Exploring Vitamin B1 Cycling and Its Connections to the Microbial Community in the North Atlantic Ocean

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.

The exchange of vitamin B1 and its biosynthesis intermediates in synthetic microbial communities shapes the community composition and reveals complexities of nutrient sharing

“…But when the nutrient is unavailable or scarce, a crosstalk that allows for the microorganisms to collectively build and share the nutrient may evolve, which will result in subsequently shaping the composition of and relative abundance of members of the community. Indeed, it has been shown that the seasonal blooms of marine microorganisms which either produce or utilize thiamin alter concentrations of thiamin biosynthesis intermediates in seawater and when the microbial numbers are low, the overall concentrations of the intermediates remain at an equilibrium (32). Such changes in the community composition have also been reported earlier for synthetic co-cultures based on their differential ability of nutrient exchange or uptake (4,5,39).…”

“…Even beyond marine ecosystems, there is a propensity for HMP exchange within the human gut microbiome (HGM) as well, wherein out of the 2,228 reference genomes studied, 199 were HMP auxotrophs, whereas only 114 were THZ auxotrophs (17). These studies, taken together with our observations, point to HMP and possibly other pyrimidine intermediates that can yield HMP via salvage as key nutrients in determining the dynamics of nutrient exchange and subsequently microbial abundance (22,31,32).…”

“…In E. coli, the formation of the HMP-P ring is catalyzed by the enzyme ThiC, the THZ-P ring is synthesized by a host of enzymes including ThiG, and subsequently, these rings are coupled together by ThiE to form TMP. Also, no known transporters and salvage enzymes of the HMP or THZ or their analogues are found in this organism, and only one known transporter ThiBPQ exists to facilitate thiamin transport (22,25,26,(30)(31)(32). We generated E. coli str.…”

Simultaneous quantification of all B vitamins and selected biosynthetic precursors in seawater and bacteria by means of different mass spectrometric approaches

“…The analysis of B vitamins in seawater is of increasing interest as numerous microbial vitamin cross-feeding interactions occur and their availability even affects marine microbial communities [7,8]. Thus, the content of B vitamins in the sea is closely linked to the occurrence of microbial producers and consumers [9,10]. Only few studies on B vitamin quantification in seawater have been conducted [11][12][13][14].…”

Ecophysiology and genomics of the brackish water adapted SAR11 subclade IIIa

“…IIIa.3 has the potential for AmMP to fulfil thiamin requirements instead of being reliant on HMP like most other SAR11( 14) due to the presence of tenA. In a recent survey of thiamin-related compound concentrations in the North Atlantic, AmMP was found in similar but higher concentrations than HMP at multiple marine stations (65). This represents a crucial niche-differentiating step for IIIa.3 from other SAR11, including the sister groups IIIa.1 and IIIa.2 that are likely reliant on HMP (14).…”