Abstract
A variety of Ross Sea summer pack ice habitats between 66 and 75°S were examined for viruses ≥110 nm capsid diameter. Maximum abundances of these viruses likely to infect eukaryotes were 106–107 ml-1 brine in surface, interior, and bottom habitats and constituted up to 18% of the total (all sizes) viruses. There is abundant ultrastructural evidence for infection of a variety of microheterotrophs and some autotrophs. One station exhibited the classical characteristics of a lower latitude algal bloom with potential viral control. The blooming alga, Pyramimonas tychotreta Daugbjerg 2000, was infected, as were two abundant heterotrophs, Cryothecomonas spp. and an unidentified flagellate, that fed on P. tychotreta. Infections were observed in only one life history stage (multiflagellate cells) of P. tychotreta, suggesting a relationship among virus-induced lysis, life-history stages, physiology, and environmental factors regulating the life cycle. There is good evidence that diatoms are not a likely source of the large viruses, and viruses in general are not a major food source for ice microheterotrophs in summer.
Similar content being viewed by others
References
Ackley SF, Sullivan CW (1994) Physical controls on the development and characteristics of Antarctic sea ice biological communities: a review and synthesis. Deep-Sea Res I 41:1583–1604
Bratbak G, Levasseur M, Michaud S, Cantin G, Fernandez E, Heimdal BR, Heldal M (1995) Viral activity in relation to Emiliania huxleyi blooms: a mechanism of DMSP release? Mar Ecol Prog Ser 128:133–142
Bratbak G, Jacobsen A, Heldal M, Nagasaki K, Thingstad F (1998) Virus production in Phaeocystis pouchetii and its relation to host cell growth and nutrition. Aquat Microb Ecol 16:1-9
Brussaard CPD, Kempers RS, Kop AJ, Riegman R, Heldal M (1996) Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea. Aquat Microb Ecol 10:105–113
Castberg T, Larsen A, Sandaa RA, Brussaard CPD, Egge JK, Heldal M, Thyhaug R, van Hannen EJ, Bratbak G (2001) Microbial population dynamics and diversity during a bloom of the marine coccolithophorid Emiliania huxleyi (Haptophyta). Mar Ecol Prog Ser 221:39–46
Cox GFN, Weeks WF (1983) Equations for determining the gas and brine volumes in sea-ice samples. J Glaciol 29:306–316
Daugbjerg N (2000) Pyramimonas tychotreta, sp. nov. (Prasinophyceae), a new marine species from Antarctica: light and electron microscopy of the motile stage and notes on growth rate. J Phycol 36:160–171
Daugbjerg N, Marchant HJ, Thomsen HA (2000) Life history stages of Pyramimonas tychotreta (Prasinophyceae, Chlorophyta) a marine flagellate from the Ross Sea, Antarctica. Phycol Res 48:199–209
Doane FW, Anderson N (1987) Electron microscopy in diagnostic virology. A practical guide and atlas. Cambridge University Press, Cambridge
Fritsen, CH, Coale S, Neenan D, Gibson A, Garrison D (2001) Biomass, production and microhabitat characteristics near the freeboard of ice floes in the Ross Sea during the austral summer. Ann Glaciol 33:280–286
Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548
Garrison DL, Buck KR (1986) Organism losses during ice melting: A serious bias in sea ice community studies. Polar Biol 6:363–365
Garrison DL, Mathot S (1996) Pelagic and sea ice microbial communities. In: Ross RM, Hofmann EE, Quetin LB (eds) Foundations for ecological research west of the Antarctic Peninsula. Antarct Res Ser 70:155–172
Gastrich MD, Anderson OR, Benmayor SS, Cosper, EM (1998) Ultrastructural analysis of viral infection in the brown-tide alga, Aureococcus anophagefferens (Pelagophyceae). Phycologia 37:300–306
González JM, Suttle CA (1993) Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Mar Ecol Prog Ser 94:1-10
Gowing MM (1993) Large virus-like particles from vacuoles of phaeodarian radiolarians and from other marine samples. Mar Ecol Prog Ser 101:33–43
Gowing MM, Riggs BE, Garrison DL, Gibson AH, Jeffries MO (2002) Large viruses in Ross Sea late autumn pack ice habitats. Mar Ecol Prog Ser 241:1-11
Horner R, Syvertsen EE, Thomas DP, Lange C (1988) Proposed terminology and reporting units for sea ice algal assemblages. Polar Biol 8:249–253
Jacobsen A, Bratbak G, Heldal M (1996) Isolation and characterization of a virus infecting Phaeocystis pouchetii (Prymnesiophyceae). J Phycol 32:923–927
Jacquet S, Heldal M, Iglesias-Rodriguez D, Larsen A, Wilson W, Bratbak G (2002) Flow cytometric analysis of an Emiliania huxleyi bloom terminated by viral infection. Aquat Microb Ecol 27:111–124
Jeffries MO and Adolphs U (1997) Early winter ice and snow thickness distribution, ice structure and development of the western Ross Sea pack ice between the ice edge and the Ross Ice Shelf. Antarct Sci 9:188–200
Jeffries MO, Krouse HR, Hurst-Cushing B, Maksym T (2001) Snow ice accretion and snow cover depletion on Antarctic first-year sea ice floes. Ann Glaciol 33:51–60
Karl DM, Christian JR, Dore JE, Letelier RM (1996) Microbiological oceanography in the region west of the Antarctic Peninsula: Microbial dynamics, nitrogen cycle and carbon flux. In: Ross RM, Hofmann EE, Quetin LB (eds) Foundations for ecosystem research west of the Antarctic Peninsula. Antarct Res Ser 70:303–332
Kepner RL, Wharton RA, Suttle CA (1998) Viruses in Antarctic lakes. Limnol Oceanogr 43:1754–1761
Lagerheim G (1893) Phaeocystis, nov. gen., grundadt p. Tetraspora Poucheti Har. Bot Not 1893:12–33
Lawrence JE, Chan A, Suttle CA (2001) A novel virus (HaNIV) causes lysis of the toxic bloom-forming alga Heterosigma akashiwo (Raphidophyceae). J Phycol 37:216–222
Lipscomb DL, Riordan GP (1995) Ultrastructural examination of virus-like particles in a marine rhizopod (Sarcodina, Protista). Acta Protozool 34:35–44
Lizotte MP (2001) The contributions of sea ice algae to Antarctic marine primary production. Am Zool 41:57–73
Lund JWG, Kipling C, LeCren ED (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:143–170
Maranger R, Bird DF, Juniper SK (1994) Viral and bacterial dynamics in Arctic sea ice during the spring algal bloom near Resolute, N.W.T., Canada. Mar Ecol Prog Ser 111:121–127
Marchant HJ, Scott, FJ (1993) Uptake of sub-micrometre particles and dissolved organic material by Antarctic choanoflagellates. Mar Ecol Prog Ser 92:59–64.
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
McFadden GI, Hill DR, Wetherbee R (1986) A study of the genus Pyramimonas (Prasinophyceae) from southeastern Australia. Nord J Bot 6:209–234
Moestrup Ø, Thomsen HA (1974) An ultrastructural study of the flagellate Pyramimonas orientalis with particular emphasis on Golgi apparatus activity and the flagellar apparatus. Protoplasma 81:247–269
Nagasaki K, Ando M, Imai I, Itakura S, Ishida Y (1993) Virus-like particles in an apochlorotic flagellate in Hiroshima Bay, Japan. Mar Ecol Prog Ser 96:307–310
Nagasaki K, Ando M, Imai I, Itakura S, Ishida Y (1995a) Virus-like particles in unicellular apochlorotic microorganisms in the coastal water of Japan. Fish Sci 61:235–239
Nagasaki K, Imai I, Itakura S, Ando M, Ishida Y (1995b) Viral infection in Heterosigma akashiwo (Raphidophyceae): A possible termination mechanism of the noxious red tide. In: Lassus P, Arzul G, Erard E, Gentien P, Marcaillou C (eds) Harmful marine algal blooms. Lavoisier Intercept, New York, pp 639–644
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
Palmisano AC, Garrison DL (1993) Microorganisms in Antarctic sea ice. In: Friedmann IE (ed) Antarctic Microbiology. Wiley-Liss, New York, pp 167–218
Parkinson CL (1992) Interannual variability of monthly Southern Ocean sea ice distributions. J Geophys Res 97:5349–5363
Proctor LM (1997) Advances in the study of marine viruses. Microsc Res Tech 37:136–161
Proctor LM, Okubo A, Fuhrman JA (1993) Calibrating estimates of phage-induced mortality in marine bacteria: ultrastructural studies of marine bacteriophage development from one-step growth experiments. Microb Ecol 25:161–182
Reisser W (1993) Viruses and virus-like particles of freshwater and marine eukaryotic algae: a review. Arch Protistenkd 143:257–265
Rousseau V, Vaulot D, Casotti R, Lenz J, Gunkel J, Baumann M (1994) The life cycle of Phaeocystis (Prymnesiophyceae): evidence and hypotheses. J Mar Syst 5:23–29
Sandaa RA, Heldal M, Castberg T, Thyrhaug R, Bratbak G (2001) Isolation and characterization of two viruses with large genome size infecting Chrysochromulina ericina (Prymnesiophyceae) and Pyramimonas orientalis (Prasinophyceae). Virology 290:272–280
Sieburth JMcN, Johnson PW, Hargraves PE (1988) Ultrastructure and ecology of Aureococcus anophagefferens gen. nov. (Chrysophyceae): the dominant phytoplankter during a bloom in Narragansett Bay, Rhode Island, Summer 1985. J Phycol 24:416–425
Spurr AR (1969) A low-viscosity epoxy resin for embedding medium for electron microscopy. J Ultrastruct Res 26:31–49
Steward GF, Smith DC, Azam F (1996) Abundance and production of bacteria and viruses in the Bering and Chukchi Seas. Mar Ecol Prog Ser 131:287–300
Suttle CA (1993) Enumeration and isolation of viruses. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Aquatic Microbial Ecology. Lewis, Boca Raton, Fla., pp 121–133
Suttle CA (2000) The ecological, evolutionary and geochemical consequences of viral infection of cyanobacteria and eukaryotic algae. In: Hurst CJ (ed) Viral ecology. Academic Press, London, pp 248–286
Tarutani K, Nagasaki K, Yamaguchi M (2000) Viral impacts on total abundance and clonal composition of the harmful bloom-forming phytoplankton Heterosigma akashiwo. Appl Environ Microbiol 66:4916–4920
Thomas DN, Dieckmann GS (2002) Antarctic sea ice-a habitat for extremophiles. Science 295:641–644
Thomsen H (1992) Plankton i de indre danske farvande. Havforskning fra miljøstyrelsen, Nr. 11. Miljøministeriet Miljøstyrelsen, Copenhagen
Thomsen HA, Buck KR, Bolt PA, Garrison DL (1991) Fine structure and biology of Cryothecomonas gen. nov. (Protista incerta sedis) from the ice biota. Can J Zool 69:1048–1070
Van Etten JL, Lane LC, Meints RH (1991) Viruses and viruslike particles of eukaryotic algae. Microbiol Rev 55:586–620
Vørs N (1992) Heterotrophic amoebae, flagellates and Heliozoa from the Tvärminne area, Gulf of Finland, in 1998–1990. Ophelia 36:1-109
Wilson WH, Lane D, Pearce DA, Ellis-Evans, JC (2000) Transmission electron microscope analysis of virus-like particles in the freshwater lakes of Signy Island, Antarctica. Polar Biol 23:657–660
Wolf S, Müller DG, Maier I (2000) Assembly of a large icosahedral DNA virus, MclaV-1, in the marine alga Myriotrichia clavaeformis (Dictyosiphonales, Phaeophyceae). Eur J Phycol 35:163–171
Wommack KE, Colwell RR (2000) Virioplankton: Viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114
Zingone A (1995) The role of viruses in the dynamics of phytoplankton blooms. G Bot Ital 129:415–423
Acknowledgements
I thank C. Venn and J.N. King for help with sampling and sample processing on the cruise, M.O. Jeffries, J.-L. Tison and S. Nihashi for coring, and C. Fritsen and the BX-325 team for collecting the slush. I thank Chief Scientist M.O. Jeffries, J. Barnes and the ASA team, Capt. J. Borkowski and the officers and crew of the "Nathaniel B. Palmer" and my NBP99–1 colleagues for making the cruise a success. Thanks go to B. Riggs and L.C. Van De Werfhorst for help in the laboratory, to R. Zalpuri of U.C. Berkeley for thin sectioning, to M.O. Jeffries for sharing sea ice physical data, to C. Fritsen et al. for sharing pigment data, and to A. Gibson for discussions on ice community data. Special thanks go to J. Fuhrman, D. Bird, G. Steward and C. Suttle for advice on light microscope preparations, to H. Thomsen, N. Daugbjerg, Ø. Moestrup, and H. Marchant for advice on taxonomy, to R.T. Hinegardner and D.L. Garrison for discussions and reviewing the manuscript, and to two anonymous reviewers for helpful suggestions. This work was supported by National Science Foundation grant OPP-9725136 to M.M. Gowing.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P.W. Sammarco, Chauvin
An erratum to this article is available at http://dx.doi.org/10.1007/s00227-003-1121-9.
Rights and permissions
About this article
Cite this article
Gowing, M.M. Large viruses and infected microeukaryotes in Ross Sea summer pack ice habitats. Marine Biology 142, 1029–1040 (2003). https://doi.org/10.1007/s00227-003-1015-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-003-1015-x