The bacterial Bmt methionine synthase is involved in lag phase shortening

Bacteria can shorten their lag phase by utilizing methyl groups from compounds such as dimethylsulfoniopropionate (DMSP). These methyl groups are then incorporated into cellular building blocks via the methionine cycle. However, the specific contribution of bacterial methionine synthesis, which is critical for assimilating and incorporating methyl groups, remains unclear.In this study, we employed transcriptomics, genetic manipulation and biochemical assays to explore the involvement of methionine synthesis in lag phase shortening using the model marine bacterium Phaeobacter inhibens. We mapped the expression profiles of the MetH-like methionine synthase components—an enzyme complex that is encoded by three genes—in response to DMSP during the lag phase. Our findings revealed transcriptional decoupling of the three genes. The deletion of the homocysteine-binding component of the MetH-like complex, namely bmt, disrupted lag phase shortening in response to DMSP. Through heterologous expression of the bmt gene product, we show that the individual Bmt enzyme produces methionine by directly demethylating DMSP and betaine in vitro. These findings reveal a metabolic route that was not previously described in marine bacteria. Since Bmt does not require tetrahydrofolate or cobalamin as co-factors for methionine synthesis, its potential to act alone as a demethylase and a methionine synthase represents a cost-effective metabolic shortcut for methyl group assimilation, which could be specifically beneficial under limiting conditions. Indeed, we show that under stress conditions, Bmt allows cells to shorten their lag phase in response to DMSP.This study enhances our understanding of the enzymatic mechanisms underlying bacterial lag phase shortening, revealing microbial adaptation strategies in response to environmental conditions.