Most harmful algal bloom species are vitamin B1 and B12 auxotrophs

Eutrophication can play a central role in promoting harmful algal blooms (HABs), and therefore many HAB studies to date have focused on macronutrients (N, P, Si). Although a majority of algal species require exogenous B vitamins (i.e., auxotrophic for B vitamins), the possible importance of organic micronutrients such as B vitamins (B1, B7, B12) in regulating HABs has rarely been considered. Prior investigations of vitamins and algae have examined a relatively small number of dinoflagellates (n = 26) and a paucity of HAB species (n = 4). In the present study, the vitamin B1, B7, and B12 requirements of 41 strains of 27 HAB species (19 dinoflagellates) were investigated. All but one species (two strains) of harmful algae surveyed required vitamin B12, 20 of 27 species required B1, and 10 of 27 species required B7, all proportions higher than the previously reported for non-HAB species. Half-saturation (Ks) constants of several HAB species for B1 and B12 were higher than those previously reported for other phytoplankton and similar to vitamin concentrations reported in estuaries. Cellular quotas for vitamins suggest that, in some cases, HAB demands for vitamins may exhaust standing stocks of vitamins in hours to days. The sum of these findings demonstrates the potentially significant ecological role of B-vitamins in regulating the dynamics of HABs.

[1]  C. Gobler,et al.  Distributions of dissolved vitamin B12 and Co in coastal and open-ocean environments , 2009 .

[2]  Songhui Lu,et al.  Relationships between nitrogen and phosphorus forms and ratios and the development of dinoflagellate blooms in the East China Sea , 2009 .

[3]  C. Gobler,et al.  Harmful algal blooms and eutrophication: Examining linkages from selected coastal regions of the United States. , 2008, Harmful algae.

[4]  Patricia M. Glibert,et al.  Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters , 2008 .

[5]  C. Gobler,et al.  Eutrophication and Harmful Algal Blooms: A Scientific Consensus. , 2008, Harmful algae.

[6]  D. Kamykowski,et al.  Benthic–pelagic coupling in sediment-associated populations of Karenia brevis , 2008 .

[7]  C. Gobler,et al.  Effect of B-vitamins (B1, B12) and inorganic nutrients on algal bloom dynamics in a coastal ecosystem , 2007 .

[8]  M. Saito,et al.  Vitamin B12 and iron colimitation of phytoplankton growth in the Ross Sea , 2007 .

[9]  Michael R Droop Vitamins, Phytoplankton and Bacteria: Symbiosis or Scavenging? , 2007 .

[10]  C. Duarte,et al.  B vitamins as regulators of phytoplankton dynamics , 2006 .

[11]  Alison G. Smith,et al.  Algae Need Their Vitamins , 2006, Eukaryotic Cell.

[12]  G. Taylor,et al.  Regulation of phytoplankton dynamics by vitamin B12 , 2006 .

[13]  Martin J. Warren,et al.  Algae acquire vitamin B12 through a symbiotic relationship with bacteria , 2005, Nature.

[14]  R. Andersen Microbiology: Algae and the vitamin mosaic , 2005, Nature.

[15]  H. Jeong,et al.  Feeding by phototrophic red-tide dinoflagellates: five species newly revealed and six species previ- ously known to be mixotrophic , 2005 .

[16]  S. Sañudo-Wilhelmy,et al.  Direct determination of vitamin B1 in seawater by solid‐phase extraction and high‐performance liquid chromatography quantification , 2005 .

[17]  Patricia M. Glibert,et al.  Prorocentrum minimum (Pavillard) Schiller A review of a harmful algal bloom species of growing worldwide importance , 2005 .

[18]  S. Sañudo-Wilhelmy,et al.  A new method for the determination of Vitamin B12 in seawater , 2004 .

[19]  C. Gobler,et al.  Nutrient limitation, organic matter cycling, and plankton dynamics during an Aureococcus anophagefferens bloom , 2004 .

[20]  Debashish Bhattacharya,et al.  A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Landsberg,et al.  The Effects of Harmful Algal Blooms on Aquatic Organisms , 2002 .

[22]  K. Steidinger,et al.  Saharan Dust and Florida Red Tides: The Cyanophyte Connection , 2001 .

[23]  F. Colijn,et al.  The vitamin B requirement of Phaeocystis globosa (Prymnesiophyceae) , 2000 .

[24]  P. Harrison,et al.  Research on red tide occurrences using enclosed experimental ecosystems in west Xiamen Harbor, China—Relationship between various factors and red tide occurrences , 2000 .

[25]  H. Jeong The Ecological Roles of Heterotrophic Dinoflagellates in Marine Planktonic Community 1 , 1999 .

[26]  G. Hallegraeff,et al.  Growth and biomass stimulation of the toxic dinoflagellate Gymnodinium catenatum (Graham) by dissolved organic substances , 1999 .

[27]  T. Smayda,et al.  Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea , 1997 .

[28]  Karen A. Steidinger,et al.  Gymnodinium breve red tide blooms: Initiation, transport, and consequences of surface circulation , 1997 .

[29]  G. Min,et al.  The effects of nitrogen, phosphorus, vitamins and trace metals on the growth of the red tide organismProrocentrum Micans , 1995 .

[30]  Michael E. Sieracki,et al.  Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton , 1992 .

[31]  E. Carpenter,et al.  Blooms of the dinoflagellate Gyrodinium aureolum in a Long Island estuary: , 1985 .

[32]  E. Granéli,et al.  Chemical composition and alkaline phosphatase activity of nutrient-saturated and P-deficient cells of four marine dinoflagellates , 1984 .

[33]  M. Takahashi,et al.  A mechanism of “red-tide” formation , 1982 .

[34]  P. Hargraves,et al.  Structural and physiological observations on some small marine diatoms , 1974 .

[35]  M. Tassigny OBSERVATIONS SUR LES BESOINS EN VITAMINES DES DESMIDIÉES (CHLOROPHYCÉES‐ZYGNEMATALES) 1 , 1971 .

[36]  A. Carlucci,et al.  PRODUCTION OF VITAMIN B12, THIAMINE, AND BIOTIN BY PHYTOPLANKTON 1 , 1970 .

[37]  A. Carlucci,et al.  BIOASSAY OF SEAWATER. III. DISTRIBUTION OF VITAMIN B12 IN THE NORTHEAST PACIFIC OCEAN1 , 1966 .

[38]  C. Forsberg Nutritional Studies of Chara in Axenic Cultures , 1965 .

[39]  L. Provasoli,et al.  Nutrition of Algae , 1964 .

[40]  D. Aldrich Photoautotrophy in Gymnodinium breve Davis , 1962, Science.

[41]  R. Guillard,et al.  Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. , 1962, Canadian journal of microbiology.

[42]  B. Parker,et al.  Facultative Heterotrophy in Some Chlorococcacean Algae , 1961, Science.

[43]  J. E. Ford B12-vitamins and growth of the flagellate Ochromonas malhamensis. , 1958, Journal of general microbiology.

[44]  M. Droop Requirement for Thiamine Among Some Marine and Supra-Littoral Protista , 1958, Journal of the Marine Biological Association of the United Kingdom.

[45]  L. Provasoli,et al.  ECOLOGICAL IMPLICATIONS OF IN VITRO NUTRITIONAL REQUIREMENTS OF ALGAL FLAGELLATES , 1953, Annals of the New York Academy of Sciences.

[46]  T. Jukes,et al.  Assay of Anti-Pernicious Anemia Factor with Euglena. , 1949, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[47]  G. E. Fogg,et al.  Studies on the growth of Xanthophyceae in pure culture , 2004, Archiv für Mikrobiologie.

[48]  张庆,et al.  THE EFFECTS OF NITROGEN,PHOSPHORUS,VITAMINS AND TRACE METALS ON THE GROWTH OF THE RED TIDE ORGANISM PROROCENTRUM MICANS , 1995 .

[49]  E. Granéli,et al.  Was the Chrysochromulina polylepis bloom in 1988 caused by a release of cobalt or vitamin B12 from a previous bloom of Skeletonema costatum , 1995 .

[50]  D. M. Anderson,et al.  Red tides. , 1994, Scientific American.

[51]  D. Anderson,et al.  Red tides : biology, environmental science, and toxicology : proceedings of the First International Symposium on Red Tides held November 10-14, 1987, in Takamatsu, Kagawa Prefecture, Japan , 1989 .

[52]  F. Tailor The biology of Dinoflagellates , 1987 .

[53]  Marta Estrada,et al.  Functional morphology of organisms involved in red tides, as adapted to decaying turbulence , 1979 .

[54]  Albert Collier Some Biochemical Aspects of Red Tides and Related Oceanographic Problems1 , 1958 .