Viruses of microorganisms in the Baltic Sea: current state of research and perspectives

Marine Biology Research

Volumn 12, Issue 2, 2016, Pages 115-124

  Šulčius, Sigitas ^a   Holmfeldt, Karin ^b  

^a VILNIUS UNIVERSITY   (Lithuania)

^b LINNAEUS UNIVERSITY   (Sweden)

Author keywords

Bacteriophages; brackish water ecosystem; culture isolates; cyanophages; lytic infections; virus diversity

Indexed keywords

BACTERIOPHAGE; BACTERIUM; BRACKISH WATER; ECOSYSTEM APPROACH; FUNGUS; GENOME; GENOTYPE; MARINE ECOSYSTEM; MICROORGANISM; PHENOTYPE; RESEARCH METHOD; SPECIES DIVERSITY;

ATLANTIC OCEAN; BALTIC SEA;

ACTINOBACTERIA; ALGAE; BACTEROIDETES; CYANOBACTERIA; FUNGI; PROTEOBACTERIA;

EID: 84960392590     PISSN: 17451000     EISSN: 17451019     Source Type: Journal    
DOI: 10.1080/17451000.2015.1118514     Document Type: Review

References (57)

1. R.Ahrens. 1971. Untersuchungen zur Verbreitung von Phagen der Gattung Agrobacterium in der Ostsee. Kieler Meeresforschungen 27:102–12.
2. R.Anderson, C.Winter, K.Jürgens. 2012. Protist grazing and viral lysis as prokaryotic mortality factors at Baltic Sea oxic-anoxic interfaces. Marine Ecology Progress Series 467:1–14. doi:10.3354/meps10001
3. R.Anderson, C.Wylezich, S.Glaubitz, M.Labrenz, K.Jürgens. 2013. Impact of protist grazing on a key bacterial group for biogeochemical cycling in Baltic Sea pelagic oxic/anoxic interfaces. Environmental Microbiology 15:1580–94. doi:10.1111/1462-2920.12078
4. H.Attoui, F.M.Jaafar, M.Belhouchet, P.De Micco, X.De Lamballerie, C.P.D.Brussaard. 2006. Micromonas pusilla reovirus: a new member of the family Reoviridae assigned to a novel proposed genus (Mimoreovirus). Journal of General Virology 87:1375–83. doi:10.1099/vir.0.81584-0
5. C.Berg, L.Listmann, V.Vandieken, A.Vogts, K.Jürgens. 2015. Chemoautotrophic growth of ammonia-oxidizing Thaumarchaeota enriched from a pelagic redox gradient in the Baltic Sea. Frontiers in Microbiology 5:786. 10 pages. doi:10.3389/fmicb.2014.00786
6. J.R.Brum, R.O.Schenck, M.B.Sullivan. 2013. Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. The ISME Journal 7:1738–51. doi:10.1038/ismej.2013.67
7. C.P.D.Brussaard, A.A.M.Noordeloos, R.A.Sandaa, M.Heldal, G.Bratbak. 2004. Discovery of a dsRNA virus infecting the marine photosynthetic protist Micromonas pusilla. Virology 319:280–91. doi:10.1016/j.virol.2003.10.033
8. C.T.Chow, D.Y.Kim, R.Sachdeva, D.A.Caron, J.A.Fuhrman. 2014. Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. The ISME Journal 8:816–29. doi:10.1038/ismej.2013.199
9. V.T.Dang, C.Howard-Varona, S.Schwenck, M.B.Sullivan. 2015. Variably lytic infection dynamics of large Bacteroidetes podovirus phi38:1 against two Cellulophaga baltica host strains. Environmental Microbiology 17:4659–71. doi:10.1111/1462-2920.13009
10. C.L.Dupont, J.Larsson, S.Yooseph, K.Ininbergs, J.Goll, J.Asplund-Samuelsson, 2014. Functional tradeoffs underpin salinity-driven divergence in microbial community composition. PLoS ONE 9:e89549. 9 pages. doi:10.1371/journal.pone.0089549
11. B.Dwivedi, B.Xue, D.Lundin, R.A.Edwards, M.Breitbart. 2013. A bioinformatic analysis of ribonucleotide reductase genes in phage genomes and metagenomes. BMC Evolutionary Biology 13:e33. 17 pages. doi:10.1186/1471-2148-13-33
12. Y.Eissler, E.Sahlsten, R.A.Quiñones. 2003. Effects of virus infection on respiration rates of marine phytoplankton and microplankton communities. Marine Ecology Progress Series 262:71–80. doi:10.3354/meps262071
13. A.Gelžinis, A.Verikas, E.Vaičiukynas, M.Bačauskienė, S.Šulčius, E.Šimoliūnas,. 2015. Automatic detection and morphological delineation of bacteriophages in electron microscopy images. Computers in Biology and Medicine 64:101–16. doi:10.1016/j.compbiomed.2015.06.015
14. T.H.A.Haverkamp, D.Schouten, M.Doeleman, U.Wollenzien, J.Huisman, L.J.Stal. 2009. Colorful microdiversity of Synechococcus strains (picocyanobacteria) isolated from the Baltic Sea. The ISME Journal 3:397–408. doi:10.1038/ismej.2008.118
15. D.P.R.Herlemann, M.Labrenz, K.Jürgens, S.Bertilsson, J.J.Waniek, A.F.Andersson. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. The ISME Journal 5:1571–79. doi:10.1038/ismej.2011.41
16. I.Hewson, S.R.Govil, D.G.Capone, E.J.Carpenter, J.A.Fuhrman. 2004. Evidence of Trichodesmium viral lysis and potential significance for biogeochemical cycling in the oligotrophic ocean. Aquatic Microbial Ecology 36:1–8. doi:10.3354/ame036001
17. K.Holmfeldt, M.Middelboe, O.Nybroe, L.Riemann. 2007. Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Applied and Environmental Microbiology 73:6730–39. doi:10.1128/AEM.01399-07
18. K.Holmfeldt, J.Titelman, L.Riemann. 2010. Virus production and lysate recycling in different sub-basins of the northern Baltic Sea. Microbial Ecology 60:572–80. doi:10.1007/s00248-010-9668-8
19. K.Holmfeldt, D.Odić, M.B.Sullivan, M.Middelboe, L.Riemann. 2012. Cultivated single-stranded DNA phages that infect marine Bacteroidetes prove difficult to detect with DNA-binding stains. Applied and Environmental Microbiology 78:892–94. doi:10.1128/AEM.06580-11
20. K.Holmfeldt, N.Solonenko, M.Shah, K.Corrier, L.Riemann, N.C.VerBerkmoes, M.B.Sullivan. 2013. Twelve previously unknown phage genera are ubiquitous in global oceans. Proceedings of the National Academy of Sciences 110:12798–803. doi:10.1073/pnas.1305956110
21. K.Holmfeldt, C.Howard-Varona, N.Solonenko, M.B.Sullivan. 2014. Contrasting genomic patterns and infection strategies of two co-existing Bacteroidetes podovirus genera. Environmental Microbiology 16:2501–13. doi:10.1111/1462-2920.12391
22. K.Ininbergs, B.Bergman, J.Larsson, M.Ekman. 2015. Microbial metagenomics in the Baltic Sea: recent advancements and prospects for environmental monitoring. Ambio 44:439–50. doi:10.1007/s13280-015-0663-7
23. M.Jakubowska-Deredas, A.Jurczak-Kurek, M.Richert, M.Loś, M.Narajczyk, B.Wróbel. 2012. Diversity of tailed phages in Baltic Sea sediment: large number of siphoviruses with extremely long tails. Research in Microbiology 163:292–96. doi:10.1016/j.resmic.2012.02.002
24. C.A.Jenkins, P.K.Hayes. 2006. Diversity of cyanophages infecting the heterocystous filamentous cyanobacterium Nodularia isolated from the brackish Baltic Sea. Journal of the Marine Biological Association of the United Kingdom 86:529–36. doi:10.1017/S0025315406013439
25. D.L.Kirchman. 2002. The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiology Ecology 39:91–100.
26. M.Labrenz, G.Jost, K.Jürgens. 2007. Distribution of abundant prokaryotic organisms in the water column of the central Baltic Sea with an oxic-anoxic interface. Aquatic Microbial Ecology 46:177–90. doi:10.3354/ame046177
27. J.Larsson, N.Celepli, K.Ininbergs, C.L.Dupont, S.Yooseph, B.Bergman, 2014. Picocyanobacteria containing a novel pigment gene cluster dominate the brackish water Baltic Sea. The ISME Journal 8:1892–903. doi:10.1038/ismej.2014.35
28. C.Leitet, L.Riemann, Å.Hagström. 2006. Plasmids and prophages in Baltic Sea bacterioplankton isolates. Journal of the Marine Biological Association of the UK 86:567–75. doi:10.1017/S0025315406013488
29. C.Lønborg, M.Middelboe, C.P.D.Brussaard. 2013. Viral lysis of Micromonas pusilla: impacts on dissolved organic matter production and composition. Biogeochemistry 116:231–40. doi:10.1007/s10533-013-9853-1
30. A.M.Luhtanen, E.Eronen-Rasimus, H.Kaartokallio, J.M.Rintala, R.Autio, E.Roine. 2014. Isolation and characterization of phage-host systems from the Baltic Sea ice. Extremophiles 18:121–30. doi:10.1007/s00792-013-0604-y
31. L.C.M.Mackinder, C.A.Worthy, G.Biggi, M.Hall, K.P.Ryan, A.Varsani, 2009. A unicellular algal virus, Emiliania huxleyi virus 86, exploits an animal-like infection strategy. Journal of General Virology 90:2306–16. doi:10.1099/vir.0.011635-0
32. R.Maranger, D.Bird. 1995. Viral abundance in aquatic systems: A comparison between marine and fresh waters. Marine Ecology Progress Series 121:217–26. doi:10.3354/meps121217
33. J.Martínez Martínez, A.Boere, I.Gilg, J.Van Lent, H.Witte, J.Van Bleijswijk, C.P.D.Brussaard. 2015. New lipid envelope-containing dsDNA virus isolates infecting Micromonas pusilla reveal a separate phylogenetic group. Aquatic Microbial Ecology 74:17–28. doi:10.3354/ame01723
34. M.Middelboe, K.Holmfeldt, L.Riemann, O.Nybroe, J.Haaber. 2009. Bacteriophages drive strain diversification in a marine Flavobacterium: implications for phage resistance and physiological properties. Environmental Microbiology 11:1971–82. doi:10.1111/j.1462-2920.2009.01920.x
35. K.Moebus, H.Nattkemper. 1983. Taxonomic investigations of bacteriophage sensitive bacteria isolated from marine waters. Helgoland Marine Research 36:357–73.
36. K.D.A.Mojica, C.P.D.Brussaard. 2014. Factors affecting virus dynamics and microbial host-virus interactions in marine environments. FEMS Microbiology Ecology 89:495–515. doi:10.1111/1574-6941.12343
37. N.H.Motwani, E.Gorokhova. 2013. Mesozooplankton grazing on picocyanobacteria in the Baltic Sea as inferred from molecular diet analysis. PLoS ONE 8:e79230. 8 pages. doi:10.1371/journal.pone.0079230
38. T.Neumann, K.Eilola, B.Gustafsson, B.Müller-Karulis, I.Kuznetsov, H.E.M.Meier, 2012. Extremes of temperature, oxygen and blooms in the Baltic Sea in a changing climate. Ambio 41:574–85. doi:10.1007/s13280-012-0321-2
39. K.Olli, R.Klais, T.Tamminen. 2015. Rehabilitating the cyanobacteria – niche partitioning, resource use efficiency, and phytoplankton community structure during diazotrophic cyanobacterial blooms. Journal of Ecology 103:1153–64. doi:10.1111/1365-2745.12437
40. L.Riemann, K.Holmfeldt, J.Titelman. 2009. Importance of viral lysis and dissolved DNA for bacterioplankton activity in a P-limited estuary, Northern Baltic Sea. Microbial Ecology 57:286–94. doi:10.1007/s00248-008-9429-0
41. E.Sahlsten. 1998. Seasonal abundance in Skagerrak-Kattegat coastal waters and host specificity of viruses infecting the marine photosynthetic flagellate Micromonas pusilla. Aquatic Microbial Ecology 16:103–08. doi:10.3354/ame016103
42. L.Scharnreitner. 2013. Virus Production in the Baltic Sea. Master's Thesis. University of Vienna, Austria: Department of Marine Biology. 43 pages.
43. A.Senčilo, A.M.Luhtanen, M.Saarijärvi, D.H.Bamford, E.Roine. 2014. Cold-active bacteriophages from the Baltic Sea ice have diverse genomes and virus-host interactions. Environmental Microbiology 10:3628–41.
44. S.Suikkanen, H.Kaartokallio, S.Hällfors, M.Huttunen, M.Laamanen. 2010. Life cycle strategies of bloom-forming, filamentous cyanobacteria in the Baltic Sea. Deep Sea Research II 57:199–209. doi:10.1016/j.dsr2.2009.09.014
45. S.Šulčius, J.Staniulis, R.Paškauskas. 2011. Morphology and distribution of phage-like particles in a eutrophic boreal lagoon. Oceanologia 53:587–603. doi:10.5697/oc.53-2.587
46. S.Šulčius, J.Staniulis, R.Paškauskas, I.Olenina, A.Salytė, A.Ivanauskaitė, 2014. Absence of evidence for viral infection in colony-embedded cyanobacterial isolates from the Curonian Lagoon. Oceanologia 56:651–60.
47. S.Šulčius, G.Alzbutas, K.Kvederavičiūtė, J.Koreivienė, L.Zakrys, A.Lubys, R.Paškauskas. 2015a. Draft genome sequence of the cyanobacterium Aphanizomenon flos-aquae strain 2012/KM1/D3, isolated from the Curonian Lagoon (Baltic Sea). Genome Announcements 3:e01392–14. 2 pages. doi: 10.1128/genomeA.01392-14
48. S.Šulčius, E.Šimoliunas, J.Staniulis, J.Koreivienė, P.Baltrušis, R.Meškys, 2015b. Characterization of a lytic cyanophage that infects the bloom-forming cyanobacterium Aphanizomenon flos-aquae. FEMS Microbiology Ecology 91:1–7. doi:10.1093/femsec/fiu012
49. M.B.Sullivan, J.B.Waterbury, S.W.Chisholm. 2003. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424:1047–51. doi:10.1038/nature01929
50. P.Thureborn, D.Lundin, J.Plathan, A.M.Poole, B.M.Sjöberg, S.Sjöling. 2013. A metagenomics transect into the deepest point of the Baltic Sea reveals clear stratification of microbial functional capacities. PLoS ONE 8:e74983. 11 pages. doi:10.1371/journal.pone.0074983
51. P.Tuomi, P.Kuuppo. 1999. Viral lysis and grazing loss of bacteria in nutrient- and carbon-manipulated brackish water enclosures. Journal of Plankton Research 21:923–37. doi:10.1093/plankt/21.5.923
52. P.Tuomi, C.Lundsgaard, J.Ekebom, K.Olli, K.Künnis. 1999. The production and potential loss mechanisms of bacterial biomass in the southern Gulf of Riga. Journal of Marine Systems 23:185–96. doi:10.1016/S0924-7963(99)00057-3
53. M.G.Weinbauer, C.Winter, M.G.Höfle. 2002. Reconsidering transmission electron microscopy based estimates of viral infection of bacterioplankton using conversion factors derived from natural communities. Aquatic Microbial Ecology 27:103–10. doi:10.3354/ame027103
54. M.G.Weinbauer, I.Brettar, M.G.Höffle. 2003. Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnology and Oceanography 48:1457–65. doi:10.4319/lo.2003.48.4.1457
55. W.H.Wilson, I.R.Joint, N.G.Carr, N.H.Mann. 1993. Isolation and molecular characterization of five marine cyanophages propagated on Synechococcus sp. strain WH7803. Applied and Environmental Microbiology 59:3736–43.
56. B.H.Yeo, K.Y.Gin. 2013. Cyanophages infecting Anabaena circinalis and Anabaena cylindrica in a tropical reservoir. Bacteriophage 3:e25571. 7 pages. doi:10.4161/bact.25571
57. A.Zakrisson, U.Larsson, H.Höglander. 2014. Do Baltic Sea diazotrophic cyanobacteria take up combined nitrogen in situ? Journal of Plankton Research 36:1368–80. doi:10.1093/plankt/fbu053