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

Abstract

Abstract Bacteria within the brine network of sea ice experience temperature-driven fluctuations in salinity on both short and long temporal scales, yet their means of osmoprotection against such fluctuations is poorly understood. One mechanism used to withstand the ion fluxes caused by salinity shifts, well-known in mesophilic bacteria, is the import and export of low molecular weight organic solutes that are compatible with intracellular functions. Working with the marine psychrophilic gammaproteobacterium, Colwellia psychrerythraea 34H, and with natural microbial assemblages present in sackhole brines drained from sea ice in Kanajorsuit Bay (2013) and Kobbefjord (2014), Greenland, we measured the utilization of 14C-choline (precursor to glycine betaine, a common compatible solute) at −1°C upon salinity shifts to double and to half the starting salinity. In all cases and across a range of starting salinities, when salinity was increased, 14C-solute (choline or derivatives) was preferentially retained as an intracellular osmolyte; when salinity was decreased, 14C-choline was preferentially respired to 14CO2. Additional experiments with cold-adapted bacteria in culture indicated that an abrupt downshift in salinity prompted rapid (subsecond) expulsion of retained 14C-solute, but that uptake of 14C-choline and solute retention resumed when salinity was returned to starting value. Overall, the results indicate that bacteria in sea-ice brines use compatible solutes for osmoprotection, transporting, storing and cycling these molecules as needed to withstand naturally occurring salinity shifts and persist through the seasons. Because choline and many commonly used compatible solutes contain nitrogen, we suggest that when brines freshen and bacteria respire such compatible solutes, the corresponding regeneration of ammonium may enhance specific biogeochemical processes in the ice, possibly algal productivity but particularly nitrification. Measurements of potential nitrification rates in parallel sea-ice samples are consistent with a link between use of the compatible solute strategy and nitrification.