Algicidal Bacteria in the Sea and their Impact on Algal Blooms1

Abstract Over the past two decades, many reports have revealed the existence of bacteria capable of killing phytoplankton. These algicidal bacteria sometimes increase in abundance concurrently with the decline of algal blooms, suggesting that they may affect algal bloom dynamics. Here, we synthesize the existing knowledge on algicidal bacteria interactions with marine eukaryotic microalgae. We discuss the effectiveness of the current methods to characterize the algicidal phenotype in an ecosystem context. We briefly consider the literature on the phylogenetic identification of algicidal bacteria, their interaction with their algal prey, the characterization of algicidal molecules, and the enumeration of algicidal bacteria during algal blooms. We conclude that, due to limitations of current methods, the evidence for algicidal bacteria causing algal bloom decline is circumstantial. New methods and an ecosystem approach are needed to test hypotheses on the impact of algicidal bacteria in algal bloom dynamics. This will require enlarging the scope of inquiry from its current focus on the potential utility of algicidal bacteria in the control of harmful algal blooms. We suggest conceptualizing bacterial algicidy within the general problem of bacterial regulation of algal community structure in the ocean.

[1]  V. Skerman,et al.  Saprospira species—Natural predators , 1981, Current Microbiology.

[2]  T. Sakata,et al.  Algicidal activity and gliding motility of Saprospira sp. SS98-5. , 2003, Canadian journal of microbiology.

[3]  G. Hallegraeff,et al.  Algicidal bacteria associated with blooms of a toxic dinoflagellate in a temperate Australian estuary , 2002 .

[4]  R. Colwell,et al.  Seasonality of Chesapeake Bay Bacterioplankton Species , 2002, Applied and Environmental Microbiology.

[5]  G. Doucette,et al.  Microbial community interactions and population dynamics of an algicidal bacterium active against Karenia brevis (Dinophyceae) , 2002 .

[6]  Mark O. Martin Predatory prokaryotes: an emerging research opportunity. , 2002, Journal of molecular microbiology and biotechnology.

[7]  D. Kirchman The ecology of Cytophaga-Flavobacteria in aquatic environments. , 2002, FEMS microbiology ecology.

[8]  F. Azam,et al.  Microscale patchiness of bacterioplankton assemblage richness in seawater , 2001 .

[9]  T. Sakata,et al.  Phylogenetic Analysis of Marine Algicidal Filamentous Bacteria Inferred from SSU rDNA and Intergenic Spacer Regions , 2001 .

[10]  T. Sunahara,et al.  Fluctuations of the red tide flagellates Chattonella spp. (Raphidophyceae) and the algicidal bacterium Cytophaga sp. in the Seto Inland Sea, Japan , 2001 .

[11]  Y. Ishida,et al.  Analysis of algicidal proteins of a diatom-lytic marine bacterium Pseudoalteromonas sp. strain A25 by two-dimensional electrophoresis , 2001 .

[12]  Y. Ishida,et al.  Isolation of an algicidal marine bacterium with activity against the harmful dinoflagellate Heterocapsa circularisquama (Dinophyceae) , 2001 .

[13]  I. Imai,et al.  Polymerase chain reaction primers for highly selective detection of algicidal Proteobacteria , 2001 .

[14]  K. Tarutani,et al.  Viral Impacts on Total Abundance and Clonal Composition of the Harmful Bloom-Forming PhytoplanktonHeterosigma akashiwo , 2000, Applied and Environmental Microbiology.

[15]  H. Ohtake,et al.  Involvement of an Extracellular Protease in Algicidal Activity of the Marine Bacterium Pseudoalteromonassp. Strain A28 , 2000, Applied and Environmental Microbiology.

[16]  慶三 長崎,et al.  英虞湾から分離された海洋細菌 AA8-2 株の Heterocapsa circularisquama に対する殺藻性に関する検討 , 2000 .

[17]  K. Nagasaki,et al.  Changes in microbial loop components: effects of a harmful algal bloom formation and its decay , 2000 .

[18]  G. Doucette,et al.  ALGICIDAL BACTERIA ACTIVE AGAINST GYMNODINIUM BREVE (DINOPHYCEAE). I. BACTERIAL ISOLATION AND CHARACTERIZATION OF KILLING ACTIVITY1,3 , 1999 .

[19]  S. Kjelleberg,et al.  Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. , 1999, FEMS microbiology ecology.

[20]  Kim Sung-Koo,et al.  Isolation and Characterization of Algicidal Bacteria KY1 , 1999 .

[21]  I. Imai,et al.  Phylogenetic analysis of algicidal bacteria (family Flavobacteriaceae) and selective detection by PCR using a specific primer set , 1999 .

[22]  Song Young Hwan,et al.  Isolation and Characterization of the Marine Bacterium, Alteromonas sp. SR-14 Inhibiting the Growth of Diatom, Chaetoceros Species , 1999 .

[23]  Kim Chang Hoon,et al.  The Activities and Characteristics of Algicidal Bacteria in Chindong Bay , 1999 .

[24]  T. Maeda,et al.  Perspectives of the Development of 16S rDNA Probe Specific for Algicidal and / or Algal-lytic Gliding Bacteria , 1998 .

[25]  A. Uchida,et al.  Population structure of algicidal marine bacteria targeting the red tide forming alga Heterosigma akashiwo (Raphidophyceae), determined by restriction fragment length polymorphism analysis of the bacterial 16S ribosomal RNA genes , 1998 .

[26]  A. Uchida,et al.  A close relationship between algicidal bacteria and termination of Heterosigma akashiwo (Raphidophyceae) blooms in Hiroshima Bay, Japan , 1998 .

[27]  R. Pistocchi,et al.  Bacterial-algal interactions in polysaccharide production , 1998 .

[28]  G. Hallegraeff,et al.  Algicidal Effects of a Novel MarinePseudoalteromonas Isolate (Class Proteobacteria, Gamma Subdivision) on Harmful Algal Bloom Species of the GeneraChattonella, Gymnodinium, andHeterosigma , 1998, Applied and Environmental Microbiology.

[29]  Y. Ishida,et al.  Relationships between dynamics of red tide‐causing raphidophycean flagellates and algicidal micro‐organisms in the coastal sea of Japan , 1998 .

[30]  E. Delong,et al.  High phylogenetic diversity in a marine-snow-associated bacterial assemblage , 1998 .

[31]  Y. Ishida,et al.  Detection and enumeration of microorganisms that are lethal to harmful phytoplankton in coastal waters , 1998 .

[32]  Park Young-Tae,et al.  Isolation of Marine Bacteria Killing Red Tide Microalgae II. Isolation and Algicidal Properties of Pseudomonas sp. LG-2 Possessing Killing Activity for Dinoflagellate, Prorocentrum micans , 1998 .

[33]  Kim Chang-Hoon,et al.  Isolation of Marine Bacteria Killing Red Tide Microalgae I. Isolation and Algicidal Properties of Micrococcus sp. LG-1 Possessing Killing Activity for Harmful Dinoflagellate, Cochlodinium polykrikoides , 1998 .

[34]  J. Ivanova,et al.  A bacterial pathogen of Rhodella reticulata , 1997 .

[35]  C. Brussaard,et al.  AUTOLYSIS KINETICS OF THE MARINE DIATOM DITYLUM BRIGHTWELLII (BACILLARIOPHYCEAE) UNDER NITROGEN AND PHOSPHORUS LIMITATION AND STARVATION 1 , 1997 .

[36]  R. Lewin Saprospira grandis: A Flexibacterium That Can Catch Bacterial Prey by ``Ixotrophy'' , 1997, Microbial Ecology.

[37]  R. Lignell,et al.  THEORETICAL MODELS FOR THE CONTROL OF BACTERIAL GROWTH RATE, ABUNDANCE, DIVERSITY AND CARBON DEMAND , 1997 .

[38]  Y. Ishida,et al.  Analysis of Algicidal Ranges of the Bacteria Killing the Marine Dinoflagellate Gymnodinium mikimotoi Isolated from Tanabe Bay, Wakayama Pref., Japan , 1997 .

[39]  C. Gallegos,et al.  Parasitism of photosynthetic dinoflagellates in a shallow subestuary of Chesapeake Bay, USA , 1996 .

[40]  Y. Nakamura,et al.  Development and collapse of a Gymnodinium mikimotoi red tide in the Seto Inland Sea , 1996 .

[41]  D. Relman,et al.  Sequence-based identification of microbial pathogens: a reconsideration of Koch's postulates , 1996, Clinical microbiology reviews.

[42]  G. Doucette,et al.  Interactions between bacteria and harmful algae: a review. , 1995, Natural toxins.

[43]  H. Abe Analysis, Distribution and Physiological Function of D-Amino Acids in Marine Organisms. Physiological Function of D-Alanine in Crustaceans. , 1995 .

[44]  Y. Ishida,et al.  Algicidal Marine Bacteria Isolated from Northern Hiroshima Bay, Japan , 1995 .

[45]  Y. Ishida,et al.  Distribution and Fluctuation of Bacteria Inhibiting the Growth of a Marine Red Tide Phytoplankton Gymnodinium mikimotoi in Tanabe Bay (Wakayama Pref., Japan) , 1995 .

[46]  A. Salyers,et al.  Bacterial Pathogenesis: A Molecular Approach , 1994 .

[47]  Y. Ishida,et al.  Killing of marine phytoplankton by a gliding bacterium Cytophaga sp., isolated from the coastal sea of Japan , 1993 .

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

[49]  David C. Smith,et al.  Bacterial transformation and transport of organic matter in the Southern California Bight , 1992 .

[50]  Y. Ishida,et al.  Lysis of Skeletonema costatum by Cytophaga sp. Isolated from the Coastal Water of the Ariake Sea. , 1992 .

[51]  K. Fukami,et al.  Isolation and Properties of a Bacterium Inhibiting the Growth of Gymnodinium nagasakiense , 1992 .

[52]  T. Nishijima,et al.  Gymnodinium nagasakiense赤潮の発生・消滅に関与する細菌の分布とその効果 , 1991 .

[53]  David C. Smith,et al.  Bacterial Influence on the Variability in the Ocean’s Biogeochemical State: A Mechanistic View , 1991 .

[54]  Y. Ishida,et al.  Isolation of a marine gliding bacterium that kills Chattonella antiqua (Raphidophyceae) , 1991 .

[55]  T. Sakata,et al.  Plaque Formation by Algicidal Saprospira sp. on a Lawn of Chaetoceros ceratosporum. , 1991 .

[56]  J. Romalde,et al.  Changes in bacterial populations during red tides caused by Mesodinium rubrum and Gymnodinium catenatum in North West Coast of Spain. , 1990, The Journal of applied bacteriology.

[57]  T. Sakata Occurrence of Marine Saprospira sp. Possessing Algicidal Activity for Diatoms , 1990 .

[58]  T. Macke,et al.  A phylogenetic definition of the major eubacterial taxa. , 1985, Systematic and applied microbiology.

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

[60]  Jonathan J. Cole,et al.  INTERACTIONS BETWEEN BACTERIA AND ALGAE IN AQUATIC ECOSYSTEMS , 1982 .

[61]  J. Fuhrman,et al.  Bacterioplankton Secondary Production Estimates for Coastal Waters of British Columbia, Antarctica, and California , 1980, Applied and environmental microbiology.

[62]  F. Azam,et al.  Predator-prey interactions between the larvacean Oikopleura dioica and bacterioplankton in enclosed water columns , 1980 .

[63]  U. Larsson,et al.  Frequency of Dividing Cells, a New Approach to the Determination of Bacterial Growth Rates in Aquatic Environments , 1979, Applied and environmental microbiology.

[64]  D. Herson,et al.  Interactions between the diatom Thallasiosira pseudonanna and an associated pseudomonad in a mariculture system , 1978, Applied and environmental microbiology.

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

[66]  T. Frede,et al.  Theoretical models for the control of bacterial growth rate , abundance , diversity and carbon demand , 2022 .