Abstract
The abundance of viral-like particles in marine ecosystems ranges from <104 ml−1 to >108 ml−1. Their distribution in time and space parallels that of other biological parameters such as bacterial abundance and chlorophyll a. There is a lack of consensus between methods used to assess viral activity, i.e., rate of change in viral abundance (increase or decrease). The highest rates, 10–100 days−1, are observed in experiments with short sampling intervals (0.2–2 h), while lower rates, on the order of 1 day−1, are observed in experiments with longer sampling intervals (days). Few studies have been carried out, but viruses appear, at least in some cases, to have a significant impact on carbon and nutrient flow in microbial food webs. Viruses have also been demonstrated to exert a species specific control of both bacteria and phytoplankton populations in natural waters.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Ahrens R (1971) Untersuchungen zur Verbreitung von Phagen der Gattung Agrobacterium in der Ostsee. Kieler Meeresforsch 27:102–112
Anderson A, Lee C, Azam F, Hagström Å (1985) Release of aminoacids and inorganic nutrients by heterotrophic marine microflagellates. Mar Ecol Prog Ser 23:99–106
Bergh Ø, Børsheim KY, Bratbak G, Heldal M (1989). High abundance of viruses found in aquatic environments. Nature (London) 340:467–468
Boehme J, Frisher ME, Jiang SC, Kellogg CA, Pichard S, Rose JB, Steinway C, Paul JH (1993) Viruses, bacterioplankton, and phytoplankton in the southeastern Gulf of Mexico: distribution and contribution to oceanic DNA pools. Mar Ecol Prog Ser 97:1–10
Børsheim KY (1993) Native marine bacteriophages. FEMS Microb Ecol 102:141–159
Børsheim Y, Bratbak G, Heldal H (1990) Enumeration and biomass estimation of planktonic bacteria and viruses by transmission electron microscopy. Appl Environ Microbiol 56:352–366
Bradley DE (1967) Ultrastructure of bacteriophages and bacteriocins. Bacteriol. Rev 31:314–320
Bratbak G, Heldal H, Norland S, Thingstad TF (1990) Viruses as partners in spring bloom microbial trophodynamics. Appl Environ Microbiol 56:1400–1405
Bratbak G, Heldal H, Thingstad TF, Riemann B, Haslund OH (1992) Incorporation of viruses into the budget of microbial C-transfer. A first approach. Mar Ecol Prog Ser 83:273–280
Bratbak G, Egge JK, Heldal M (1993) Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar Ecol Prog Ser 93:39–48
Cannon RE (1987) Cyanophage ecology. In: Goyal SM, Gerba CP, Bitton G (eds) Phage ecology. John Wiley & Sons, New York, pp 137–156
Caron DA, Davis PG, Madin LP, Sieburth JMcN (1986) Enrichment of microbial populations in macroaggregates (marine snow) from surface waters of the North Atlantic. J Mar Res 44:543–565
Cochlan WP, Wikner J, Steward GF, Smith DC, Azam F (1993) Spatial distribution of viruses, bacteria, and chlorophyll a in nertic, oceanic, and estuarine environments. Mar Ecol Prog Ser 92:77–87
Cottrell MT, Suttle CA (1991) Wide-spread occurrence and clonal variation in viruses which cause lysis of a cosmopolitan eucaryotic marine phytoplankter, Micromonas pusilla. Mar Ecol Prog Ser 78:1–9
Dunstall TG, Nalewajko C (1975) Extracellular release in planktonic bacteria. Verh Int Verein Limnol 19:2643–3649
Freifelder G (1987) Microbial genetics. Jones and Bartlett Publishers Inc., Boston
Fuhrman J (1992) Bacterioplankton roles in cycling of organic matter: the microbial food web. In: Falkowski PG, Woodhead AD (eds) Primary productivity and biogeochemical cycles in the sea. Plenum Press, New York, pp 361–383
Fuhrman JA, Suttle CA (1993) Viruses in marine planktonic systems. (Oceanography) 6(2):51–63
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
Hara S, Terauchi K, Koike I (1991) Abundance of viruses in marine waters: assessment by epifluorescence and transmission electron microscopy. Appl Environ Microbiol 57:2731–2734
Heldal M, Bratbak G (1991) Production and decay of viruses in marine waters. Mar Ecol Prog Ser 72:205–212
Hutchinson GE (1961) The paradox of the plankton. Am Nat 95:137–145
Iturriaga R, Zsolnay A (1981) Transformation of some dissolved organic compounds by a natural heterotrophic population. Mar Biol 62:125–129
Kapuscinski RB, Michell R (1980) Processes controlling virus inactivation in coastal waters. Water Res 14:363–371
Lenski RE (1988) Dynamics of interaction between bacteria and virulent bacteriophage. Adv Microb Ecol 10:1–44
Martin E, Benson R (1988) Phages of cyanobacteria. In: Calender R (ed) The bacteriophages, vol 2. Plenum Press, New York, pp 606–645
Maruyama A, Oda M, Higashihara T (1993) Abundance of virus-sized non-DNase-digestible DNA (coated DNA) in eutrophic seawater. Appl Environ Microbiol 59:712–717
Miller RV, Sayler GS (1992) Bacteriophage-host interactions in aquatic systems. In: Wellington EMH, van Elsas JD (eds) Genetic interactions among microorganisms in the natural environment. Pergamon Press, Oxford, pp 176–193
Moebus K (1987) Ecology of marine bacteriophages. In: Goyal SM, Gerba CP, Bitton G (eds) Phage Ecology, John Wiley & Sons, New York, pp 137–156
Moebus K (1992) Laboratory investigations on the survival of marine bacteriophages in raw and treated seawater. Helgoländer Meeresunter 46:251–273
Moebus K (1992) Further investigations on the concentration of marine bacteriophages in the water around Helgoland, with reference to the phage-host systems encountered. Helgoländer Meeresunter 46:275–292
Murray AG, Jackson GA (1992) Viral dynamics: a model of the effects of size, shape, motion, and abundance of single-celled planktonic organisms and other particles. Mar Ecoi Prog Ser 89:103–116
Ogunseitan OA, Sayler GS, Miller RV (1990) Dynamic interactions of Pseudomonas aeruginosa and bacteriophages in lake water. Microb Ecol 19:171–185
Paul JH, DeFlaun MF, Jeffrey WH, David AW (1988) Seasonal and diel variability in dissolved DNA and in microbial biomass and activity in a subtropical estuary. Appl Environ Microbiol 54:718–727
Paul JH, Jiang SC, Rose JB (1991) Concentration of viruses and dissolved DNA from aquatic environments by vortex flow filtration. Appl Environ Microbiol 57:2197–2204
Paul JH, Rose JB, Jiang SC, Kellogg CA, Dickson L (1993) Distribution of viral abundance in the reef environment of Key Largo, Florida. Appl Environ Microbiol 59:718–724
Proctor LM, Fuhrman JA (1990) Viral mortality of marine bacteria and cyanobacteria. Nature (London) 343:60–62
Proctor LM, Fuhrman JA (1991) Roles of viral infection in organic particle flux. Mar Ecol Prog Ser 69:133–142
Proctor LM, Fuhrman JA, Ledbetter MC (1988) Marine bacteriophages and bacterial mortality. EOS 69:1111–1112.
Proctor LM, Okubo A, Fuhrman JH (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 eucaryotic algae—a review. Arch Protistenkd 143:257–265
Sanders RW, Porter KG (1987) Phagotrophic phytoflagellates. In: Marshall KC (ed) Advances in microbial ecology, vol 10. Plenum Press, New York, pp 167–192
Sherr EB (1988) Direct use of high molecular weight polysaccharide by heterotrophic flagellates. Nature (London) 335:348–351
Sieburth JMcN, Johnson PW, Hargraves PE (1988) Ultrastructure and ecology of Aureococcus anophagefferens gen. et sp. nov. (Chrysophyceae): The dominant picoplankter during a bloom in Narragansett Bay, Rhode Island, summer 1985. J Phycol 24:416–425
Stent GS (1963) Molecular biology of bacterial viruses. Freeman and Company, San Francisco
Steward GF, Wikner J, Cochlan WP, Smith DC, Azam F (1992) Estimation of virus production in the sea. II. Field results. Mar Microb Food Webs 6:79–90
Steward GF, Wikner J, Smith DC, Cochlan WP, Azam F (1992) Estimation of virus production in the sea. I. Method development. Mar Microb Food Webs 6:57–78
Stoecker DK, Michaels AE, Davis LH (1987) Large proportion of marine planktonic ciliates found to contain functional chloroplasts. Nature (London) 326:790–793
Suttle CA, Chen F (1992) Mechanisms and rates of decay of marine viruses in seawater. Appl Environ Microbiol 58:3721–3729
Taylor GT, Iturriaga R, Sullivan CW (1985) Interactions of bactivorous grazers and heterotrophic bacteria with dissolved organic matter. Mar Ecol Prog Ser 23:129–141
Torrella F, Morita RY (1979) Evidence for a high incidence of bacteriophage particles in the waters of Yaquina Bay, Oregon: ecological and taxonomical implications. Appl Environ Microbiol 37:774–778
Turley CM, Newell RC, Robins DB (1986) Survival strategies of two small marine ciliates and their role in regulating bacterial community structure under experimental conditions. Mar Ecol Prog Ser 33:59–70
van Etten JL, Lane LC, Meints RH (1991) Viruses and viruslike particles of eucaryotic algae. Microbiol Rev 55:586–620
Wommack KE, Hill RT, Kellel M, Russek-Cohen E, Colwell RR (1992) Distribution of viruses in the Chesapeake Bay. Appl Environ Microbiol 58:2965–2970
Zachary A (1976) Physiology and ecology of bacteriophages in the marine bacterium Beneckea natrigens: salinity. Appl Environ Microbiol 31:415–422
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bratbak, G., Thingstad, F. & Heldal, M. Viruses and the microbial loop. Microb Ecol 28, 209–221 (1994). https://doi.org/10.1007/BF00166811
Issue Date:
DOI: https://doi.org/10.1007/BF00166811