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.
Highlights
The sea-ice environment is characterized by temperature fluctuations across a wide range of temporal scales, from short-term (< 1 d) diurnal oscillations to long-term seasonal shifts (Mikkelsen et al, 2008; Ewert and Deming, 2013, 2014)
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 at −1°C upon salinity shifts to double and to half the starting salinity
To complement the work with field samples, we examined the use of choline by the marine psychrophile, Colwellia psychrerythraea 34H, a gammaproteobacterium originally isolated from subzero arctic marine sediments, but considered to be well-adapted to inhabiting sea ice, where the species has since been found (Methé et al, 2005; Boetius et al, 2015)
Summary
The sea-ice environment is characterized by temperature fluctuations across a wide range of temporal scales, from short-term (< 1 d) diurnal oscillations to long-term (days to months) seasonal shifts (Mikkelsen et al, 2008; Ewert and Deming, 2013, 2014) These temperature fluctuations cause corresponding changes to the salinity of brines within the porous matrix of the ice (brine salinities, if not measured directly, can be calculated from equations set forth in Cox and Weeks, 1983). The extent of these fluctuations depends on geographic location, depth within the ice, and season. In more temperate (subarctic) climes, brine salinity varies less: measurements over the entirety of the 2005–2006 sea-ice season (December through May) in Kobbefjord, Greenland, indicated that brine salinity in the upper ice (0–10 cm) varied between 10 and 70 ppt (span of 60 ppt; Mikkelsen et al, 2008).
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