Appl Environ Microbiol. 2025 Jan 22. e0142224
Vitamin B12 (cobalamin, herein B12) is a key cofactor for most organisms being involved in essential metabolic processes. In microbial communities, B12 is often scarce, largely because only few prokaryotes can synthesize B12 de novo and are thus considered B12-prototrophs. B12-auxotrophy is mostly manifested by the absence of the B12-independent methionine synthase, MetE. Here, we focus on bacteria that we classified as facultative B12 consumers as they encode both B12-independent and -dependent (MetH) methionine synthases yet largely cannot synthesize B12 de novo. The genus Vibrio belongs to this group, and our work shows that upon B12 supply growth of Vibrio campbellii is accelerated and autoinducer-2 (AI-2) concentrations are enhanced. We speculate that methionine synthesis efficiency, dependent on B12 availability, is linked to AI-2 synthesis. The precursor for AI-2 synthesis is S-adenosyl-L-homocysteine (SAH), which in turn requires methionine as a precursor. In almost all Vibrio species studied, btuF (B12-binding protein), which is required for B12 uptake, and cobD (Adenosylcobinamide-phosphate synthase), which enables remodeling of B12-like compounds, are encoded on the same operon as pfs (or mtnN, Adenosylhomocysteine nucleosidase), the first enzyme in the two-step AI-2 synthesis reaction. Transcriptomic analyses show that virulence factors, such as toxin synthesis, fimbriae formation, and activation of the type-6 secretion system, which have been shown to be regulated by quorum sensing via AI-2, are significantly upregulated in V. campbellii when B12 is available. Our results demonstrate that V. campbellii is a facultative B12 consumer and indicate that B12 availability affects AI-2 levels and thus potentially virulence factor regulation.IMPORTANCEMetabolites play a key role in microbial metabolism and communication. While vitamin B12 is an essential cofactor for important enzymatic reactions, autoinducer-2 mediates interspecies signaling and can regulate the expression of genes that are crucial for virulence and survival. In our study, we hypothesize and present findings how these two important metabolites are linked in Vibrio species. Vibrio campbellii grows without B12 but at an accelerated rate when B12 is present, and we detect higher AI-2 values in cultures with B12 amendment. Transcriptome analyses show how vitamin B12 availability significantly upregulates gene expression of virulence factors such as toxin synthesis, fimbrial formation, and activation of the type-6 secretion system in V. campbellii.
Keywords: Gammaproteobacteria; Vibrio campbellii; Vibrionales; autoinducer-2; facultative vitamin B12 consumer; methionine; virulence factor; vitamin B12