Globally Important Haptophyte Algae Use Exogenous Pyrimidine Compounds More Efficiently than Thiamin

Abstract

Vitamin B1 (thiamin) is a cofactor for critical enzymatic processes and is scarce in surface oceans. Several eukaryotic marine algal species thought to rely on exogenous thiamin are now known to grow equally well on the precursor 4-amino-5-hydroxymethyl-2-methylpyrimidine (HMP), including the haptophyte Emiliania huxleyi. Because the thiamin biosynthetic capacities of the diverse and ecologically important haptophyte lineage are otherwise unknown, we investigated the pathway in transcriptomes and two genomes from 30 species representing six taxonomic orders. HMP synthase is missing in data from all studied taxa, but the pathway is otherwise complete, with some enzymatic variations. Experiments on axenic species from three orders demonstrated that equivalent growth rates were supported by 1 µM HMP or thiamin amendment. Cellular thiamin quotas were quantified in the oceanic phytoplankter E. huxleyi using the thiochrome assay. E. huxleyi exhibited luxury storage in standard algal medium [(1.16 ± 0.18) × 10−6 pmol thiamin cell−1], whereas quotas in cultures grown under more environmentally relevant thiamin and HMP supplies [(2.22 ± 0.07) × 10−7 or (1.58 ± 0.14) × 10−7 pmol thiamin cell−1, respectively] were significantly lower than luxury values and prior estimates. HMP and its salvage-related analog 4-amino-5-aminomethyl-2-methylpyrimidine (AmMP) supported higher growth than thiamin under environmentally relevant supply levels. These compounds also sustained growth of the stramenopile alga Pelagomonas calceolata. Together with identification of a salvage protein subfamily (TENA_E) in multiple phytoplankton, the results indicate that salvaged AmMP and exogenously acquired HMP are used by several groups for thiamin production. Our studies highlight the potential importance of thiamin pathway intermediates and their analogs in shaping phytoplankton community structure.

Transcriptomic and proteomic responses of the oceanic diatomPseudo‐nitzschia graniito iron limitation

“…The continued expression of thiamine biosynthesis genes despite thiamine being added to the culture medium suggests P. granii does not have a mechanism to take up HMP‐P from the environment, and continues to biosynthesize products even when thiamine is present externally. The THIC gene has not been identified in diverse and globally abundant haptophytes with available transcriptomes and genomes, consistent with observations of haptophyte members utilizing exogenously‐acquired intermediates to fulfill thiamine demands (Gutowska et al, ). These findings support substantial differences in vitamin utilization strategies between haptophytes and diatoms, and even within the diatom lineage, likely influencing niche differentiation in natural surface plankton communities, micronutrient recycling patterns and regional microbial community dynamics.…”

“…(2015),Allen et al (2011), Bender et al (2014,Bertrand et al (2012),Gutowska et al (2017),Hockin et al (2012),Lommer et al (2012),McRose et al (2014),Paerl et al (2016),Pearson et al (2015),Pourcel et al (2013),Smith et al, (2016) andWolfe-Simon et al (2006). [Cytosol] ISIP1: iron starvation-induced protein 1; ISIP2A: iron starvation-induced protein 2A; ISIP3: iron starvation-induced protein 3; ABC.FEV.S: iron complex transport system substrate-binding protein; ABC.FEV.A: Iron (III) dicitrate transport ATP-binding protein; ACACA: biotin carboxylase; HSP70: heat shock protein 70 kDa 1/8; TYR: tyrosinase; NRT2: nitrate transporter; AMT: ammonium transporter; NR: nitrate reductase; NIRB: NADPH-nitrite reductase; UTP: urea transporter; SLC14: solute carrier family 14 (urea transporter); URE: urease; ARG: arginase; ASL: argininosuccinate lysase; ASSY: argininosuccinate synthase; AQP: aquaporin; THIC: phosphomethylpyrimidine synthase; THIDE: hydroxymethylpyrimidine kinase; THIG: thiazole synthase; TPK: thiamine pyrophosphokinase; COBH: precorrin-8X/cobalt-precorrin-8 methylmutase; COBB: cobyrinic acid a,c-diamide synthase; COBN, COBS, COBT: cobaltochelatase; COBR: cob(II)yrinic acid a,c-diamide reductase; COBA: cob(I)alamin adenosyltransferase; COBQ: adenosylcobyric acid synthase; COBD: adenosylcobinamide-phosphate synthase; COBP: adenosylcobinamide kinase; COBU: nicotinate-nucleotide-dimethylbenzimidazole phosphoribosyltransferase; COBC: alpha-ribazole phosphatase; COBS: adenosylcobinamide-GDP ribazoletransferase; CBA1: cobalamin acquisition protein 1.…”

Mosaic patterns of B‐vitamin synthesis and utilization in a natural marine microbial community

“…However, the matter of VB 1 availability is further complicated by the fact that several microbial groups can only meet their biological demands with the uptake of VB 1 precursors instead of the complete VB 1 molecule (Carini et al, 2014). Even though we did not quantify the different moieties of this vitamin, knowing the standing stock of VB 1 is relevant, as some of its decomposition products could be used for cellular growth by diverse phytoplankton groups (Gutowska et al, 2017). Future studies will need to address the effect of VB 1 moieties and pathway intermediates in natural communities as recently established in culture growth studies (Gutowska et al, 2017;Paerl et al, 2017).…”

B Vitamins and Their Congeners as Potential Drivers of Microbial Community Composition in an Oligotrophic Marine Ecosystem

“…B vitamins can influence both eukaryotic and prokaryotic members of the microbial community via a complex ecological interplay between producers and auxotrophs in the water column (Gómez‐Consarnau et al, ) as well as in the sediments (Monteverde et al, ). However, most of the field studies to date have only focused on their impact on eukaryotic phytoplankton (Bertrand & Allen, ; Bertrand et al, , ; Cohen et al, ; Gobler et al, ; Gutowska et al, ; Koch et al, ; McRose et al, ; Paerl et al, , ; Panze ca et al, , ). One of the questions that remains unanswered is to what extent the geographical distribution of marine microbes are related to the availability of these exogenous metabolites.…”