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

Abstract

Microbial communities occupy diverse niches in nature, and exchanges of metabolites such as carbon sources, amino acids, and vitamins occur routinely among the community members. While large-scale metagenomic and metabolomic studies shed some light on these exchanges, the contribution of individual species and the molecular details of specific interactions are difficult to track. Here, we explore the molecular picture of vitamin B1 (thiamin) metabolism occurring in synthetic communities of Escherichia coli thiamin auxotrophs which engage in the exchange of thiamin and its biosynthesis intermediates. In E. coli, the two parts of thiamin - the 4-amino-5-hydroxymethyl-2-methylpyrimidine and the 4-methyl-5-(2-hydroxyethyl)thiazole - are synthesized by separate pathways using enzymes ThiC and ThiG, respectively, and are then joined by ThiE to form thiamin. We observed that even though E. coli {Delta}thiC, {Delta}thiE, and{Delta} thiG mutants are thiamin auxotrophs, co-cultures of{Delta} thiC-{Delta}thiE and{Delta} thiC-{Delta}thiG grow in a thiamin-deficient minimal medium, whereas the{Delta} thiE-{Delta}thiG co-culture does not. Analysis of the exchange of thiamin and its intermediates in Vibrio anguillarum co-cultures, and in mixed co-cultures of V. anguillarum and E. coli revealed that the general pattern of thiamin metabolism and exchange among microbes is conserved across species. Specifically, the microorganisms exchange HMP and thiamin easily among themselves but not THZ. Furthermore, we observe that the availability of exogenous thiamin in the media affects whether these strains interact with each other or grow independently. This underscores the importance of the exchange of essential metabolites as a defining factor in building and modulating synthetic or natural microbial communities.