCL.html
22. Hopkins M, Kailasan S, Cohen A, Roux S and others (2014) Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein. ISME J 8: 2093-2103
23. Ignacio-Espinoza JC, Sullivan MB (2012) Phylogenomics of T4 cyanophages: lateral gene transfer in the 'core'and origins of host genes. Environ Microbiol 14: 2113-2126
24. Jacquet S, Bratbak G (2003) Effects of ultraviolet radiation on marine virus-phytoplankton interactions. FEMS Microbiol Ecol 44: 279-289
25. Labonté JM, Suttle CA (2013) Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J 7: 2169-2177
26. Lomas M, Bates N, Johnson R, Knap A, Steinberg D, Carlson C (2013) Two decades and counting: 24-years of sustained open ocean biogeochemical measurements in the Sargasso Sea. Deep-Sea Res II 93: 16-32
27. Lozier MS, Dave AC, Palter JB, Gerber LM, Barber RT (2011) On the relationship between stratification and primary productivity in the North Atlantic. Geophys Res Lett 38, L18609, doi:10.1029/2011GL049414
28. Malmstrom RR, Coe A, Kettler GC, Martiny AC, Frias-Lopez J, Zinser ER, Chisholm SW (2010) Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans. ISME J 4: 1252-1264
29. Martiny AC, Tai AP, Veneziano D, Primeau F, Chisholm SW (2009) Taxonomic resolution, ecotypes and the biogeography of Prochlorococcus. Environ Microbiol 11: 823-832
30. Matteson AR, Rowe JM, Ponsero AJ, Pimentel TM, Boyd PW, Wilhelm SW (2013) High abundances of cyanomyoviruses in marine ecosystems demonstrate ecological relevance. FEMS Microbiol Ecol 84: 223-234
31. Michaels A, Knap A (1996) Overview of the US JGOFS Bermuda Atlantic Time-series Study and the Hydrostation S program. Deep-Sea Res II 43: 157-198
32. Moebus K (1992) Laboratory investigations on the survival of marine bacteriophages in raw and treated seawater. Helgolander Meeresun 46: 251-273
33. Morris RM, Rappé MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, Giovannoni SJ (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420: 806-810
34. Morris R, Vergin K, Cho J, Rappé M, Carlson C, Giovannoni S (2005) Temporal and spatial response of bacterioplankton lineages to annual convective overturn at the Ber muda Atlantic Time-series Study site. Limnol Oceanogr 50: 1687-1696
35. Morrison JR, Nelson NB (2004) Seasonal cycle of phytoplankton UV absorption at the Bermuda Atlantic Time-series Study (BATS) site. Limnol Oceanogr 49: 215-224
36. Mühling M, Fuller N, Millard A, Somerfield P and others (2005) Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: evidence for viral control of phytoplankton. Environ Microbiol 7: 499-508
37. Needham DM, Chow CET, Cram JA, Sachdeva R, Parada A, Fuhrman JA (2013) Short-term observations of marine bacterial and viral communities: patterns, connections and resilience. ISME J 7: 1274-1285
38. Nelson N, Siegel D, Yoder J (2004) The spring bloom in the northwestern Sargasso Sea: spatial extent and relationship with winter mixing. Deep-Sea Res II 51: 987-1000
39. Noble RT, Fuhrman J (1997) Virus decay and its causes in coastal waters. Appl Environ Microbiol 63: 77-83
40. Oksanen J, Blanchet FG, Kindt R, Legendre P and others (2013) vegan: community ecology package. http://cran.r-project.org
41. Palter JB, Lozier MS, Barber RT (2005) The effect of advection on the nutrient reservoir in the North Atlantic subtropical gyre. Nature 437: 687-692
42. Parsons RJ, Breitbart M, Lomas MW, Carlson CA (2012) Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J 6: 273-284
43. Price MN, Dehal PS, Arkin AP (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5: e9490
44. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. www.r-project.org
45. Ramette A (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75: 2495-2505
46. Rocap G, Distel DL, Waterbury JB, Chisholm SW (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68: 1180-1191
47. Roux S, Enault F, Robin A, Ravet V and others (2012) Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS ONE 7: e33641
48. Roux S, Hawley AK, Beltran MT, Scofield M and others (2014) Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics. eLife 3: e03125
49. Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, Vol 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
50. Siegel DA, McGillicuddy DJ, Fields EA (1999) Mesoscale eddies, satellite altimetry, and new production in the Sargasso Sea. J Geophys Res-Oceans 104: 13359-13379
51. Sprintall J, Tomczak M (1992) Evidence of the barrier layer in the surface layer of the tropics. J Geophys Res-Oceans 97: 7305-7316
52. Srinivasiah S, Lovett J, Polson S, Bhavsar J and others (2013) Direct assessment of viral diversity in soils by random PCR amplification of polymorphic DNA. Appl Environ Microbiol 79: 5450-5457
53. Steinberg DK, Carlson CA, Bates NR, Johnson RJ, Michaels AF, Knap AH (2001) Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decadescale look at ocean biology and biogeochemistry. Deep-Sea Res II 48: 1405-1447
54. Sullivan MB (2015) Viromes, not gene markers for studying dsDNA viral communities. J Virol 89: 2459-2461
55. Sullivan MB, Huang K, Ignacio Espinoza J, Berlin A and others (2010) Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol 12: 3035-3056
56. Suttle CA (2007) Marine viruses - major players in the global ecosystem. Nat Rev Microbiol 5: 801-812
57. Suttle CA, Chen F (1992) Mechanisms and rates of decay of marine viruses in seawater. Appl Environ Microbiol 58: 3721-3729
58. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564-577
59. Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F (2009) Laboratory procedures to generate viral metagenomes. Nat Protoc 4: 470-483
60. Treusch AH, Vergin KL, Finlay LA, Donatz MG, Burton RM, Carlson CA, Giovannoni SJ (2009) Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J 3: 1148-1163
61. Treusch AH, Demir-Hilton E, Vergin KL, Worden AZ and others (2012) Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids. ISME J 6: 481-492
62. Tucker KP, Parsons R, Symonds EM, Breitbart M (2011) Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean. ISME J 5: 822-830
63. Vergin KL, Beszteri B, Monier A, Thrash JC and others (2013) High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences. ISME J 7: 1322-1332
64. Weinbauer MG, Suttle CA (1999) Lysogeny and prophage induction in coastal and offshore bacterial communities. Aquat Microb Ecol 18: 217-225
65. Wilhelm SW, Weinbauer MG, Suttle CA, Jeffrey WH (1998) The role of sunlight in the removal and repair of viruses in the sea. Limnol Oceanogr 43: 586-592
66. Winter C, Weinbauer MG (2010) Randomly amplified polymorphic DNA reveals tight links between viruses and microbes in the bathypelagic zone of the northwestern Mediterranean Sea. Appl Environ Microbiol 76: 6724-6732
67. Wommack KE, Hill RT, Muller TA, Colwell RR (1996) Effects of sunlight on bacteriophage viability and structure. Appl Environ Microbiol 62: 1336-1341
68. Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc Series B Stat Methodol 73: 3-36
69. Yu Y, Breitbart M, McNairnie P, Rohwer F (2006) Fast-GroupII: a web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinformatics 7: 57
70. Zhao Y, Temperton B, Thrash JC, Schwalbach MS and others (2013) Abundant SAR11 viruses in the ocean. Nature 494: 357-360
71. Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S and others (2008) Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10: 147-161