Dual roles of glycine betaine (GB), dimethylglycine, and sarcosine as osmoprotectants and nutrient sources in Vibrio natriegens

Authors: THOMAS, HEATHER - University Of Delaware; BOAS LLCHTY, KATHERINE - University Of Delaware; Richards, Gary; BOYD, FIDELMA - University Of Delaware

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/25/2025
Publication Date: 4/23/2025
Citation: Thomas, H., Boas Llchty, K.E., Richards, G.P., Boyd, F.E. 2025. Dual roles of glycine betaine (GB), dimethylglycine, and sarcosine as osmoprotectants and nutrient sources in Vibrio natriegens. Applied and Environmental Microbiology. https://doi.org/10.1128/aem.00619-25.
DOI: https://doi.org/10.1128/aem.00619-25

Interpretive Summary: Compatible solutes are small, organic compounds that can accumulate to high levels in bacteria, thus allowing bacteria to adapt to high salinity or other physical stresses within their environments. Compatible solutes can be either taken up from the environment or biosynthesized by bacteria and other life forms. Compatible solutes include glycine betaine, dimethylglycine, and sarcosine which are energy sources in many bacteria as well as potential carbon sources to support bacterial growth when nutrients are limited. This study showed that Vibrio natriegens bacteria, which are naturally found in the marine environment, can grow in 1% to 7% salt, biosynthesize and break down compatible solutes, and transport them through their cell walls to reduce salt stress. They also have the genetic machinery to utilize compatible solutes as carbon, nitrogen and energy sources for their growth and development. Genes associated with the breakdown of compatible solutes were explored and found in many Vibrio and non-Vibrio species. These genes provide a competitive advantage for V. natriegens and other Vibrio and non- Vibrio bacteria within the marine environment.

Technical Abstract: Bacteria respond to osmotic stress by intracellularly accumulating low molecular weight compounds called compatible solutes (CS), also known as osmolytes. Glycine betaine (N,N,N-trimethylglycine, GB) is a highly effective and widely available osmolyte used by bacteria, algae, and plants for abiotic stress protection. Here, we highlight the dual roles of GB, dimethyl glycine (DMG), and sarcosine for both osmoprotection and a less known role as sole carbon sources. First, we showed that the marine halophile Vibrio natriegens can grow in 1% to 7% NaCl and biosynthesize GB, ectoine, and glutamate, and imported GB, DMG, and sarcosine in response to osmotic stress. Betaine-carnitine-choline transporters (BCCTs) for the uptake of GB and DMG, but not sarcosine, were identified. Bioinformatics analyses uncovered homologs of GB, DMG, and sarcosine catabolism genes (dgcAB_fixAB, gbcA, gbcB, purU, soxBDAG, glyA, glxA) clustered in the V. natriegens genome and these genes had a limited distribution among vibrios. We showed V. natriegens ATCC 14048 grew on GB, DMG, and sarcosine as sole carbon sources and gbcA and dgcA were required for growth. A contiguous catabolism cluster was present in a subset of V. fluvialis strains, and we demonstrated growth of V. fluvialis 2013V-1197 in DMG and sarcosine as sole carbon sources. Phylogenetic analysis revealed the catabolism cluster did not share a common ancestor among vibrios.