6 – Ecological, Evolutionary, and Geochemical Consequences of Viral Infection of Cyanobacteria and Eukaryotic Algae

This chapter discusses ecological, evolutionary, and geochemical consequences of viral infection of cyanobacteria and eukaryotic algae. In this chapter, algae are treated as a functional group rather than as a taxonomic unit. The primary focus of the chapter is on viruses that infect phytoplankton. The landscape of algal virus ecology is rapidly changing as new viruses are isolated on a regular basis and new methods for quantifying the effect of viruses in the natural environment are developed. This chapter presents taxonomy, morphology, and evolution of algal viruses. It demonstrates that algal viruses are a ubiquitous component of marine and freshwater ecosystems. Viral infection is common in algal populations, and they are extremely important as vectors of genetic information among algal populations in nature. Viruses may have significant effects on pathways of cycling of organic and inorganic nutrients, and may even be involved in the release of greenhouse gases.

[1]  T. O. Diener,et al.  Isolation and characterization of AS-1, a phycovirus infecting the blue-green algae, Anacystis nidulans and Synechococcus cedrorum. , 1972, Virology.

[2]  A. Wood,et al.  Biomass of bacteria, cyanobacteria, prochlorophytes and photosynthetic eukaryotes in the Sargasso Sea , 1992 .

[3]  G. Garabedian,et al.  Virucidal action of sea water. , 1967, American journal of epidemiology.

[4]  M. Weinbauer,et al.  Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the gulf of Mexico , 1996, Applied and environmental microbiology.

[5]  N. J. Lang,et al.  VIRUS‐LIKE PARTICLES AND NUCLEAR INCLUSIONS IN THE RED ALGA PORPHYRIDIUM PURPUREUM (BORY) DREW ET ROSS 1 , 1973 .

[6]  R. Knippers,et al.  Genome structure of a virus infecting the marine brown alga Ectocarpus siliculosus. , 1993, Virology.

[7]  M. Potts,et al.  Host Range of LPP Cyanophages , 1985 .

[8]  K. Nagasaki,et al.  Effect of temperature on the algicidal activity and the stability of HaV (Heterosigma akashiwo virus) , 1998 .

[9]  P. Bisen,et al.  Mutation to resistance for virus AS-1 in the cyanobacterium Anacystis nidulans , 1985 .

[10]  O. Anderson,et al.  Ultrastructural analysis of viral infection in the brown-tide alga, Aureococcus anophagefferens (Pelagophyceae) , 1998 .

[11]  Curtis A. Suttle,et al.  Marine cyanophages infecting oceanic and coastal strains of Synechococcus: abundance, morphology, cross-infectivity and growth characteristics , 1993 .

[12]  R. Benner,et al.  Major biochemical composition of dissolved high molecular weight organic matter in seawater , 1996 .

[13]  M. Cottrell,et al.  Genetic Diversity of Algal Viruses Which Lyse the Photosynthetic Picoflagellate Micromonas pusilla (Prasinophyceae) , 1995, Applied and environmental microbiology.

[14]  R. Haselkorn,et al.  Isolation and characterization of a virus infecting the blue-green alga Nostoc muscorum. , 1971, Virology.

[15]  M. Weinbauer,et al.  MEASUREMENTS OF DNA DAMAGE AND PHOTOREACTIVATION IMPLY THAT MOST VIRUSES IN MARINE SURFACE WATERS ARE INFECTIVE , 1998 .

[16]  Koji Sode,et al.  Induction of a temperate marine cyanophage by heavy metal , 1997 .

[17]  G. Bratbak,et al.  Viral lysis of Phaeocystis pouchetii and bacterial secondary production , 1998 .

[18]  E. Sahlsten.  Seasonal abundance in Skagerrak-Kattegat coastal waters and host specificity of viruses infecting the marine photosynthetic flagellate Micromonas pusilla , 1998 .

[19]  M. Heldal,et al.  Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea , 1996 .

[20]  A. Oppenheim,et al.  Isolation and genetic mapping of temperature-sensitive mutants of cyanophage LPP2-SPI. , 1974, Virology.

[21]  C. Suttle,et al.  Viruses and Nutrient Cycles in the Sea Viruses play critical roles in the structure and function of aquatic food webs , 1999 .

[22]  C. Gobler,et al.  Release and bioavailability of C, N, P Se, and Fe following viral lysis of a marine chrysophyte , 1997 .

[23]  C. Suttle.  Inhibition of photosynthesis in phytoplankton by the submicron size fraction concentrated from seawater , 1992 .

[24]  Alexander G. Murray,et al.  Phytoplankton exudation: exploitation of the microbial loop as a defence against algal viruses , 1995 .

[25]  Jm González,et al.  Grazing by marine nanofiagellates on viruses and virus-sized particles: ingestion and digestion , 1993 .

[26]  C. Emiliani.  Viral extinctions in deep-sea species. , 1993, Nature.

[27]  R. Dulbecco.  Reactivation of Ultra-Violet-Inactivated Bacteriophage by Visible Light , 1949, Nature.

[28]  K. Nagasaki,et al.  Intra-species host specificity of HaV (Heterosigma akashiwo virus) clones , 1998 .

[29]  R. Safferman,et al.  Algal Virus: Isolation , 1963, Science.

[30]  R. Knippers,et al.  Single-stranded regions in the genome of the Ectocarpus siliculosus virus. , 1994, Virology.

[31]  J. V. Van Etten,et al.  Giant viruses infecting algae. , 1999, Annual review of microbiology.

[32]  S. Turner.  Molecular systematics of oxygenic photosynthetic bacteria , 1997 .

[33]  W. H. Wilson,et al.  THE EFFECT OF PHOSPHATE STATUS ON THE KINETICS OF CYANOPHAGE INFECTION IN THE OCEANIC CYANOBACTERIUM SYNECHOCOCCUS SP. WH7803 1 , 1996 .

[34]  C. Suttle,et al.  Genetic diversity in marine algal virus communities as revealed by sequence analysis of DNA polymerase genes , 1996, Applied and environmental microbiology.

[35]  E. Druffel,et al.  Radiocarbon in dissolved organic matter in the central North Pacific Ocean , 1987, Nature.

[36]  A. Wilmotte.  Molecular Evolution and Taxonomy of the Cyanobacteria , 1994 .

[37]  A. Zingone.  The role of viruses in the dynamics of phytoplankton blooms , 1995 .

[38]  G. Bratbak,et al.  ISOLATION AND CHARACTERIZATION OF A VIRUS INFECTING PHAEOCYSTIS POUCHETII (PRYMNESIOPHYCEAE) 1 , 1996 .

[39]  M. Pace,et al.  Bacterial production in fresh and saltwater ecosystems: a cross-system overview , 1988 .

[40]  A. Gibbs,et al.  A tobamovirus of a green alga. , 1975, Virology.

[41]  F. Taylor,et al.  A virus which lyses the marine nanoflagellate Micromonas pusilla , 1979, Nature.

[42]  Jed A. Fuhrman,et al.  Viruses in Marine Planktonic Systems , 1993 .

[43]  R. Lewin,et al.  Photoreactivation of UV-irradiated blue-green algal virus LPP-1. , 1967, Virology.

[44]  R. Haselkorn,et al.  An electron microscope study of infection by the blue-green algal virus SM-1. , 1972, Virology.

[45]  D. Müller,et al.  Intergeneric Infection and Persistence of Ectocarpus Virus DNA in Kuckuckia (Phaeophyceae, Ectocarpales) , 1996 .

[46]  Paul W. Johnson,et al.  ULTRASTRUCTURE AND ECOLOGY OF AUREOCOCCUS ANOPHAGEFERENS GEN. ET SP. NOV. (CHRYSOPHYCEAE): THE DOMINANT PICOPLANKTER DURING A BLOOM IN NARRAGANSETT BAY, RHODE ISLAND, SUMMER 1985 1 , 1988 .

[47]  M. Alexander,et al.  Minimum bacterial density for bacteriophage replication: implications for significance of bacteriophages in natural ecosystems , 1985, Applied and environmental microbiology.

[48]  J. Ito,et al.  Compilation, alignment, and phylogenetic relationships of DNA polymerases. , 1993, Nucleic acids research.

[49]  L. Sherman,et al.  Cyanophages and Viruses of Eukaryotic Algae , 1978 .

[50]  H. Jannasch,et al.  Processes controlling virus inactivation in seawater , 1969 .

[51]  A. M. Chan,et al.  Dynamics and Distribution of Cyanophages and Their Effect on Marine Synechococcus spp , 1994, Applied and environmental microbiology.

[52]  M. Cottrell,et al.  Wide-spread occurrence and clonal variation in viruses which cause lysis of a cosmopolitan, eukaryotic marine phytoplankter Micromonas pusilla , 1991 .

[53]  C. Emiliani.  Extinction and viruses. , 1993, Bio Systems.

[54]  E. Martin,et al.  Phages of Cyanobacteria , 1988 .

[55]  R. Haselkorn,et al.  Growth of the blue-green algae virus LPP-1 under conditions which impair photosynthesis. , 1971, Virology.

[56]  T. Platt,et al.  Autotrophic Picoplankton in the Tropical Ocean , 1983, Science.

[57]  R. Safferman,et al.  Observations on the Occurrence, Distribution, and Seasonal Incidence of Blue-green Algal Viruses. , 1967, Applied microbiology.

[58]  B. Molfino,et al.  Global synchroneity of late Quaternary coccolith datum levels Validation by oxygen isotopes , 1977 .

[59]  J. Hobbie,et al.  Use of nuclepore filters for counting bacteria by fluorescence microscopy , 1977, Applied and environmental microbiology.

[60]  G. Jackson,et al.  Viral dynamics: a model of the effects of size shape, motion and abundance of single-celled olanktonic organisms and other particles , 1992 .

[61]  R. Haselkorn,et al.  Classification and nomenclature of viruses of cyanobacteria. , 1983, Intervirology.

[62]  P. Liss,et al.  Elevated production of dimethylsulfide resulting from viral infection of cultures of Phaeocystis pouchetii , 1998 .

[63]  R. Haselkorn,et al.  Photosynthesis and the development of blue-green algal virus N-1. , 1972, Virology.

[64]  T. Thiel,et al.  UV-inducible DNA repair in the cyanobacteria Anabaena spp , 1987, Journal of bacteriology.

[65]  A. Zachary.  An ecological study of bacteriophages of Vibrio natriegens. , 1978, Canadian journal of microbiology.

[66]  B. Prézelin,et al.  Contribution ofSynechococcus spp. to size-fractioned primary productivity in three water masses in the Northwest Atlantic Ocean , 1986 .

[67]  D. Caron,et al.  The contribution of microorganisms to particulate carbon and nitrogen in surface waters of the Sargasso Sea near Bermuda , 1995 .

[68]  Ronald D. Jones,et al.  Photochemical degradation of dissolved organic carbon and its impact on the oceanic carbon cycle , 1991, Nature.

[69]  P. Hatcher,et al.  Bulk Chemical Characteristics of Dissolved Organic Matter in the Ocean , 1992, Science.

[70]  Use of the polymerase chain reaction and denaturing gradient gel electrophoresis to study diversity in natural virus communities , 1999 .

[71]  M. Weinbauer,et al.  The role of sunlight in the removal and repair of viruses in the sea , 1998 .

[72]  M. Cottrell,et al.  Use of Ultrafiltration To Isolate Viruses from Seawater Which Are Pathogens of Marine Phytoplankton , 1991, Applied and environmental microbiology.

[73]  G. Bratbak,et al.  VIRUS PRODUCTION IN PHAEOCYSTIS POUCHETII AND ITS RELATION TO HOST CELL GROWTH AND NUTRITION , 1998 .

[74]  H. Ducklow,et al.  Oceanic Bacterial Production , 1992 .

[75]  W. Stewart,et al.  Microbial pathogens of cyanophycean blooms , 1977 .

[76]  M. Kim,et al.  A new Synechococcus cyanophage from a reservoir in Korea. , 1994, Virology.

[77]  J. G. Field,et al.  The Ecological Role of Water-Column Microbes in the Sea* , 1983 .

[78]  J. Fuhrman,et al.  Virus decay and its causes in coastal waters , 1997, Applied and environmental microbiology.

[79]  D. Müller,et al.  MOLECULAR SYSTEMATICS OF ECTOCARPUS AND KUCKUCKIA (ECTOCARPALES, PHAEOPHYCEAE) INFERRED FROM PHYLOGENETIC ANALYSIS OF NUCLEAR‐ AND PIASTTD‐ENCODED DNA SEQUENCES , 1997 .

[80]  P. Hearing,et al.  CHARACTERIZATION OF A LYTIC VIRUS INFECTIOUS TO THE BLOOM‐FORMING MICROALGA AUREOCOCCUS ANOPHAGEFFERENS (PELAGOPHYCEAE) , 1998 .

[81]  G. Bratbak,et al.  High abundance of viruses found in aquatic environments , 1989, Nature.

[82]  R. Meints,et al.  THE DNA POLYMERASE GENE OF A BROWN ALGAL VIRUS: STRUCTURE AND PHYLOGENY , 1998 .

[83]  C. Suttle,et al.  Mechanisms and Rates of Decay of Marine Viruses in Seawater , 1992, Applied and environmental microbiology.

[84]  J. Schopf,et al.  Early Archean (3.3-billion to 3.5-billion-year-old) microfossils from Warrawoona Group, Australia. , 1987, Science.

[85]  D. Caron,et al.  CHROOCOCCOID CYANOBACTERIA IN LAKE ONTARIO: VERTICAL AND SEASONAL DISTRIBUTIONS DURING 1982 1 , 1985 .

[86]  K. Børsheim.  Native marine bacteriophages , 1993 .

[87]  E. Padan,et al.  Lysogeny of the blue-green alga Plectonema boryanum by LPP2-SPI cyanophage. , 1972, Virology.

[88]  J. Fuhrman,et al.  Dominance of bacterial biomass in the Sargasso Sea and its ecological implications , 1989 .

[89]  G. Bratbak,et al.  Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms , 1993 .

[90]  S. Turner,et al.  Population Dynamics of Phytoplankton and Viruses in a Phosphate-limited Mesocosm and their Effect on DMSP and DMS Production , 1998 .

[91]  A. M. Chan,et al.  Fluorescently Labeled Virus Probes Show that Natural Virus Populations Can Control the Structure of Marine Microbial Communities , 1995, Applied and environmental microbiology.

[92]  I. Joint,et al.  Occurrence of a Sequence in Marine Cyanophages Similar to That of T4 g20 and Its Application to PCR-Based Detection and Quantification Techniques , 1998, Applied and Environmental Microbiology.

[93]  J. V. Van Etten,et al.  Viruses and viruslike particles of eukaryotic algae , 1991, Microbiological reviews.

[94]  R. Hill,et al.  Effects of sunlight on bacteriophage viability and structure , 1996, Applied and environmental microbiology.

[95]  P. Singh,et al.  Isolation of Cyanophages from India , 1967, Nature.

[96]  J. V. Van Etten,et al.  Chlorella viruses isolated in China , 1988, Applied and environmental microbiology.

[97]  D. Müller.  Mendelian Segregation of a Virus Genome during Host Meiosis in the Marine Brown Alga Ectocarpus siliculosus , 1991 .

[98]  Emilio Fernández,et al.  Viral activity in relation to Emiliania huxleyi blooms: a mechanism of DMSP release? , 1995 .

[99]  K. Nagasaki,et al.  Isolation of a virus infectious to the harmful bloom causing microalga Heterosigma akashiwo (Raphidophyceae) , 1997 .

[100]  Johannessen,et al.  Toxic Algal Bloom in Scandinavian Waters, May–June 1988 , 1989 .

[101]  J. Dodds,et al.  Microscopy and biology of Uronema gigas, a filamentous eucaryotic green alga, and its associated tailed virus-like particle. , 1980, Virology.

[102]  D. I. Taylor,et al.  Subtidal Volume Fluxes, Nutrient Inputs and the Brown Tide—an Alternate Hypothesis , 1994 .

[103]  R. Knippers,et al.  New members of a group of DNA viruses infecting brown algae , 1997 .

[104]  R. Meints,et al.  Repetitive DNA insertion in a protein kinase ORF of a latent FSV (Feldmannia sp. virus) genome. , 1998, Virology.

[105]  J. V. Van Etten,et al.  The DNA polymerase gene from chlorella viruses PBCV-1 and NY-2A contains an intron with nuclear splicing sequences. , 1992, Virology.

[106]  John B. Waterbury,et al.  Resistance to Co-Occurring Phages Enables Marine Synechococcus Communities To Coexist with Cyanophages Abundant in Seawater , 1993, Applied and environmental microbiology.

[107]  Curtis A. Suttle,et al.  Infection of phytoplankton by viruses and reduction of primary productivity , 1990, Nature.

[108]  E. Cosper,et al.  Isolation of Virus Capable of Lysing the Brown Tide Microalga, Aureococcus anophagefferens , 1994, Science.

[109]  I. Joint,et al.  Isolation and Molecular Characterization of Five Marine Cyanophages Propagated on Synechococcus sp. Strain WH7803 , 1993, Applied and environmental microbiology.

[110]  R. Lee.  Systemic viral material in the cells of the freshwater red alga Sirodotia tenuissima (Holden) skuja. , 1971, Journal of cell science.

[111]  B. Karlson,et al.  Vertical distribution of virus-like particles (VLP) and viruses infecting Micromonas pusilla during late summer in the southeastern Skagerrak, North Atlantic , 1998 .

[112]  J. V. Van Etten,et al.  Viral infection of the symbiotic chlorella-like alga present in Hydra viridis. , 1981, Virology.

[113]  A. M. Chan,et al.  Viruses infecting the marine Prymnesiophyte Chrysochromulina spp.: isolation, preliminary characterization and natural abundance , 1995 .

[114]  M. Weinbauer,et al.  Photoreactivation compensates for UV damage and restores infectivity to natural marine virus communities , 1997, Applied and environmental microbiology.

[115]  S. Gartner.  Late Pleistocene calcareous nannofossils in the caribbean and their interoceanic correlation , 1972 .

[116]  F. Azam,et al.  Biogeochemical significance of bacterial biomass in the ocean's euphotic zone , 1990 .

[117]  R. Meints,et al.  A Feldmannia algal virus has two genome size-classes. , 1996, Virology.

[118]  C. Suttle,et al.  Amplification of DNA polymerase gene fragments from viruses infecting microalgae , 1995, Applied and environmental microbiology.

[119]  C. Pringle.  Virus Taxonomy – 1999 , 2014, Archives of Virology.

[120]  Y. Ishida,et al.  Virus-like particles in Heterosigma akashiwo (Raphidophyceae): a possible red tide disintegration mechanism , 1994 .

[121]  M. S. Shane,et al.  Lysogeny of a blue-green alga, Plectonema boryanum. , 1971, Virology.

[122]  A. T. Chan,et al.  Micromonas pusilla Virus: the Virus Growth Cycle and Associated Physiological Events Within the Host Cells; Host Range Mutation , 1982 .

[123]  E. Padan,et al.  The reproductive cycle of cyanophage LPP1-G in Plectonema boryanum and its dependence on photosynthetic and respiratory systems. , 1970, Virology.

[124]  Nicholas H. Mann,et al.  Lysogenic and lytic viral production in marine microbial communities , 1997 .

[125]  Curtis A. Suttle,et al.  Cyanophages and Their Role in the Ecology of Cyanobacteria , 2000 .

[126]  D. M. Ward,et al.  Denaturing Gradient Gel Electrophoresis Profiles of 16 S rRNA-Defined Populations Inhabiting a Hot Spring Microbial Mat Community , 1996 .

[127]  T. Giddings,et al.  New Anabaena and Nostoc cyanophages from sewage settling ponds. , 1981, Virology.

[128]  J. V. Van Etten,et al.  Growth cycle of a virus, PBCV-1, that infects Chlorella-like algae. , 1983, Virology.

[129]  G. Bratbak,et al.  Production and decay of viruses in aquatic environments , 1991 .

[130]  P. Lemke.  Viruses of eucaryotic microorganisms. , 1976, Annual review of microbiology.

[131]  W. Whitman,et al.  Prokaryotes: the unseen majority. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[132]  W. Reisser,et al.  Viruses and Virus-Like Particles of Freshwater and Marine Eukaryotic Algae — a Review , 1993 .

[133]  L. Sherman,et al.  Infection of Synechococcus cedrorum by the cyanophage AS-1M. I. Ultrastructure of infection and phage assembly. , 1976, Virology.

[134]  M. Cottrell,et al.  Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process , 1998 .

[135]  Yoshihiko Fujita,et al.  OCCURRENCE OF A TEMPERATE CYANOPHAGE LYSOGENIZING THE MARINE CYANOPHYTE PHORMIDIUM PERSICINUM 1 , 1996 .

[136]  L. Oliveira,et al.  A Virus Infection in the Brown Alga Sorocarpus uvaeformis (Lyngbye) Pringsheim (Phaeophyta, Ectocarpales) , 1978 .

[137]  Sunny C. Jiang,et al.  Seasonal and Diel Abundance of Viruses and Occurrence of Lysogeny/Bacteriocinogeny in the Marine Environment , 1994 .

[138]  L. Pomeroy.  The Ocean's Food Web, A Changing Paradigm , 1974 .

[139]  W. Stewart,et al.  A VIRUS OF BLUE‐GREEN ALGAE FROM FRESHWATER HABITATS IN SCOTLAND , 1970 .

[140]  I. Joint,et al.  Production of picoplankton and small nanoplankton in the Celtic Sea , 1983 .

[141]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[142]  J. V. Van Etten,et al.  A survey for viruses from fresh water that infect a eucaryotic chlorella-like green alga , 1985, Applied and environmental microbiology.

[143]  H. L. Berryhill.  Late Quaternary Facies and Structure, Northern Gulf of Mexico: Interpretations from Seismic Data , 1987 .

[144]  J. V. Van Etten,et al.  Lytic viruses infecting a Chlorella-like alga. , 1985, Virology.

[145]  A. Zachary.  Physiology and ecology of bacteriophages of the marine bacterium Beneckea natriegens: salinity , 1976, Applied and environmental microbiology.

[146]  M. V. Regenmortel,et al.  Virus taxonomy: classification and nomenclature of viruses. Seventh report of the International Committee on Taxonomy of Viruses. , 2000 .

[147]  M. Cottrell,et al.  Dynamics of lytic virus infecting the photosynthetic marine picoflagellate Micromonas pusilla , 1995 .

[148]  H. C. Bold,et al.  Introduction to the algae , 1978 .

[149]  J. Maniloff,et al.  Taxonomy of bacterial viruses: establishment of tailed virus genera and the other Caudovirales , 1998, Archives of Virology.

[150]  Jed A. Fuhrman,et al.  Viral mortality of marine bacteria and cyanobacteria , 1990, Nature.

[151]  S. Agustí,et al.  Dissolved esterase activity as a tracer of phytoplankton lysis: Evidence of high phytoplankton lysis rates in the northwestern Mediterranean , 1998 .

[152]  Hongbin Liu,et al.  Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean , 1997 .

[153]  C. Emiliani.  Extinctive evolution: Extinctive and competitive evolution combine into a unified model of evolution , 1982 .

[154]  G. Jackson,et al.  Viral dynamics II: a model of the interaction of ultraviolet light and mixing processes on virus survival in seawater , 1993 .

[155]  C. Suttle,et al.  The Effect of Cyanophages on the Mortality of Synechococcus spp. and Selection for UV Resistant Viral Communities , 1998, Microbial Ecology.

[156]  Y. Ishida,et al.  Viral mortality in the final stage of Heterosigma akashiwo (Raphidophyceae) red tide , 1994 .

[157]  M. Middelboe,et al.  Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton , 1996, Applied and environmental microbiology.

[158]  A. Gibbs,et al.  Further studies on Chara corallina virus. , 1976, Virology.

[159]  G. Bratbak,et al.  Viral control of Emiliania huxleyi blooms , 1996 .

[160]  R. Meints,et al.  A PERSISTENT VIRUS INFECTION IN FELDMANNIA (PHAEOPHYCEAE) 1 , 1992 .

[161]  R. Pienaar.  Virus-like particles in three species of phytoplankton from San Juan Island, Washington , 1976 .

[162]  J. Stockner,et al.  Algal Picoplankton from Marine and Freshwater Ecosystems: A Multidisciplinary Perspective , 1986 .

[163]  J. Stockner,et al.  Autotrophic Picoplankton: Community Composition, Abundance and Distribution across a Gradient of Oligotrophic British Columbia and Yukon Territory Lakes , 1991 .

[164]  R. Safferman,et al.  Control of Algae With Viruses , 1964 .

[165]  Sunny C. Jiang,et al.  Occurrence of Lysogenic Bacteria in Marine Microbial Communities as Determined by Prophage Induction , 1996 .

[166]  C. Suttle,et al.  Evolutionary relationships among large double-stranded DNA viruses that infect microalgae and other organisms as inferred from DNA polymerase genes. , 1996, Virology.