Comparative genomics and mutagenesis analyses of choline metabolism in the marine Roseobacter clade

Abstract

SummaryCholine is ubiquitous in marine eukaryotes and appears to be widely distributed in surface marine waters; however, its metabolism by marine bacteria is poorly understood. Here, using comparative genomics and molecular genetic approaches, we reveal that the capacity for choline catabolism is widespread in marine heterotrophs of the marine Roseobacter clade (MRC). Using the model bacterium R uegeria pomeroyi, we confirm that the bet A, bet B and bet C genes, encoding choline dehydrogenase, betaine aldehyde dehydrogenase and choline sulfatase, respectively, are involved in choline metabolism. The bet T gene, encoding an organic solute transporter, was essential for the rapid uptake of choline but not glycine betaine (GBT). Growth of choline and GBT as a sole carbon source resulted in the re‐mineralization of these nitrogen‐rich compounds into ammonium. Oxidation of the methyl groups from choline requires formyltetrahydrofolate synthetase encoded by fhs in R . pomeroyi, deletion of which resulted in incomplete degradation of GBT. We demonstrate that this was due to an imbalance in the supply of reducing equivalents required for choline catabolism, which can be alleviated by the addition of formate. Together, our results demonstrate that choline metabolism is ubiquitous in the MRC and reveal the role of Fhs in methyl group oxidation in R . pomeroyi.

Ecological Genomics of the Uncultivated Marine Roseobacter Lineage CHAB-I-5

“…Next, we discuss in detail the genetic potential of one-car- ). These compounds are produced in large amounts by all cellular organisms in the ocean (64,65). Catabolic genes for C 1 compounds, such as those encoding the NAD-dependent formate dehydrogenase (fsdD) and the formaldehyde-activating protein (fae), are rare in all the roseobacters analyzed here ( Table 4), suggesting that roseobacters in general are not competitive in the utilization of C 1 compounds.…”

Microbial Surface Colonization and Biofilm Development in Marine Environments

“…When sessile, they are usually associated with the phycospheres of diatoms, dinoflagellates, and other algae and with zooplankton fecal pellets, marine particles, and submerged surfaces (8,13,173,272,450,594,756,(759)(760)(761). These bacteria are generally heterotrophs, able to metabolize a variety of labile and recalcitrant organic substrates, including monocyclic and polycyclic aromatic hydrocarbons as well as various algal osmolytes and other metabolites (173,175,272,594,(762)(763)(764)(765)(766)(767). They usually react to and grow quickly after small increases in levels of labile organic substrates, such as amino acids, simple sugars, and DMSP, especially during the initial phase of algal blooms (8,13,252,265,272,(768)(769)(770)(771)(772).…”

Deciphering ocean carbon in a changing world

“…A full suite of DMSP gene discoveries is now enabling studies of the dominant transformation pathways and their regulation in the ocean (94,95). Similarly, the genes mediating marine bacterial transport and metabolism of organic compounds such as sulfonates (90,96), ectoine and hydroxyectoine (97), and methylamines and choline (31,98,99) have been recently elucidated through model organism systems.…”