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Vitamin B1 Ecophysiology of Marine Picoeukaryotic Algae: Strain-Specific Differences and a New Role for Bacteria in Vitamin Cycling

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Vitamin B1 Ecophysiology of Marine Picoeukaryotic Algae: Strain-Specific Differences and a New Role for Bacteria in Vitamin Cycling LIMNOLOGY and Limnol. Oceanogr. 00, 2015, 1–26 OCEANOGRAPHY VC 2015 Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10009 Vitamin B1 ecophysiology of marine picoeukaryotic algae: Strain-specific differences and a new role for bacteria in vitamin cycling R. W. Paerl,1* E. M. Bertrand,2,3 A. E. Allen,2,3 B. Palenik,1 F. Azam1 1Scripps Institution of Oceanography, Marine Biology Research Division, University of California at San Diego, La Jolla, California 2Scripps Institution of Oceanography, Integrative Oceanography Division, University of California at San Diego, La Jolla, California 3J. Craig Venter Institute, Microbial and Environmental Genomics Department, La Jolla, California Abstract 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 21 growth constants (Ks) for B1 between 1.26 and 6.22 pmol B1 L , which is higher than reported seawater con- centrations. Minimum B1 cell quotas for Ostreococcus and Micromonas spp. are high (2.20 3 1028–4.46 3 1028 pmol B1 cell21) 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 pro- vided 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 Pseu- doalteromonas 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. Vitamin B1 (called B1 herein), also known as thiamine, is or below (Sanudo-Wilhelmy~ et al. 2012). Despite the scarcity required by all cells due to its role as a cofactor in the form of B1 in the upper ocean, especially the oligotrophic regions of thiamine pyrophosphate (also called thiamine diphos- where published B1 concentrations are < 0.05 pmol L21 phate [TDP]) for enzymes critical to carbon and amino acid (Barada et al. 2013), several marine plankton (eukaryotes and metabolism (Jurgenson et al. 2009). Additionally, certain prokaryotes) persist as B1 auxotrophs, unable to synthesize riboswitches, untranslated sections of messenger ribonucleic their own vitamin B1. Surveys of the occurrence of vitamin acid (RNA) capable of regulating gene expression, are acti- auxotrophy within phytoplankton noted that a large per- vated by binding TDP, B1, and moieties (parts of the thia- centage ( 80%) of prymnesiophytes were B1 auxotrophs mine molecule, e.g., thiazole and pyrimidine; Moulin et al. (Provasoli and Carlucci 1974; Croft et al. 2006). In contrast, 2013). Notably, this is one of the few documented ribos- a majority of diatoms produce B1 (Provasoli and Carlucci witch systems in eukaryotes, and appears to be important in 1974), and both B1 producing and auxotrophic bacteria are regulating thiamine metabolism in marine microbes (McRose present in the ocean (MacLeod et al. 1954; Burkholder and et al. 2014). Lewis 1968). In the euphotic upper ocean, thiamine concentrations Many new algal strains have been isolated as the pioneer- appear to be low relative to macronutrients, e.g., pmol L21 ing surveys of auxotrophy (Provasoli and Carlucci 1974), including multiple picoeukaryotic algal strains (less than *Correspondence: [email protected] three micrometer in cell diameter). There is increasing 1 Paerl et al. Marine picoeukaryote thiamine physiology evidence, based largely on genome analysis, that several key cell yield relation by Droop (2007)] are available for a small picoeukaryotic algae are B1 auxotrophs (Palenik et al. 2007; set of algae, specifically Pavlova lutheri (Carlucci and Silberna- Worden et al. 2009; Bertrand and Allen 2012; McRose et al. gel 1966), A. anophagefferens and larger dinoflagellate strains 2014) but also based on a small set of experiments with (Tang et al. 2010). No such data have been reported for axenic cultures (e.g., Aureococcus anophagefferens CCMP1984, Ostreococcus, Micromonas,orPelagomonas spp. B1 kinetic Micromonas spp.; Tang et al. 2010; Bertrand and Allen 2012; growth constant and B1 cell quota data for auxotrophic McRose et al. 2014). Picoeukaryotic phytoplankton are picoeukaryotic phytoplankton would provide a better sense important contributors to marine primary production and of; (1) whether or not they have the potential to be growth- phytoplankton biomass (Li 1994; Worden et al. 2004). Also limited by B1 availability in the euphotic ocean, (2) any some B1 auxotrophic picoeukaryotic and larger eukaryotic dependence on intimate interactions with other microbes algae are harmful algal bloom (HAB)-associated species, e.g., for B1, and (3) their influence on B1 cycling based on their A. anophagefferens and Phaeocystis globosa (Peperzak 2000; B1 demand (pmol B1 cell21). Tang et al. 2010). Thus, vitamin B1 availability may influ- We conducted laboratory-based experiments with putative ence primary production rates, marine algal community vitamin B1 auxotrophic and cosmopolitan picoeukaryotic structure, and water quality by influencing the growth and phytoplankton, specifically, Ostreococcus lucimarinus CCE9901, activity of picoeukaryotic phytoplankton. Ostreococcus sp. CCE1301, Micromonas pusilla CCMP487, and Several studies found positive correlations between pri- Pelagomonas calceolata CCMP1756. Using axenic cultures, we mary productivity rates and additions of B1 or increases in confirmed these strains as B1 auxotrophs, determined their natural B1 seawater concentrations. B1 additions to subarctic vitamin B1 half (Ks)andmaximum(Kmax) saturation growth N. Pacific seawater stimulated bulk primary productivity constants, their ability to utilize B1 chemical analogs (moi- (Natarajan 1970), a significant positive correlation between eties and phosphorylated forms), and their respective mini- net primary productivity and B1 concentrations was found mal B1 cell quotas. Lastly, we examined if the presence of a at one location off La Jolla, California (Carlucci 1970) and simple microbial population (Gammaproteobacterium Pseudo- most recently, a positive correlation between B1 seawater monas sp. TW7) would enable a B1 auxotrophic algae (O. luci- concentrations and primary production (as well as nitrogen marinus CCE9901) to utilize a phosphorylated B1 analog it fixation) was reported for the upper water column of the cannot use in isolation. western tropical Atlantic (Barada et al. 2013). The degree to which vitamin B1 availability affects growth of B1 auxotro- phic algae will in part depend on multiple aspects of algal Methods B1-related physiology, e.g., utilizable forms, uptake affinity, M. pusilla CCMP487, Ostreococcus spp., and P. lutheri cul- and per cell requirements. tures were grown on modified F/2 medium (Guillard 1975) Early vitamin research showed that B1 moieties or chemi- plus sodium selenite and sodium citrate (as formulated by cal analogs (compounds sharing structural similarity to thia- Palenik unpubl.). The seawater base was twice 0.22 lm fil- mine) satisfied the B1 requirement of auxotrophic marine tered, microwaved and treated with activated charcoal to algae, specifically flagellates, and benthic diatoms isolated remove organics as previously described (Carlucci and Silber- from vitamin replete sediment and intertidal habitats (Prova- nagel 1966). This seawater base was then supplemented with soli and Carlucci 1974). Additionally, a representative strain autoclaved F/2 nitrate and phosphate solutions as well as 0.2 of the ubiquitous marine bacterial family Pelagibacteraceae lm filter-sterilized stocks of the trace metal mix, sodium sel- (also known as the SAR11 clade) exhibits an obligate require- enite (87 nmol L21 final), and sodium citrate (50 lmol L21 ment for 4-amino-5-hydroxymethyl-2-methylpyrimidine final). P. calceolata CCMP1756 cultures were grown in Aquil (HMP) that cannot be satisfied by B1 (Carini et al 2014), and synthetic seawater supplemented with F/2 concentrations of the coccolithophore Emiliania huxleyi is able to use both B1 filter-sterilized nitrate, phosphorus, and trace metal mix. For and HMP to satisfy its B1 requirements (McRose et al. 2014), all cultures, filter-sterilized vitamin B12 (cobalamin) and B7 emphasizing the importance of understanding B1 moiety (biotin; 184 pmol L21 and 1 nmol L21 final respective con- utilization patterns in marine microbes. In contrast, two centrations) solutions were added individually so that B1 strains of Micromonas only use B1 and not its precursors to could be added later at varying concentrations (medium satisfy thiamine requirements (McRose et al. 2014); it
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