Vitamin B1 ecophysiology of marine picoeukaryotic algae: Strain‐specific differences and a new role for bacteria in vitamin cycling

We confirmed multiple picoeukaryotic algae, Ostreococcus, Micromonas, and Pelagomonas spp., as thiamine (vitamin B1) auxotrophs in laboratory experiments with axenic cultures. Examined strains have half saturation growth constants (Ks) for B1 between 1.26 and 6.22 pmol B1 L−1, which is higher than reported seawater concentrations. Minimum B1 cell quotas for Ostreococcus and Micromonas spp. are high (2.20 × 10−8–4.46 × 10−8 pmol B1 cell−1) relative to other B1 auxotrophic phytoplankton, potentially making them B1 rich prey for zooplankton and significant B1 reservoirs in oligotrophic marine habitats. Ostreococcus and Micromonas genomes are nonuniformly missing portions of the B1 biosynthesis pathway. Given their gene repertoires, Ostreococcus lucimarinus CCE9901 and Ostreococcus tauri OTH95 are expected to salvage B1 from externally provided 4‐methyl‐5‐thiazoleethanol (HET) and 4‐amino‐5‐hydroxymethyl‐2‐methylpyrimidine (HMP). However, in culture, neither could use HET plus HMP instead of B1, highlighting current limitations of genome‐based prediction of B1 salvaging by picoeukaryotic algae. HMP and phosphorylated B1 use varied amongst tested strains and notably all Prasinophytes tested could not use HMP. B1‐limited O. lucimarinus CCE9901 could not grow on added thiamine diphosphate (TDP), a phosophorylated B1 form. However, in co‐culture with Pseudoalteromonas sp. TW7, a bacterium known to exhibit phosphatase activity, O. lucimarinus CCE9901 exhibited increased growth following TDP additions. This demonstrates that bacteria influence vitamin B1 availability beyond de novo synthesis and consumption; they can also serve as conduits that chemically alter, but not completely degrade or retain B1 analogs (e.g., TDP), and make them accessible to a broader range of microbes.

[1]  J. Archibald,et al.  Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages , 2014, The ISME Journal.

[2]  S. Giovannoni,et al.  Discovery of a SAR11 growth requirement for thiamin’s pyrimidine precursor and its distribution in the Sargasso Sea , 2014, The ISME Journal.

[3]  E. Webb,et al.  The role of B vitamins in marine biogeochemistry. , 2014, Annual review of marine science.

[4]  F. Morel,et al.  Preparation and chemistry of the artificial algal culture medium aquil , 2013 .

[5]  Alison G. Smith,et al.  Analysis of Chlamydomonas thiamin metabolism in vivo reveals riboswitch plasticity , 2013, Proceedings of the National Academy of Sciences.

[6]  J. Montoya,et al.  The distribution of thiamin and pyridoxine in the western tropical North Atlantic Amazon River plume , 2013, Front. Microbiol..

[7]  C. Gobler,et al.  Vitamin B1 and B12 Uptake and Cycling by Plankton Communities in Coastal Ecosystems , 2012, Front. Microbio..

[8]  E. Bertrand,et al.  Influence of vitamin B auxotrophy on nitrogen metabolism in eukaryotic phytoplankton , 2012, Front. Microbio..

[9]  D. Karl,et al.  Multiple B-vitamin depletion in large areas of the coastal ocean , 2012, Proceedings of the National Academy of Sciences.

[10]  Ruben E. Valas,et al.  Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage , 2011, The ISME Journal.

[11]  C. Gobler,et al.  Most harmful algal bloom species are vitamin B1 and B12 auxotrophs , 2010, Proceedings of the National Academy of Sciences.

[12]  Jürgen Pleiss,et al.  The Thiamine diphosphate dependent Enzyme Engineering Database: A tool for the systematic analysis of sequence and structure relations , 2009, BMC Biochemistry.

[13]  T. Begley,et al.  The structural and biochemical foundations of thiamin biosynthesis. , 2009, Annual review of biochemistry.

[14]  A. Salamov,et al.  Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas , 2009, Science.

[15]  B. Palenik,et al.  Temporal variation of Synechococcus clades at a coastal Pacific Ocean monitoring site , 2009, The ISME Journal.

[16]  Kimberly D. Chichester,et al.  Enzymatic assay of marine bacterial phosphatases by capillary electrophoresis with laser‐induced fluorescence detection , 2008, Electrophoresis.

[17]  G. Tarran,et al.  Nutrient limitation of picophytoplankton photosynthesis and growth in the tropical North Atlantic , 2008 .

[18]  D. Hutchins,et al.  Potential cobalt limitation of vitamin B12 synthesis in the North Atlantic Ocean , 2008 .

[19]  A. Starosta,et al.  Molecular characterization of the thi3 gene involved in thiamine biosynthesis in Zea mays: cDNA sequence and enzymatic and structural properties of the recombinant bifunctional protein with 4-amino-5-hydroxymethyl-2-methylpyrimidine (phosphate) kinase and thiamine monophosphate synthase activities. , 2007, The Biochemical journal.

[20]  Nicholas H. Putnam,et al.  The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation , 2007, Proceedings of the National Academy of Sciences.

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

[22]  S. Zabrodskaya,et al.  Antioxidant properties of thiamine , 2000, Bulletin of Experimental Biology and Medicine.

[23]  A. Starosta,et al.  Molecular characterization of the thi 3 gene involved in thiamine biosynthesis in Zea mays : cDNA sequence and enzymatic and structural properties of the recombinant bifunctional protein with 4-amino-5-hydroxymethyl-2-methylpyrimidine ( phosphate ) kinase and thiamine monophosphate synthase activiti , 2007 .

[24]  Yong-Hwan Lee,et al.  Vitamin B1-Induced Priming Is Dependent on Hydrogen Peroxide and the NPR1 Gene in Arabidopsis1 , 2006, Plant Physiology.

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

[26]  S. Dyhrman,et al.  Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: Implications for dissolved organic phosphorus remineralization , 2006 .

[27]  D. Caron,et al.  Abundance and Distribution of Ostreococcus sp. in the San Pedro Channel, California, as Revealed by Quantitative PCR , 2006, Applied and Environmental Microbiology.

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

[29]  A. Worden,et al.  Assessing the dynamics and ecology of marine picophytoplankton: The importance of the eukaryotic component , 2004 .

[30]  C. Suttle The significance of viruses to mortality in aquatic microbial communities , 1994, Microbial Ecology.

[31]  E. Sherr,et al.  Bacterivory and herbivory: Key roles of phagotrophic protists in pelagic food webs , 1994, Microbial Ecology.

[32]  M. Pedersen,et al.  Density-dependent patterns of thiamine and pigment production in the diatom Nitzschia microcephala. , 2003, Phytochemistry.

[33]  F. Azam,et al.  Bacterial control of silicon regeneration from diatom detritus: Significance of bacterial ectohydrolases and species identity , 2001 .

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

[35]  Elizabeth L. Mann,et al.  Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific , 2000 .

[36]  G. Heijne,et al.  ChloroP, a neural network‐based method for predicting chloroplast transit peptides and their cleavage sites , 1999, Protein science : a publication of the Protein Society.

[37]  G. Tarran,et al.  Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S , 1998 .

[38]  D. Downs,et al.  thiBPQ Encodes an ABC Transporter Required for Transport of Thiamine and Thiamine Pyrophosphate inSalmonella typhimurium * , 1998, The Journal of Biological Chemistry.

[39]  Sean R. Eddy,et al.  Profile hidden Markov models , 1998, Bioinform..

[40]  William K. W. Li Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting , 1994 .

[41]  R. Guillard,et al.  Culture of Phytoplankton for Feeding Marine Invertebrates , 1975 .

[42]  R. Guillard,et al.  GROWTH OF VITAMIN B12‐REQUIRING MARINE DIATOMS IN MIXED LABORATORY CULTURES WITH VITAMIN B12‐PRODUCING MARINE BACTERIA 1 2 , 1974 .

[43]  K. Natarajan DISTRIBUTION AND SIGNIFICANCE OF VITAMIN B12 AND THIAMINE IN THE SUBARCTIC PACIFIC OCEAN1 , 1970 .

[44]  J. Strickland The Ecology of the plankton off La Jolla, California,: In the period April through September, 1967 , 1970 .

[45]  S. Lewis,et al.  Some patterns of B vitamin requirements among neritic marine bacteria. , 1968, Canadian journal of microbiology.

[46]  A. Carlucci,et al.  Bioassay of seawater. II. Methods for the determination of concentrations of dissolved vitamin B1 in seawater. , 1966, Canadian journal of microbiology.