Viral Control of Phytoplankton Populations—a Review1
Abstract
ABSTRACT. Phytoplankton population dynamics are the result of imbalances between reproduction and losses. Losses include grazing, sinking, and natural mortality. As the importance of microbes in aquatic ecology has been recognized, so has the potential significance of viruses as mortality agents for phytoplankton. The field of algal virus ecology is steadily changing and advancing as new viruses are isolated and new methods are developed for quantifying the impact of viruses on phytoplankton dynamics and diversity. With this development, evidence is accumulating that viruses can control phytoplankton dynamics through reduction of host populations, or by preventing algal host populations from reaching high levels. The identification of highly specific host ranges of viruses is changing our understanding of population dynamics. Viral‐mediated mortality may not only affect algal species succession, but may also affect intraspecies succession. Through cellular lysis, viruses indirectly affect the fluxes of energy, nutrients, and organic matter, especially during algal bloom events when biomass is high. Although the importance of viruses is presently recognized, it is apparent that many aspects of viral‐mediated mortality of phytoplankton are still poorly understood. It is imperative that future research addresses the mechanisms that regulate virus infectivity, host resistance, genotype richness, abundance, and the fate of viruses over time and space.
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Microalgal growth facilities can be an excellent habitat for undesirable guests, which in most cases are detrimental for algal growth by acting as competitors, parasites or predators.
“Microalgal growth facilities can be an excellent habitat for a wide variety of undesirable guests. In most cases, these will be detrimental for algal growth by acting as competitors (other algae with low oil production or bacteria), parasites (virus, fungus or protozoans) or predators (protozoans, fungus or aquatic invertebrates [54–57].”
From Biofuels from algae: Challenges and potential (2010) · cites this paper as [54]
Cites
The Ecological Role of Water-Column Microbes in the Sea
Azam, F., Fenchel, T., Field, J., Gray, J. S., Meyer-Reil, L., & Thingstad, T. F. (1983) · Marine Ecology Progress Series · doi:10.3354/meps010257 · Cited by 5,398 · see citing works
The Minimal Gene Complement of <i>Mycoplasma genitalium</i>
Fraser, C. M., Gocayne, J. D., White, O., Adams, M. D., Clayton, R. A., Fleischmann, R. D., Bult, C. J., Kerlavage, A. R., Sutton, G., Kelley, J. M., et al. (1995) · Science · doi:10.1126/science.270.5235.397 · Cited by 2,545 · see citing works
A review of harmful algal blooms and their apparent global increase
Hallegraeff, G. M. (1993) · Phycologia · doi:10.2216/i0031-8884-32-2-79.1 · Cited by 2,466 · see citing works
Marine viruses and their biogeochemical and ecological effects
Fuhrman, J. A. (1999) · Nature · doi:10.1038/21119 · Cited by 2,257 · see citing works
Virioplankton: Viruses in Aquatic Ecosystems
Wommack, K. E., & Colwell, R. R. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.1.69-114.2000 · Cited by 2,153 · see citing works
High abundance of viruses found in aquatic environments
Bergh, Ø., Børsheim, K. Y., Bratbak, G., & Heldal, M. (1989) · Nature · doi:10.1038/340467a0 · Cited by 1,650 · see citing works
The ecology of cyanobacteria: their diversity in time and space.
Whitton, B. A., & Potts, M. (2000) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-46855-7 · Cited by 1,429 · see citing works
Viruses and Nutrient Cycles in the Sea
Wilhelm, S. W., & Suttle, C. A. (1999) · BioScience · doi:10.2307/1313569 · Cited by 1,263 · see citing works
Estimating the grazing impact of marine micro-zooplankton
Landry, M. R., & Hassett, R. P. (1982) · Marine Biology · doi:10.1007/bf00397668 · Cited by 1,243 · see citing works
Thingstad, T. F. (2000) · Limnology and Oceanography · doi:10.4319/lo.2000.45.6.1320 · Cited by 1,085 · see citing works
Viral mortality of marine bacteria and cyanobacteria
Proctor, L. M., & Fuhrman, J. A. (1990) · Nature · doi:10.1038/343060a0 · Cited by 1,029 · see citing works
Cloern, J. E. (1996) · Reviews of Geophysics · doi:10.1029/96rg00986 · Cited by 821 · see citing works
Enumeration of Marine Viruses in Culture and Natural Samples by Flow Cytometry
Marie, D., Brussaard, C. P. D., Thyrhaug, R., Bratbak, G., & Vaulot, D. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.1.45-52.1999 · Cited by 646 · see citing works
Self-citationUse of active fluorescence to estimate phytoplankton photosynthesis in situ
Kolber, Z., & Falkowski, P. G. (1993) · Limnology and Oceanography · doi:10.4319/lo.1993.38.8.1646 · Cited by 611 · see citing works
The Encyclopedia of life sciences
(2002) · Choice Reviews Online · doi:10.5860/choice.39sup-0266 · Cited by 583 · see citing works
On the diets of calanoid copepods
Kleppel, G. S. (1993) · Marine Ecology Progress Series · doi:10.3354/meps099183 · Cited by 567 · see citing works
Infection of phytoplankton by viruses and reduction of primary productivity
Suttle, C. A., Chan, A. M., & Cottrell, M. T. (1990) · Nature · doi:10.1038/347467a0 · Cited by 548 · see citing works
Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms
Bratbak, G., Egge, J., & Heldal, M. (1993) · Marine Ecology Progress Series · doi:10.3354/meps093039 · Cited by 537 · see citing works
Ecology of Protozoa: The Biology of Free-living Phagotrophic Protists
Fenchel, T. (2014) · Cited by 503 · see citing works
Mechanisms and Rates of Decay of Marine Viruses in Seawater
Suttle, C. A., & Chen, F. (1992) · Applied and Environmental Microbiology · doi:10.1128/aem.58.11.3721-3729.1992 · Cited by 494 · see citing works
Jumars, P. A., Penry, D. L., Baross, J. A., Perry, M. J., & Frost, B. W. (1989) · Deep Sea Research Part A Oceanographic Research Papers · doi:10.1016/0198-0149(89)90001-0 · Cited by 456 · see citing works
Waterbury, J. B., & Valois, F. W. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.10.3393-3399.1993 · Cited by 441 · see citing works
Viruses and viruslike particles of eukaryotic algae
Etten, J. L. V., Lane, L. C., & Meints, R. H. (1991) · Microbiological Reviews · doi:10.1128/mr.55.4.586-620.1991 · Cited by 386 · see citing works
Esteban, G. F., & Fenchel, T. (2020) · Springer eBooks · doi:10.1007/978-3-030-59979-9 · Cited by 368 · see citing works
Dynamics and Distribution of Cyanophages and Their Effect on Marine Synechococcus spp
Suttle, C. A., & Chan, A. M. (1994) · Applied and Environmental Microbiology · doi:10.1128/aem.60.9.3167-3174.1994 · Cited by 324 · see citing works
Suttle, C. A., & Chan, A. M. (1993) · Marine Ecology Progress Series · doi:10.3354/meps092099 · Cited by 323 · see citing works
Virus decay and its causes in coastal waters
Noble, R. T., & Fuhrman, J. A. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.1.77-83.1997 · Cited by 320 · see citing works
Release and bioavailability of C, N, P Se, and Fe following viral lysis of a marine chrysophyte
Gobler, C. J., Hutchins, D. A., Fisher, N. S., Cosper, E. M., & Sañudo‐Wilhelmy, S. A. (1997) · Limnology and Oceanography · doi:10.4319/lo.1997.42.7.1492 · Cited by 317 · see citing works
Viruses in Marine Planktonic Systems
Fuhrman, J. A., & Suttle, C. A. (1993) · Oceanography · doi:10.5670/oceanog.1993.14 · Cited by 315 · see citing works
van Hannen, E. J., Zwart, G., van Agterveld, M. P., et al. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.2.795-801.1999 · Cited by 311 · see citing works
Murray, A. G., & Jackson, G. (1992) · Marine Ecology Progress Series · doi:10.3354/meps089103 · Cited by 307 · see citing works
Species differences in accumulation of nitrogen pools in phytoplankton
Dortch, Q., Clayton, J. R., Thoresen, S. S., & Ahmed, S. I. (1984) · Marine Biology · doi:10.1007/bf00393218 · Cited by 299 · see citing works
Flow cytometric detection of viruses
Brussaard, C. P. D., Marie, D., & Bratbak, G. (2000) · Journal of Virological Methods · doi:10.1016/s0166-0934(99)00167-6 · Cited by 288 · see citing works
Self-citationGrazing by marine nanofiagellates on viruses and virus-sized particles: ingestion and digestion
Grau, J. M. G., & Suttle, C. A. (1993) · Marine Ecology Progress Series · doi:10.3354/meps094001 · Cited by 272 · see citing works
Wilhelm, S. W., BRIGDEN, S. M., & Suttle, C. A. (2002) · Microbial Ecology · doi:10.1007/s00248-001-1021-9 · Cited by 267 · see citing works
Bacterial Growth Rate and Marine Virus–Host Dynamics
Middelboe, M. (2000) · Microbial Ecology · doi:10.1007/s002480000050 · Cited by 253 · see citing works
Brussaard, C. P. D., Riegman, R., Noordeloos, A., et al. (1995) · Marine Ecology Progress Series · doi:10.3354/meps123259 · Cited by 236 · see citing works
Self-citationWilson, W. H., Carr, N. G., & Mann, N. H. (1996) · Journal of Phycology · doi:10.1111/j.0022-3646.1996.00506.x · Cited by 233 · see citing works
Tilman, D., Mattson, M. D., & Langer, S. (1981) · Limnology and Oceanography · doi:10.4319/lo.1981.26.6.1020 · Cited by 232 · see citing works
Etten, J. L. V., & Meints, R. H. (1999) · Annual Review of Microbiology · doi:10.1146/annurev.micro.53.1.447 · Cited by 227 · see citing works
Wommack, K. E., Ravel, J., Hill, R. T., et al. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.1.231-240.1999 · Cited by 217 · see citing works
Dortch, Q. (1982) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/0022-0981(82)90072-7 · Cited by 216 · see citing works
Roles of viral infection in organic particle flux
Proctor, L., & Fuhrman, J. A. (1991) · Marine Ecology Progress Series · doi:10.3354/meps069133 · Cited by 212 · see citing works
Growth cycle of a virus, PBCV-1, that infects Chlorella-like algae
Etten, J. L. V., Burbank, D. E., Xia, Y., et al. (1983) · Virology · doi:10.1016/0042-6822(83)90466-x · Cited by 210 · see citing works
Regeneration of dissolved organic matter by viral lysis in marine microbial communities
Middelboe, M., & Lyck, P. (2002) · Aquatic Microbial Ecology · doi:10.3354/ame027187 · Cited by 198 · see citing works
Principles of Virology: Molecular Biology, Pathogenesis, and Control
Flint, S. J., Enquist, L. W., Krug, R. M., Racaniello, V. R., & Skalka, A. M. (1999) · Medical Entomology and Zoology · Cited by 195 · see citing works
Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection
Jacquet, S., Heldal, M., Iglesias-Rodrı́guez, D., et al. (2002) · Aquatic Microbial Ecology · doi:10.3354/ame027111 · Cited by 189 · see citing works
Schroeder, D. C., Oke, J., Malin, G., et al. (2002) · Archives of Virology · doi:10.1007/s00705-002-0841-3 · Cited by 188 · see citing works
Cottrell, M. T., & Suttle, C. A. (1991) · Marine Ecology Progress Series · doi:10.3354/meps078001 · Cited by 187 · see citing works
Evans, C., Archer, S. D., Jacquet, S., et al. (2003) · Aquatic Microbial Ecology · doi:10.3354/ame030207 · Cited by 186 · see citing works
The role of sunlight in the removal and repair of viruses in the sea
Wilhelm, S. W., Weinbauer, M. G., Suttle, C. A., & Jeffrey, W. H. (1998) · Limnology and Oceanography · doi:10.4319/lo.1998.43.4.0586 · Cited by 178 · see citing works
Fuller, N. J., Wilson, W. H., Joint, I. R., et al. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.6.2051-2060.1998 · Cited by 177 · see citing works
Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea
Brussaard, C. P. D., Kempers, R., Kop, A., et al. (1996) · Aquatic Microbial Ecology · doi:10.3354/ame010105 · Cited by 174 · see citing works
Self-citationAgustı́, S., Satta, M. P., Mura, M. P., & Benavent, E. (1998) · Limnology and Oceanography · doi:10.4319/lo.1998.43.8.1836 · Cited by 173 · see citing works
Epibiotic microorganisms on copepods and other marine crustaceans
Carman, K. R., & Dobbs, F. C. (1997) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19970415)37:2 · Cited by 172 · see citing works
Zhong, Y. W., Chen, F., Wilhelm, S. W., et al. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.4.1576-1584.2002 · Cited by 169 · see citing works
Steward, G. F., Montiel, J. L., & Azam, F. (2000) · Limnology and Oceanography · doi:10.4319/lo.2000.45.8.1697 · Cited by 168 · see citing works
Chen, F., Suttle, C. A., & Short, S. M. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.8.2869-2874.1996 · Cited by 163 · see citing works
Tarutani, K., Nagasaki, K., & Yamaguchi, M. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.11.4916-4920.2000 · Cited by 162 · see citing works
Principles of Virology: Molecular Biology, Pathogenesis, and Control
Webster, R. G. (2001) · JAMA · doi:10.1001/jama.285.7.942-a · Cited by 156 · see citing works
Dynamics of lytic virus infecting the photosynthetic marine picoflagellate Micromonas pusilla
Cottrell, M. T., & Suttle, C. A. (1995) · Limnology and Oceanography · doi:10.4319/lo.1995.40.4.0730 · Cited by 155 · see citing works
Population dynamics and diversity of phytoplankton, bacteria and viruses in a seawater enclosure
Larsen, A., Castberg, T., Sandaa, R., Brussaard, C. P. D., Egge, J., Heldal, M., Paulino, A., Thyrhaug, R., van Hannen, E. J., & Bratbak, G. (2001) · Marine Ecology Progress Series · doi:10.3354/meps221047 · Cited by 154 · see citing works
Self-citationMalin, G., Wilson, W. H., Bratbak, G., Liss, P. S., & Mann, N. H. (1998) · Limnology and Oceanography · doi:10.4319/lo.1998.43.6.1389 · Cited by 151 · see citing works
Suttle, C. A. (2000) · Elsevier eBooks · doi:10.1016/b978-012362675-2/50007-0 · Cited by 150 · see citing works
Rynearson, T. A., & Armbrust, E. V. (2000) · Limnology and Oceanography · doi:10.4319/lo.2000.45.6.1329 · Cited by 149 · see citing works
Sandaa, R., Heldal, M., Castberg, T., et al. (2001) · Virology · doi:10.1006/viro.2001.1161 · Cited by 148 · see citing works
Impact of phytoplankton bloom magnitude on a pelagic microbial food web
Brussaard, C. P. D., Gast, G., van Duyl, F. C., et al. (1996) · Marine Ecology Progress Series · doi:10.3354/meps144211 · Cited by 147 · see citing works
Self-citationISOLATION AND CHARACTERIZATION OF A VIRUS INFECTING PHAEOCYSTIS POUCHETII (PRYMNESIOPHYCEAE)1
Jacobsen, A., Bratbak, G., & Heldal, M. (1996) · Journal of Phycology · doi:10.1111/j.0022-3646.1996.00923.x · Cited by 146 · see citing works
Nagasaki, K., & Yamaguchi, M. (1997) · Aquatic Microbial Ecology · doi:10.3354/ame013135 · Cited by 146 · see citing works
Castberg, T., Larsen, A., Sandaa, R., et al. (2001) · Marine Ecology Progress Series · doi:10.3354/meps221039 · Cited by 144 · see citing works
Mathias, C., Kirschner, A. K. T., & Velimirov, B. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.10.3734-3740.1995 · Cited by 141 · see citing works
A virus which lyses the marine nanoflagellate Micromonas pusilla
Mayer, J. A., & Taylor, F. J. R. (1979) · Nature · doi:10.1038/281299a0 · Cited by 139 · see citing works
Short, S. M., & Suttle, C. A. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.3.1290-1296.2002 · Cited by 137 · see citing works
CHEN, F., & Suttle, C. A. (1996) · Virology · doi:10.1006/viro.1996.0234 · Cited by 131 · see citing works
Stable coexistence in marine algal host-virus systems
Thyrhaug, R., Larsen, A., Thingstad, T., & Bratbak, G. (2003) · Marine Ecology Progress Series · doi:10.3354/meps254027 · Cited by 128 · see citing works
Rapid Virus Production and Removal as Measured with Fluorescently Labeled Viruses as Tracers
Noble, R. T., & Fuhrman, J. A. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.9.3790-3797.2000 · Cited by 127 · see citing works
Cyanophages and Their Role in the Ecology of Cyanobacteria
Suttle, C. A. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-46855-7_20 · Cited by 124 · see citing works
Garza, D. R., & Suttle, C. A. (1998) · Microbial Ecology · doi:10.1007/s002489900115 · Cited by 123 · see citing works
Viral activity in relation to Emiliania huxleyi blooms:a mechanism of DMSP release?
Bratbak, G., Levasseur, M., Michaud, S., et al. (1995) · Marine Ecology Progress Series · doi:10.3354/meps128133 · Cited by 122 · see citing works
Cell viability in natural phytoplankton communities quantified by a membrane permeability probe
Agustı́, S., & Sánchez, M. C. (2002) · Limnology and Oceanography · doi:10.4319/lo.2002.47.3.0818 · Cited by 121 · see citing works
Hill, R., White, B. C., Cottrell, M. T., et al. (1998) · Aquatic Microbial Ecology · doi:10.3354/ame014001 · Cited by 120 · see citing works
Tai, V., Lawrence, J. E., Lang, A. S., et al. (2003) · Journal of Phycology · doi:10.1046/j.1529-8817.2003.01162.x · Cited by 119 · see citing works
Viral mortality in the final stage of Heterosigma akashiwo (Raphidophyceae) red tide
Nagasaki, K., Andô, M., Itakura, S., et al. (1994) · Journal of Plankton Research · doi:10.1093/plankt/16.11.1595 · Cited by 117 · see citing works
Virus production in Phaeocystis pouchetii and its relation to host cell growth and nutrition
Bratbak, G., Jacobsen, A., Heldal, M., et al. (1998) · Aquatic Microbial Ecology · doi:10.3354/ame016001 · Cited by 110 · see citing works
Coveney, M. F., Cronberg, G. T. T., Enell, M., et al. (1977) · Oikos · doi:10.2307/3543288 · Cited by 108 · see citing works
Viral control of Emiliania huxleyi blooms?
Bratbak, G., Wilson, W. H., & Heldal, M. (1996) · Journal of Marine Systems · doi:10.1016/0924-7963(96)00018-8 · Cited by 107 · see citing works
Moestrup, Ø., & Thomsen, H. A. (1974) · PROTOPLASMA · doi:10.1007/bf01275815 · Cited by 105 · see citing works
Loss rates from a lake phytoplankton community1
Jassby, A. D., & Goldman, C. R. (1974) · Limnology and Oceanography · doi:10.4319/lo.1974.19.4.0618 · Cited by 105 · see citing works
Tarutani, K., Nagasaki, K., Itakura, S., & Yamaguchi, M. (2001) · Aquatic Microbial Ecology · doi:10.3354/ame023103 · Cited by 104 · see citing works
Flow cytometric analysis of phytoplankton viability following viral infection
Brussaard, C. P. D., Marie, D., Thyrhaug, R., & Bratbak, G. (2001) · Aquatic Microbial Ecology · doi:10.3354/ame026157 · Cited by 102 · see citing works
Self-citationNagasaki, K., Andô, M., Imai, I., et al. (1994) · Marine Biology · doi:10.1007/bf00349570 · Cited by 102 · see citing works
Weinbauer, M. G., Wilhelm, S. W., Suttle, C. A., & Garza, D. R. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.6.2200-2205.1997 · Cited by 102 · see citing works
Viral lysis of Phaeocystis pouchetii and bacterial secondary production
Bratbak, G., Jacobsen, A., & Heldal, M. (1998) · Aquatic Microbial Ecology · doi:10.3354/ame016011 · Cited by 98 · see citing works
ISOLATION AND CHARACTERIZATION OF A VIRUS THAT INFECTS EMILIANIA HUXLEYI (HAPTOPHYTA)1
Castberg, T., Thyrhaug, R., Larsen, A., et al. (2002) · Journal of Phycology · doi:10.1046/j.1529-8817.2002.02015.x · Cited by 97 · see citing works
Infection of a chlorella-like alga with the virus, PBCV-1: Ultrastructural studies
Meints, R. H., Lee, K., Burbank, D. E., et al. (1984) · Virology · doi:10.1016/0042-6822(84)90358-1 · Cited by 94 · see citing works
Nagasaki, K., Tarutani, K., & Yamaguchi, M. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.3.898-902.1999 · Cited by 94 · see citing works
Processes controlling virus inactivation in coastal waters
Kapuscinski, R. B., & Mitchell, R. (1980) · Water Research · doi:10.1016/0043-1354(80)90084-6 · Cited by 92 · see citing works
Hybridization Analysis of Chesapeake Bay Virioplankton
Wommack, K. E., Ravel, J., Hill, R. T., & Colwell, R. R. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.1.241-250.1999 · Cited by 91 · see citing works
Suttle, C. A., & Chan, A. M. (1995) · Marine Ecology Progress Series · doi:10.3354/meps118275 · Cited by 89 · see citing works
Waters, R. E., & Chan, A. T. (1982) · Journal of General Virology · doi:10.1099/0022-1317-63-1-199 · Cited by 86 · see citing works
van Bleijswijk, J. D. L., Kempers, R. S., Veldhuis, M. J. W., et al. (1994) · Journal of Phycology · doi:10.1111/j.0022-3646.1994.00230.x · Cited by 85 · see citing works
Brussaard, C. P. D., Thyrhaug, R., Marie, D., et al. (1999) · Journal of Phycology · doi:10.1046/j.1529-8817.1999.3550941.x · Cited by 85 · see citing works
Self-citationEffect of colloids on the survival of bacteriophages in seawater
Bitton, G., & MITCHELL, R. (1974) · Water Research · doi:10.1016/0043-1354(74)90159-6 · Cited by 83 · see citing works
Suttle, C. A. (1992) · Marine Ecology Progress Series · doi:10.3354/meps087105 · Cited by 80 · see citing works
Peduzzi, P., & Weinbauer, M. G. (1993) · Limnology and Oceanography · doi:10.4319/lo.1993.38.7.1562 · Cited by 80 · see citing works
Zingone, A. (1999) · Journal of Plankton Research · doi:10.1093/plankt/21.11.2143 · Cited by 79 · see citing works
Sommer, U. J. (1994) · Limnology and Oceanography · doi:10.4319/lo.1994.39.7.1680 · Cited by 79 · see citing works
Strong seasonality in phytoplankton cell lysis in the NW Mediterranean littoral
Agustı́, S., & Duarte, C. M. (2000) · Limnology and Oceanography · doi:10.4319/lo.2000.45.4.0940 · Cited by 75 · see citing works
Lawrence, J. E., Chan, A. M., & Suttle, C. A. (2001) · Journal of Phycology · doi:10.1046/j.1529-8817.2001.037002216.x · Cited by 74 · see citing works
Riemann, L., & Middelboe, M. (2002) · Ophelia · doi:10.1080/00785236.2002.10409490 · Cited by 73 · see citing works
Wilhelm, S. W., Weinbauer, M. G., Suttle, C. A., Pledger, R., & Mitchell, D. (1998) · Aquatic Microbial Ecology · doi:10.3354/ame014215 · Cited by 71 · see citing works
Virus dynamics in a coccolithophore-dominated bloom in the North Sea
Wilson, W. H., Tarran, G. A., & Zubkov, M. V. (2002) · Deep Sea Research Part II Topical Studies in Oceanography · doi:10.1016/s0967-0645(02)00065-6 · Cited by 68 · see citing works
Lawrence, J. E., Chan, A. M., & Suttle, C. A. (2002) · Limnology and Oceanography · doi:10.4319/lo.2002.47.2.0545 · Cited by 68 · see citing works
Gendron, D. (1992) · Marine Ecology Progress Series · doi:10.3354/meps087001 · Cited by 68 · see citing works
Phytoplankton death in the sea
Kirchman, D. L. (1999) · Nature · doi:10.1038/18570 · Cited by 67 · see citing works
Assembly site of the virus PBCV-1 in a Chlorella-like green alga: Ultrastructural studies
Meints, R. H., Lee, K., & Etten, J. L. V. (1986) · Virology · doi:10.1016/0042-6822(86)90448-4 · Cited by 66 · see citing works
Cottrell, M. T., & Suttle, C. A. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.8.3088-3091.1995 · Cited by 65 · see citing works
Nagasaki, K., & Yamaguchi, M. (1998) · Aquatic Microbial Ecology · doi:10.3354/ame015211 · Cited by 63 · see citing works
Viruses and Virus-Like Particles of Freshwater and Marine Eukaryotic Algae — a Review
Reißer, W. (1993) · Archiv für Protistenkunde · doi:10.1016/s0003-9365(11)80293-9 · Cited by 61 · see citing works
Sunlight-induced DNA damage and resistance in natural viral communities
Weinbauer, M. G., Wilhelm, S. W., Suttle, C. A., et al. (1999) · Aquatic Microbial Ecology · doi:10.3354/ame017111 · Cited by 60 · see citing works
Intra-species host specificity of HaV (Heterosigma akashiwo virus) clones
Nagasaki, K., & Yamaguchi, M. (1998) · Aquatic Microbial Ecology · doi:10.3354/ame014109 · Cited by 60 · see citing works
Using light scatter signal to estimate bacterial biovolume by flow cytometry
Bouvier, T. C., Troussellier, M., Anzil, A., Courties, C., & Servais, P. (2001) · Cytometry · doi:10.1002/1097-0320(20010701)44:3 · Cited by 55 · see citing works
Sahlsten, E. (1998) · Aquatic Microbial Ecology · doi:10.3354/ame016103 · Cited by 55 · see citing works
Phytoplankton exudation: exploitation of the microbial loop as a defence against algal viruses
Murray, A. G. (1995) · Journal of Plankton Research · doi:10.1093/plankt/17.5.1079 · Cited by 53 · see citing works
Processes controlling virus inactivation in seawater
Mitchell, R., & Jannasch, H. W. (1969) · Environmental Science & Technology · doi:10.1021/es60033a007 · Cited by 52 · see citing works
Juneau, P., Lawrence, J., Suttle, C. A., et al. (2003) · Aquatic Microbial Ecology · doi:10.3354/ame031009 · Cited by 52 · see citing works
The classification and nomenclature of viruses
Fenner, F. J., & Maurin, J. (1976) · Archives of Virology · doi:10.1007/bf01317843 · Cited by 48 · see citing works
Natural Inactivation of Enteric Viruses in Seawater
Gironés, R., Jofre, J., & Bosch, A. (1989) · Journal of Environmental Quality · doi:10.2134/jeq1989.00472425001800010006x · Cited by 46 · see citing works
Short, S. M., & Suttle, C. A. (1999) · Springer eBooks · doi:10.1007/978-94-011-4201-4_3 · Cited by 44 · see citing works
Gastrich, M. D., Anderson, O. R., Benmayor, S. S., & Cosper, E. M. (1998) · Phycologia · doi:10.2216/i0031-8884-37-4-300.1 · Cited by 40 · see citing works
Virus-like particles in three species of phytoplankton from San Juan Island, Washington
Pienaar, R. N. (1976) · Phycologia · doi:10.2216/i0031-8884-15-2-185.1 · Cited by 37 · see citing works
Murray, A. E., & Jackson, G. (1993) · Marine Ecology Progress Series · doi:10.3354/meps095105 · Cited by 35 · see citing works
Barker, G., Green, J. C., Hayes, P. K., et al. (1994) · Sarsia · doi:10.1080/00364827.1994.10413562 · Cited by 32 · see citing works
Short, S. M., & Suttle, C. A. (1999) · Hydrobiologia · doi:10.1023/a:1003711115967 · Cited by 31 · see citing works
Chen, F., & Suttle, C. A. (1995) · PubMed · Cited by 27 · see citing works
Murray, A. G., & Jackson, G. (1993) · Marine Ecology Progress Series · doi:10.3354/meps102105 · Cited by 26 · see citing works
CELL CYCLE DEPENDENT VIRUS PRODUCTION IN MARINE PHYTOPLANKTON1
Thyrhaug, R., Larsen, A., Brussaard, C. P. D., et al. (2002) · Journal of Phycology · doi:10.1046/j.1529-8817.2002.01154.x · Cited by 24 · see citing works
Self-citationSeaton, G., Lee, K., & Rohozinski, J. (1995) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.4.1431 · Cited by 22 · see citing works
The use of dissolved esterase activity as a tracer of phytoplankton lysis
Riegman, R., van Bleijswijk, J. D. L., & Brussaard, C. P. D. (2002) · Limnology and Oceanography · doi:10.4319/lo.2002.47.3.0916 · Cited by 21 · see citing works
Self-citationVirus–like particles and endophytic bacteria in Paraphysomonas and Chromophysomonas (Chrysophyceae)
Preisig, H. R., & Hibberd, D. J. (1984) · Nordic Journal of Botany · doi:10.1111/j.1756-1051.1984.tb01499.x · Cited by 21 · see citing works
Effects of photosynthetic inhibitors and light-dark regimes on the replication of cyanophage SM-2
Benson, R. L., & Martin, E. L. (1981) · Archives of Microbiology · doi:10.1007/bf00455355 · Cited by 17 · see citing works
ENTRY OF A CHLORELLA‐VIRUS INTO ITS HOST CELL1
Reißer, W., & Kapaun, E. (1991) · Journal of Phycology · doi:10.1111/j.0022-3646.1991.00609.x · Cited by 12 · see citing works
Domestication of Eucaryotic Microalgal Viruses from Marine Environments.
Nagasaki, K. (2001) · Microbes and Environments · doi:10.1264/jsme2.2001.3 · Cited by 6 · see citing works
Phytoplankton cell lysis and its ecological implocations
Brussaard, C. P. D. (1997) · University of Groningen research database (University of Groningen / Centre for Information Technology) · Cited by 1 · see citing works
Self-citationRapid virus production and removal as measured with fluorescently labeled viruses as tracers
Fuhrman, J. A., & Noble, R. T. (2022) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/pncm-nm34 · Cited by 1 · see citing works
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Biofuels from algae: Challenges and potential
Hannon, M., Gimpel, J., Tran, M., Rasala, B., & Mayfield, S. (2010) · Biofuels · doi:10.4155/bfs.10.44 · Cited by 813 · see citing works
Parasites and Phytoplankton, with Special Emphasis on Dinoflagellate Infections<sup>1</sup>
PARK, M. G., YIH, W., & COATS, D. W. (2004) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.2004.tb00539.x · Cited by 221 · see citing works
Genomic Insights into Marine Microalgae
Parker, M. S., Mock, T., & Armbrust, E. V. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.42.110807.091417 · Cited by 182 · see citing works
Microalgae culture quality indicators: a review
Elisabeth, B., Rayen, F., & Behnam, T. (2021) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2020.1854672 · Cited by 175 · see citing works
Beacham, T. A., Sweet, J. B., & Allen, M. J. (2017) · Algal Research · doi:10.1016/j.algal.2017.04.028 · Cited by 160 · see citing works
Uyaguari-Diaz, M. I., Chan, M., Chaban, B. L., Croxen, M. A., Finke, J. F., Hill, J. E., Peabody, M. A., Van Rossum, T., Suttle, C. A., Brinkman, F. S. L., et al. (2016) · Microbiome · doi:10.1186/s40168-016-0166-1 · Cited by 104 · see citing works
- Authors
- BRUSSAARD, C. P. D.
- Affiliations
- Royal Netherlands Institute for Sea Research (NL)
- Corresponding author
- BRUSSAARD, CORINA P. D.
- Venue
- Journal of Eukaryotic Microbiology
- Publisher
- Wiley
- Published
- 2004-03
- Volume
- 51
- Issue
- 2
- Pages
- 125-138
- ISSN
- 1066-5234 (ISSN-L)
- 1550-7408
- OpenAlex
- W2159463353
- Cited by
- 501
- References
- 145
- Citations by year
- 2026: 13 · 2025: 10 · 2024: 25 · 2023: 23 · 2022: 33 · 2021: 31 · 2020: 15 · 2019: 23 · 2018: 29 · 2017: 31 · 2016: 21 · 2015: 19 · 2014: 30 · 2013: 19 · 2012: 18
- FWCI
- 2.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Eukaryotic Microbiology (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Topics
- Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
- Physical Sciences › Environmental Science › Environmental Chemistry › Aquatic Ecosystems and Phytoplankton Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Plant and Fungal Interactions Research
- Keywords
- viral shunt, phytoplankton dynamics, algal viruses, host range specificity, algal blooms, algal succession, host resistance, viral infectivity, nutrient cycling
- MeSH terms
- Pest Control, Biological, Phytoplankton, Population Dynamics, Water Microbiology, Ecosystem, Phycodnaviridae, Food Chain, Biodiversity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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