An inter-order horizontal gene transfer event enables the catabolism of compatible solutes by Colwellia psychrerythraea 34H

Abstract

Colwellia is a genus of mostly psychrophilic halophilic Gammaproteobacteria frequently isolated from polar marine sediments and sea ice. In exploring the capacity of Colwellia psychrerythraea 34H to survive and grow in the liquid brines of sea ice, we detected a duplicated 37 kbp genomic island in its genome based on the abnormally high G + C content. This island contains an operon encoding for heterotetrameric sarcosine oxidase and is located adjacent to several genes used in the serial demethylation of glycine betaine, a compatible solute commonly used for osmoregulation, to dimethylglycine, sarcosine, and glycine. Molecular clock inferences of important events in the adaptation of C. psychrerythraea 34H to compatible solute utilization reflect the geological evolution of the polar regions. Validating genomic predictions, C. psychrerythraea 34H was shown to grow on defined media containing either choline or glycine betaine, and on a medium with sarcosine as the sole organic source of carbon and nitrogen. Growth by 8 of 9 tested Colwellia species on a newly developed sarcosine-based defined medium suggested that the ability to catabolize glycine betaine (the catabolic precursor of sarcosine) is likely widespread in the genus Colwellia. This capacity likely provides a selective advantage to Colwellia species in cold, salty environments like sea ice, and may have contributed to the ability of Colwellia to invade these extreme niches.

Choline Catabolism in Burkholderia thailandensis Is Regulated by Multiple Glutamine Amidotransferase 1-Containing AraC Family Transcriptional Regulators

“…The ability to utilize GB as a compatible solute, providing protection against osmotic and other stresses without creating significant disruption of normal cell processes, is nearly ubiquitous among bacteria; however, the ability to catabolize GB is not as widespread (46). B. thailandensis and other species in this genus possess the enzymes for utilizing choline and its metabolites as carbon and nitrogen sources, taking advantage of this widely available biomolecule as befits their description as metabolically adaptable bacteria.…”

Bacterial use of choline to tolerate salinity shifts in sea-ice brines

“…Osmolyte respiration would yield energy for metabolism and growth (consistent with the genetic potential of C. psychrerythraea 34H and its ability to grow on choline; Collins and Deming, 2013) in the absence of any external input of resources for heterotrophs (or autotrophs). Thus could individual bacteria (and archaea) in sea-ice brines withstand the seasonal increase in salinity with the approach of winter and decrease in salinity with the onset of warmer seasons, as well as any transient or abrupt shifts in salinity.…”

“…C. psychrerythraea 34H possesses genes that code for the specific transport of choline (and other compatible solutes) into the cell, the conversion of choline to glycine betaine (and beyond), and the release of solutes like choline through mechanosensitive ion channels (Collins and Deming, 2013;Ewert and Deming, 2014), yet kinetic studies on the use of choline or any other solute by this psychrophile had not been performed. Another cold-adapted (psychrotolerant) marine gammaproteobacterium, Psychrobacter sp.…”

“…Numerous small organic compounds, particularly sugars and amino acids, can serve as effective compatible solutes; among these, glycine betaine (N,N,N-trimethylglycine) is considered a potent compatible solute and is used by a wide spectrum of marine microorganisms (Kiene, 1998;Keller et al, 1999;Armbrust et al, 2004;Collins and Deming, 2013). Halophilic eubacteria, for example, accumulate betaine intracellularly in proportion to the salinity of the culturing medium (Imhoff and Rodriguez-Valera, 1984).…”

Bacterial Community Structures in Freshwater Polar Environments of Svalbard

“…However, psychrophiles overcome these severe conditions through complex adaptive mechanisms. Increased membrane fluidity at lower temperatures (59), the accumulation of compatible osmolytes and secretion of anti-freezing proteins (16, 26), the induction of cold-shock proteins (32), and conformational flexibility of psychrophilic enzymes (56) are among the main adaptive strategies adopted by the cryophilic microbiota.…”