Abstract
Vitamin B1 (thiamin) is an essential coenzyme for all cells. Recent findings from experimental cell biology and genome surveys have shown that thiamin cycling by plankton is far more complex than was previously understood. Many plankton cells cannot produce thiamin (are auxotrophic) and obligately require an exogenous source of thiamin or one or more of 5 different thiamin-related compounds (TRCs). Despite this emerging evidence for the evolution among plankton of complex interactions related to thiamin, the influence of TRCs on plankton community structure and productivity are not understood. We report measurements of three dissolved TRCs 4-amino-5-aminomethyl-2-methylpyrimidine (AmMP), 5-(2-hydroxyethyl)-4-methyl-1,3-thiazole-2-carboxylic acid (cHET), and 4-methyl-5-thiazoleethanol (HET) that have never before been assayed in seawater. Here we characterize them alongside other TRCs that were measured previously [thiamin and 4-amino-5-hydroxymethyl-2-methylpyrimidine (HMP)], in depth profiles from a latitudinal transect in the north Atlantic in March 2018. TRC concentrations ranged from femptomolar to picomolar. Surface depletion relative to a maximum near the bottom of the euphotic zone and low concentrations at deeper depths were consistent features. Our observations suggest that when bacterial abundance and production are low, TRC concentrations approach a steady state where TRC production and consumption terms are balanced. Standing stocks of TRCs also appear to be positively correlated with bacterial production. However, near the period of peak biomass in the accumulation phase of a bloom we observed an inverse relationship between TRCs and bacterial production, coincident with an increased abundance of Flavobacteria that comparative genomics indicates could be vitamin B1 auxotrophs. While these observations suggest that the dissolved pool of TRCs is often at steady state, with TRC production and consumption balanced, our data suggests that bloom induced shifts in microbial community structure and activity may cause a decoupling between TRC production and consumption, leading to increased abundances of some populations of bacteria that are putatively vitamin B1 auxotrophs.
Highlights
Vitamin B1, known as thiamin, is an essential coenzyme required for carbon metabolism across all domains of life (Monteverde et al, 2017)
Given the predominance of Flavobacteria and other copiotrophs in the surface B1 depleted water at station 2 (Figure 5), we further investigated their potential B1 auxotropy status to determine if they had a requirement for thiamin-related compounds (TRCs)
To this end we searched available databases and identified 31 single amplified genomes (SAGs) (Supplementary Table 2) of the class Flavobacteria and surveyed key enzymes involved in the de novo pathway to synthesize vitamin B1 (dxs, thiH, thiD, thiC, thiE, thiG, and thiL; Supplementary Table 4)
Summary
Vitamin B1, known as thiamin, is an essential coenzyme required for carbon metabolism across all domains of life (Monteverde et al, 2017). In marine systems there are over 30 vitamin B1 dependent enzymes found in microbial genomes (Schowen, 1998; Sañudo-Wilhelmy et al, 2014) These enzymes are mainly used for carbohydrate and branched chain amino acid metabolism and include pyruvate dehydrogenase, transketolase, and oxoglutarate dehydrogenase, which catalyze key steps in the TCA and Calvin-Benson cycles (Rapala-Kozik, 2011). Vitamin B1 has a heterocyclic structure consisting of a pyrimidine and a thiazole ring (Begley et al, 1999; Chatterjee et al, 2006; Jurgenson et al, 2009) These rings are biosynthesized by separate metabolic pathways and ligated together to form thiamin, vitamin B1 (Jurgenson et al, 2009). Cell membrane transport proteins for vitamin B1 are common in marine microbes, indicating that some members of the microbial community can assimilate exogenous vitamin B1 and its related compounds from the dissolved pool (Gómez-Consarnau et al, 2016; Donovan et al, 2018)
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