The baltic sea virome: Diversity and transcriptional activity of DNA and RNA viruses

mSystems

Volumn 2, Issue 1, 2017, Pages

  Allen, Lisa Zeigler ^a   McCrow, John P ^a   Ininbergs, Karolina ^c   Dupont, Christopher L ^a   Badger, Jonathan H ^a,d   Hoffman, Jeffery M ^a   Ekman, Martin ^c   Allen, Andrew E ^a,b   Bergman, Birgitta ^c   Venter, J Craig ^a  

^a J CRAIG VENTER INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STOCKHOLM UNIVERSITY   (Sweden)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Marine microbiology; Viral ecology; Viral metagenomics; Viral metatranscriptomics; Viral host inference

Indexed keywords

EID: 85033380550     PISSN: None     EISSN: 23795077     Source Type: Journal    
DOI: 10.1128/mSystems.00125-16     Document Type: Article

References (94)

1. Fuhrman JA. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-548. https://doi.org/10.1038/21119.
2. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F. 1983. The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257-263. https://doi.org/10.3354/meps010257.
3. Kirchman DL. 1994. The uptake of inorganic nutrients by heterotrophic bacteria. Microb Ecol 28:255-271. https://doi.org/10.1007/BF00166816.
4. Azam F. 1998. Microbial control of oceanic carbon flux: the plot thickens. Science 280:694-696. https://doi.org/10.1126/science.280.5364.694.
5. Wilhelm SW, Suttle CA. 1999. Viruses and nutrient cycles in the sea. BioScience 49:781-788. https://doi.org/10.2307/1313569.
6. Matthaus W, Schinke H. 1999. The influence of river runoff on deep water conditions of the Baltic Sea. Hydrobiologia 393:1-10. https://doi.org/10.1023/A:1003573328473.
7. DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard NU, Martinez A, Sullivan MB, Edwards R, Brito BR, Chisholm SW, Karl DM. 2006. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311:496-503. https://doi.org/10.1126/science.1120250.
8. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66-74. https://doi.org/10.1126/science.1093857.
9. Williamson SJ, Allen LZ, Lorenzi HA, Fadrosh DW, Brami D, Thiagarajan M, McCrow JP, Tovchigrechko A, Yooseph S, Venter JC. 2012. Metagenomic exploration of viruses throughout the Indian Ocean. PLoS One 7:e42047. https://doi.org/10.1371/journal.pone.0042047.
10. Breitbart M, Felts B, Kelley S, Mahaffy JM, Nulton J, Salamon P, Rohwer F. 2004. Diversity and population structure of a near-shore marinesediment viral community. Proc Biol Sci 271:565-574. https://doi.org/10.1098/rspb.2003.2628.
11. 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. https://doi.org/10.1371/journal.pone.0057355.
12. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM, Furlan M, Desnues C, Haynes M, Li L, McDaniel L, Moran MA, Nelson KE, Nilsson C, Olson R, Paul J, Brito BR, Ruan Y, Swan BK, Stevens R, Valentine DL, Thurber RV, Wegley L, White BA, Rohwer F. 2008. Functional metagenomic profiling of nine biomes. Nature 452:629-632. https://doi.org/10.1038/nature06810.
13. Andersson AF, Riemann L, Bertilsson S. 2010. Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities. ISME J 4:171-181. https://doi.org/10.1038/ismej.2009.108.
14. Jenkins DE, Auger EA, Matin A. 1991. Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival. J Bacteriol 173:1992-1996. https://doi.org/10.1128/jb.173.6.1992-1996.1991.
15. Jenkins CA, Hayes PK. 2006. Diversity of cyanophages infecting the heterocystous filamentous cyanobacterium Nodularia isolated from the brackish Baltic Sea. J Mar Biol Assoc U.K. 86:529-536. https://doi.org/10.1017/S0025315406013439.
16. Herlemann DP, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ, Andersson AF. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571-1579. https://doi.org/10.1038/ismej.2011.41.
17. Herlemann DP, Woelk J, Labrenz M, Jurgens K. 2014. Diversity and abundance of "Pelagibacterales" (SAR 11). Syst Appl Microbiol 37: 601-604. https://doi.org/10.1016/j.syapm.2014.09.002.
18. Farnelid H, Bentzon-Tilia M, Andersson AF, Bertilsson S, Jost G, Labrenz M, Jurgens K, Riemann L. 2013. Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea. ISME J 7:1413-1423. https://doi.org/10.1038/ismej.2013.26.
19. Dupont CL, Larsson J, Yooseph S, Ininbergs K, Goll J, Asplund-Samuelsson J, McCrow JP, Celepli N, Allen LZ, Ekman M, Lucas AJ, Hagstrom A, Thiagarajan M, Brindefalk B, Richter AR, Andersson AF, Tenney A, Lundin D, Tovchigrechko A, Nylander JA, Brami D, Badger JH, Allen AE, Rusch DB, Hoffman J, Norrby E, Friedman R, Pinhassi J, Venter JC, Bergman B. 2014. Functional tradeoffs underpin salinity-driven divergence in microbial community composition. PLoS One 9:e89549. https://doi.org/10.1371/journal.pone.0089549.
20. Larsson J, Celepli N, Ininbergs K, Dupont CL, Yooseph S, Bergman B, Ekman M. 2014. Picocyanobacteria containing a novel pigment gene cluster dominate the brackish water Baltic Sea. ISME J 8:1892-1903. https://doi.org/10.1038/ismej.2014.35.
21. Thureborn P, Lundin D, Plathan J, Poole AM, Sjoberg BM, Sjoling S. 2013. A metagenomics transect into the deepest point of the Baltic Sea reveals clear stratification of microbial functional capacities. PLoS One 8:e74983. https://doi.org/10.1371/journal.pone.0074983.
22. Asplund-Samuelsson J, Sundh J, Dupont CL, Allen AE, McCrow JP, Celepli NA, Bergman B, Ininbergs K, Ekman M. 2016. Diversity and expression of bacterial metacaspases in an aquatic ecosystem. Front Microbiol 7:1043. https://doi.org/10.3389/fmicb.2016.01043.
23. Feike J, Jurgens K, Hollibaugh JT, Kruger S, Jost G, Labrenz M. 2012. Measuring unbiased metatranscriptomics in suboxic waters of the central Baltic Sea using a new in situ fixation system. ISME J 6:461-470. https://doi.org/10.1038/ismej.2011.94.
24. Brindefalk B, Ekman M, Ininbergs K, Dupont CL, Yooseph S, Pinhassi J, Bergman B. 2016. Distribution and expression of microbial rhodopsins in the Baltic Sea and adjacent waters. Environ Microbiol 18:4442-4455. https://doi.org/10.1111/1462-2920.13407.
25. Šulčius S, Holmfeldt K. 2016. Viruses of microorganisms in the Baltic Sea: current state of research and perspectives. Mar Biol Res 12:115-124. https://doi.org/10.1080/17451000.2015.1118514.
26. Weinbauer MG, Brettar I, Hofle MG. 2003. Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol Oceanogr 48:1457-1465. https://doi.org/10.4319/lo.2003.48.4.1457.
27. Riemann L, Holmfeldt K, Titelman J. 2009. Importance of viral lysis and dissolved DNA for bacterioplankton activity in a P-limited estuary, northern Baltic Sea. Microb Ecol 57:286-294. https://doi.org/10.1007/s00248-008-9429-0.
28. Holmfeldt K, Titelman J, Riemann L. 2010. Virus production and lysate recycling in different sub-basins of the northern Baltic Sea. Microb Ecol 60:572-580. https://doi.org/10.1007/s00248-010-9668-8.
29. Luhtanen AM, Eronen-Rasimus E, Kaartokallio H, Rintala JM, Autio R, Roine E. 2014. Isolation and characterization of phage-host systems from the Baltic Sea ice. Extremophiles 18:121-130. https://doi.org/10.1007/s00792-013-0604-y.
30. Senčilo A, Luhtanen AM, Saarijarvi M, Bamford DH, Roine E. 2015. Cold-active bacteriophages from the Baltic Sea ice have diverse genomes and virus-host interactions. Environ Microbiol 17:3628-3641. https://doi.org/10.1111/1462-2920.12611.
31. Jakubowska-Deredas M, Jurczak-Kurek A, Richert M, Łoś M, Narajczyk M, Wrobel B. 2012. Diversity of tailed phages in Baltic Sea sediment: large number of siphoviruses with extremely long tails. Res Microbiol 163: 292-296. https://doi.org/10.1016/j.resmic.2012.02.002.
32. Zeigler Allen L, Allen EE, Badger JH, McCrow JP, Paulsen IT, Elbourne LD, Thiagarajan M, Rusch DB, Nealson KH, Williamson SJ, Venter JC, Allen AE. 2012. Influence of nutrients and currents on the genomic composition of microbes across an upwelling mosaic. ISME J 6:1403-1414. https://doi.org/10.1038/ismej.2011.201.
33. Wu M, Eisen JA. 2008. A simple, fast, and accurate method of phylogenomic inference. Genome Biol 9:R151. https://doi.org/10.1186/gb-2008-9-10-r151.
34. Ahlgren NA, Rocap G. 2012. Diversity and distribution of marine Synechococcus: multiple gene phylogenies for consensus classification and development of qPCR assays for sensitive measurement of clades in the ocean. Front Microbiol 3:213. https://doi.org/10.3389/fmicb.2012.00213.
35. Waterbury JB, Watson FW, Valois FW, Franks DG. 1986. Biological and ecological characterization of the marine unicellular cyanobacterium Synechococcus, p 71-120. In Platt T, Li WKW (ed), Photosynthetic picoplankton. Canadian Department of Fisheries and Oceans, Ottawa, Ontario, Canada.
36. Palenik B. 2001. Chromatic adaptation in marine Synechococcus strains. Appl Environ Microbiol 67:991-994. https://doi.org/10.1128/AEM.67.2.991-994.2001.
37. Sullivan MB, Krastins B, Hughes JL, Kelly L, Chase M, Sarracino D, Chisholm SW. 2009. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial "mobilome". Environ Microbiol 11:2935-2951. https://doi.org/10.1111/j.1462-2920.2009.02081.x.
38. Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, Landry ZC, Ellisman M, Deerinck T, Sullivan MB, Giovannoni SJ. 2013. Abundant SAR11 viruses in the ocean. Nature 494:357-360. https://doi.org/10.1038/nature11921.
39. Rohwer F, Segall A, Steward G, Seguritan V, Breitbart M, Wolven F, Azam F. 2000. The complete genomic sequence of the marine phage Roseophage SIO1 shares homology with nonmarine phages. Limnol Oceanogr 45:408-418. https://doi.org/10.4319/lo.2000.45.2.0408.
40. Angly F, Youle M, Nosrat B, Srinagesh S, Rodriguez-Brito B, McNairnie P, Deyanat-Yazdi G, Breitbart M, Rohwer F. 2009. Genomic analysis of multiple Roseophage SIO1 strains. Environ Microbiol 11:2863-2873. https://doi.org/10.1111/j.1462-2920.2009.02021.x.
41. Suttle CA. 2007. Marine viruses - major players in the global ecosystem. Nat Rev Microbiol 5:801-812. https://doi.org/10.1038/nrmicro1750.
42. Weinbauer MG. 2004. Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127-181. https://doi.org/10.1016/j.femsre.2003.08.001.
43. Proctor LM, Fuhrman JA. 1990. Viral mortality of marine bacteria and cyanobacteria. Nat Lond 343:60-62. https://doi.org/10.1038/343060a0.
44. Fuhrman JA. 1992. Bacterioplankton roles in cycling of organic matter: the microbial food web, p 361-383. In Falkowski PG, Woodhead AD (ed), Primary productivity and biogeochemical cycles in the sea. Plenum Press, New York, NY.
45. Gobler CJ, Hutchins DA, Fisher NS, Cosper EM, Saňudo-Wilhelmy SA. 1997. Release and bioavailability of C, N, P, Se, and Fe following viral lysis of a marine chrysophyte. Limnol Oceanogr 42:1492-1504. https://doi.org/10.4319/lo.1997.42.7.1492.
46. Wommack KE, Colwell RR. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69-114. https://doi.org/10.1128/MMBR.64.1.69-114.2000.
47. Weitz JS, Wilhelm SW. 2012. Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol Rep 4:17. https://doi.org/10.3410/B4-17.
48. Holmfeldt K, Odić D, Sullivan MB, Middelboe M, Riemann L. 2012. Cultivated single-stranded DNA phages that infect marine Bacteroidetes prove difficult to detect with DNA-binding stains. Appl Environ Microbiol 78:892-894. https://doi.org/10.1128/AEM.06580-11.
49. Wommack KE, Hill RT, Colwell RR. 1995. A simple method for the concentration of viruses from natural water samples. J Microbiol Methods 22:57-67. https://doi.org/10.1016/0167-7012(94)00064-E.
50. Maranger R, Bird DF. 1995. Viral abundance in aquatic systems: a comparison between marine and fresh-waters. Mar Ecol Prog Ser 121: 217-226. https://doi.org/10.3354/meps121217.
51. Cassman N, Prieto-Davo A, Walsh K, Silva GG, Angly F, Akhter S, Barott K, Busch J, McDole T, Haggerty JM, Willner D, Alarcon G, Ulloa O, DeLong EF, Dutilh BE, Rohwer F, Dinsdale EA. 2012. Oxygen minimum zones harbour novel viral communities with low diversity. Environ Microbiol 14:3043-3065. https://doi.org/10.1111/j.1462-2920.2012.02891.x.
52. Bratbak G, Heldal M, Naess A, Roeggen T. 1993. Viral impact on microbial communities, p 299-302. In Guerrero R, Pedros-Alio C (ed), Trends in microbial ecology. Spanish Society for Microbiology, Barcelona, Spain.
53. Hewson I, Fuhrman JA. 2006. Viral impacts upon marine bacterioplankton assemblage structure. J Mar Biol Assoc U.K. 86:577-589. https://doi.org/10.1017/S002531540601349X.
54. Keesing F, Brunner J, Duerr S, Killilea M, Logiudice K, Schmidt K, Vuong H, Ostfeld RS. 2009. Hosts as ecological traps for the vector of Lyme disease. Proc Biol Sci 276:3911-3919. https://doi.org/10.1098/rspb.2009.1159.
55. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS. 2010. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647-652. https://doi.org/10.1038/nature09575.
56. Ostfeld RS, Levi T, Jolles AE, Martin LB, Hosseini PR, Keesing F. 2014. Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens. PLoS One 9:e107387. https://doi.org/10.1371/journal.pone.0107387.
57. Johnson PT, Ostfeld RS, Keesing F. 2015. Frontiers in research on biodiversity and disease. Ecol Lett 18:1119-1133. https://doi.org/10.1111/ele.12479.
58. Keesing F, Ostfeld RS. 2015. Ecology. Is biodiversity good for your health? Science 349:235-236. https://doi.org/10.1126/science.aac7892.
59. Knowles B, Silveira CB, Bailey BA, Barott K, Cantu VA, Cobian-Guemes AG, Coutinho FH, Dinsdale EA, Felts B, Furby KA, George EE, Green KT, Gregoracci GB, Haas AF, Haggerty JM, Hester ER, Hisakawa N, Kelly LW, Lim YW, Little M, Luque A, McDole-Somera T, McNair K, de Oliveira LS, Quistad SD, Robinett NL, Sala E, Salamon P, Sanchez SE, Sandin S, Silva GG, Smith J, Sullivan C, Thompson C, Vermeij MJ, Youle M, Young C, Zgliczynski B, Brainard R, Edwards RA, Nulton J, Thompson F, Rohwer F. 2016. Lytic to temperate switching of viral communities. Nature 531: 466-470. https://doi.org/10.1038/nature17193.
60. Thingstad TF, Lignell R. 1997. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13:19-27. https://doi.org/10.3354/ame013019.
61. Bianchi TS, Johansson B, Elmgren R. 2000. Breakdown of phytoplankton pigments in Baltic sediments: effects of anoxia and loss of depositfeeding macrofauna. J Exp Mar Biol Ecol 251:161-183. https://doi.org/10.1016/S0022-0981(00)00212-4.
62. Kahru M, Elmgren R. 2014. Multidecadal time series of satellite-detected accumulations of cyanobacteria in the Baltic Sea. Biogeosciences 11: 3619-3633. https://doi.org/10.5194/bg-11-3619-2014.
63. Voss B, Bolhuis H, Fewer DP, Kopf M, Moke F, Haas F, El-Shehawy R, Hayes P, Bergman B, Sivonen K, Dittmann E, Scanlan DJ, Hagemann M, Stal LJ, Hess WR. 2013. Insights into the physiology and ecology of the brackish-water-adapted cyanobacterium Nodularia spumigena CCY9414 based on a genome-transcriptome analysis. PLoS One 8:e60224. https://doi.org/10.1371/journal.pone.0060224.
64. Funkey CP, Conley DJ, Reuss NS, Humborg C, Jilbert T, Slomp CP. 2014. Hypoxia sustains cyanobacteria blooms in the Baltic Sea. Environ Sci Technol 48:2598-2602. https://doi.org/10.1021/es404395a.
65. Hu YO, Karlson B, Charvet S, Andersson AF. 2016. Diversity of pico-to mesoplankton along the 2000 km salinity gradient of the Baltic Sea. Front Microbiol 7:679. https://doi.org/10.3389/fmicb.2016.00679.
66. Bertos-Fortis M, Farnelid HM, Lindh MV, Casini M, Andersson A, Pinhassi J, Legrand C. 2016. Unscrambling cyanobacteria community dynamics related to environmental factors. Front Microbiol 7:625. https://doi.org/10.3389/fmicb.2016.00625.
67. 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. https://doi.org/10.1128/mBio.00373-12.
68. Nagasaki K, Ando M, Imai I, Itakura S, Ishida Y. 1994. Virus-like particles in Heterosigma Akashiwo (Raphidophyceae): a possible red tide disintegration mechanism. Mar Biol 119:307-312. https://doi.org/10.1007/BF00349570.
69. Nagasaki K, Tomaru Y, Katanozaka N, Shirai Y, Nishida K, Itakura S, Yamaguchi M. 2004. Isolation and characterization of a novel singlestranded RNA virus infecting the bloom-forming diatom Rhizosolenia setigera. Appl Environ Microbiol 70:704-711. https://doi.org/10.1128/AEM.70.2.704-711.2004.
70. Nagasaki K. 2008. Dinoflagellates, diatoms, and their viruses. J Microbiol 46:235-243. https://doi.org/10.1007/s12275-008-0098-y.
71. Tomaru Y, Takao Y, Suzuki H, Nagumo T, Nagasaki K. 2009. Isolation and characterization of a single-stranded RNA virus infecting the bloomforming diatom Chaetoceros socialis. Appl Environ Microbiol 75: 2375-2381. https://doi.org/10.1128/AEM.02580-08.
72. Culley AI, Lang AS, Suttle CA. 2003. High diversity of unknown picornalike viruses in the sea. Nature 424:1054-1057. https://doi.org/10.1038/nature01886.
73. Culley AI, Mueller JA, Belcaid M, Wood-Charlson EM, Poisson G, Steward GF. 2014. The characterization of RNA viruses in tropical seawater using targeted PCR and metagenomics. mBio 5:e01210-14. https://doi.org/10.1128/mBio.01210-14.
74. Rosario K, Duffy S, Breitbart M. 2009. Diverse circovirus-like genome architectures revealed by environmental metagenomics. J Gen Virol 90:2418-2424. https://doi.org/10.1099/vir.0.012955-0.
75. Rosario K, Dayaram A, Marinov M, Ware J, Kraberger S, Stainton D, Breitbart M, Varsani A. 2012. Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). J Gen Virol 93:2668-2681. https://doi.org/10.1099/vir.0.045948-0.
76. Dunlap DS, Ng TF, Rosario K, Barbosa JG, Greco AM, Breitbart M, Hewson I. 2013. Molecular and microscopic evidence of viruses in marine copepods. Proc Natl Acad Sci U S A 110:1375-1380. https://doi.org/10.1073/pnas.1216595110.
77. Kim KH, Bae JW. 2011. Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl Environ Microbiol 77:7663-7668. https://doi.org/10.1128/AEM.00289-11.
78. Dean FB, Nelson JR, Giesler TL, Lasken RS. 2001. Rapid amplification of plasmid and phage DNA using Phi 29 DNA polymerase and multiplyprimed rolling circle amplification. Genome Res 11:1095-1099. https://doi.org/10.1101/gr.180501.
79. Balcere A, Noren G, Holmgren S, Hrytsyshyn P, Lobanov E, Marttila J, Merisaar M, Rimavicius R, Roggenbuck A. 2015. Report on industrial swine and cattle farming in the Baltic Sea catchment area. http://www.ccb.se/documents/indfarmencorr-000.pdf.
80. Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J, McMahon TA, Ortega CN, Sauer EL, Sehgal T, Young S, Rohr JR. 2015. Biodiversity inhibits parasites: broad evidence for the dilution effect. Proc Natl Acad Sci U S A 112:8667-8671. https://doi.org/10.1073/pnas.1506279112.
81. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. 2008. Global trends in emerging infectious diseases. Nature 451: 990-993. https://doi.org/10.1038/nature06536.
82. Morgulis A, Gertz EM, Schaffer AA, Agarwala R. 2006. A fast and symmetric DUST implementation to mask low-complexity DNA sequences. J Comput Biol 13:1028-1040. https://doi.org/10.1089/cmb.2006.13.1028.
83. Allen LZ, Ishoey T, Novotny MA, McLean JS, Lasken RS, Williamson SJ. 2011. Single virus genomics: a new tool for virus discovery. PLoS One 6:e17722. https://doi.org/10.1371/journal.pone.0017722.
84. Rho M, Tang H, Ye Y. 2010. FragGeneScan: predicting genes in short and error-prone reads. Nucleic Acids Res 38:e191. https://doi.org/10.1093/nar/gkq747.
85. Allen LZ, Allen EE, Badger JH, McCrow JP, Paulsen IT, Elbourne LD, Thiagarajan M, Rusch DB, Nealson KH, Williamson SJ, Venter JC, Allen AE. 2012. Influence of nutrients and currents on the genomic composition of microbes across an upwelling mosaic. ISME J 6:1403-1414. https://doi.org/10.1038/ismej.2011.201.
86. Schmieder R, Lim YW, Edwards R. 2012. Identification and removal of ribosomal RNA sequences from metatranscriptomes. Bioinformatics 28: 433-435. https://doi.org/10.1093/bioinformatics/btr669.
87. Bertrand EM, McCrow JP, Moustafa A, Zheng H, McQuaid JB, Delmont TO, Post AF, Sipler RE, Spackeen JL, Xu K, Bronk DA, Hutchins DA, Allen AE. 2015. Phytoplankton-bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge. Proc Natl Acad Sci U S A 112:9938-9943. https://doi.org/10.1073/pnas.1501615112.
88. Gotelli NJ, Rohde K. 2002. Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecol Lett 5:86-94. https://doi.org/10.1046/j.1461-0248.2002.00288.x.
89. Cadotte MW, Davies J. 2016. Building and using phylogenies, p 10-40. In Phylogenies in ecology: a guide to concepts and methods. Princeton University Press, Princeton, New Jersey.
90. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ. 2002. Phylogenies and community ecology. Annu Rev Ecol Syst 33:475-505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448.
91. Matsen FA, Kodner RB, Armbrust EV. 2010. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 11:538. https://doi.org/10.1186/1471-2105-11-538.
92. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JF, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers Y-H, Falcon LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC. 2007. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77. https://doi.org/10.1371/journal.pbio.0050077.
93. Gomez-Alvarez V, Teal TK, Schmidt TM. 2009. Systematic artifacts in metagenomes from complex microbial communities. ISME J 3:1314-1317. https://doi.org/10.1038/ismej.2009.72.
94. Stewart FJ, Ottesen EA, DeLong EF. 2010. Development and quantitative analyses of a universal rRNA-subtraction protocol for microbial metatranscriptomics. ISME J 4:896-907. https://doi.org/10.1038/ismej.2010.18.