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Abstract Vitamin B1 (thiamin, B1) is an essential micronutrient for cells, yet intriguingly in aquatic systems most bacterioplankton are unable to synthesize it de novo (auxotrophy), requiring an exogenous source. Cycling of this valuable metabolite in aquatic systems has not been fully investigated and vitamers (B1-related compounds) have only begun to be measured and incorporated into the B1 cycle. Here, we identify potential key producers and consumers of B1 and gain new insights into the dynamics of B1 cycling through measurements of B1 and vitamers (HMP: 4-amino-5-hydroxymethyl-2-methylpyrimidine, HET: 4-methyl-5-thiazoleethanol, FAMP: N-formyl-4-amino-5-aminomethyl-2-methylpyrimidine) in the particulate and dissolved pool in a temperate coastal system. Dissolved B1 was not the primary limiting nutrient for bacterial production and was relatively stable across seasons with concentrations ranging from 74–117 pM, indicating a balance of supply and demand. However, vitamer concentration changed markedly with season as did transcripts related to vitamer salvage and transport suggesting use of vitamers by certain bacterioplankton, e.g. Pelagibacterales. Genomic and transcriptomic analyses showed that up to 78% of the bacterioplankton taxa were B1 auxotrophs. Notably, de novo B1 production was restricted to a few abundant bacterioplankton (e.g. Vulcanococcus, BACL14 (Burkholderiales), Verrucomicrobiales) across seasons. In summer, abundant picocyanobacteria were important putative B1 sources, based on transcriptional activity, leading to an increase in the B1 pool. Our results provide a new dynamic view of the players and processes involved in B1 cycling over time in coastal waters, and identify specific priority populations and processes for future study. 

ABSTRACT Vitamin B1 (thiamin) is a vital nutrient for most cells in nature, including marine plankton. Early and recent experiments show that B1 degradation products instead of B1 can support the growth of marine bacterioplankton and phytoplankton. However, the use and occurrence of some degradation products remains uninvestigated, namely N-formyl-4-amino-5-aminomethyl-2-methylpyrimidine (FAMP), which has been a focus of plant oxidative stress research. We investigated the relevance of FAMP in the ocean. Experiments and global ocean meta-omic data indicate that eukaryotic phytoplankton, including picoeukaryotes and harmful algal bloom species, use FAMP while bacterioplankton appear more likely to use deformylated FAMP, 4-amino-5-aminomethyl-2-methylpyrimidine. Measurements of FAMP in seawater and biomass revealed that it occurs at picomolar concentrations in the surface ocean, heterotrophic bacterial cultures produce FAMP in the dark—indicating non-photodegradation of B1 by cells, and B1-requiring (auxotrophic) picoeukaryotic phytoplankton produce intracellular FAMP. Our results require an expansion of thinking about vitamin degradation in the sea, but also the marine B1 cycle where it is now crucial to consider a new B1-related compound pool (FAMP), as well as generation (dark degradation—likely via oxidation), turnover (plankton uptake), and exchange of the compound within the networks of plankton. IMPORTANCEResults of this collaborative study newly show that a vitamin B1 degradation product, N-formyl-4-amino-5-aminomethyl-2-methylpyrimidine (FAMP), can be used by diverse marine microbes (bacteria and phytoplankton) to meet their vitamin B1 demands instead of B1 and that FAMP occurs in the surface ocean. FAMP has not yet been accounted for in the ocean and its use likely enables cells to avoid B1 growth deficiency. Additionally, we show FAMP is formed in and out of cells without solar irradiance—a commonly considered route of vitamin degradation in the sea and nature. Altogether, the results expand thinking about oceanic vitamin degradation, but also the marine B1 cycle where it is now crucial to consider a new B1-related compound pool (FAMP), as well as its generation (dark degradation—likely via oxidation), turnover (plankton uptake), and exchange within networks of plankton. 

B-vitamins are essential micronutrients for marine plankton. Additionally, we now know many marine plankton cannot synthesize B-vitamins de novo (from scratch) and thus are reliant on external supplies. Details of B-vitamin exchange, whether ‘active’ or ‘passive’ (i.e. through cell secretion or mortality), are lacking and as a result we struggle to predict microbial physiology, community composition and biogeochemistry. We argue that significant advances in understanding of the impact of B-vitamin exchange and cycling on marine community structure and biogeochemistry can be made by focusing on unknowns related to the ‘in’s and out’s’ of B-vitamin transport, exchange between plankton, and ecosystem scale processing/transformation of B-vitamins. We point out that it is particularly necessary to reach beyond traditional categorization of populations as B-vitamin auxotrophs (requiring supplied vitamin) or prototrophs ( de novo vitamin synthesizers) and begin addressing which populations are net ‘providers’ and/or ‘consumers’. This is a particularly interesting problem as organisms cannot be confidently categorized as net ‘providers’ and/or ‘consumers’ based on genome-based prediction, and it is possible the two roles may change over time and environmental conditions. We posit that greater knowledge of B-vitamin exchange, e.g. cross-feeding, acquisition and secretion systems, environmental triggers of ‘provision’ and ‘consumption’, will reveal unforeseen networking and novel niches across marine planktonic communities. Last, we advocate for further experiments tracking the responses of isolates or natural communities relative to vitamin availability, tracing flow of B-vitamins between cells using novel approaches (e.g. isotopic, fluorometric), and greater consideration of altered B-vitamin exchange and cycling under future climate scenarios.