Sea ice microorganisms: environmental constraints and extracellular responses

Abstract

Inherent to sea ice, like other high latitude environments, is the strong seasonality driven by changes in insolation throughout the year. Sea-ice organisms are exposed to shifting, sometimes limiting, conditions of temperature and salinity. An array of adaptations to survive these and other challenges has been acquired by those organisms that inhabit the ice. One key adaptive response is the production of extracellular polymeric substances (EPS), which play multiple roles in the entrapment, retention and survival of microorganisms in sea ice. In this concept paper we consider two main areas of sea-ice microbiology: the physico-chemical properties that define sea ice as a microbial habitat, imparting particular advantages and limits; and extracellular responses elicited in microbial inhabitants as they exploit or survive these conditions. Emphasis is placed on protective strategies used in the face of fluctuating and extreme environmental conditions in sea ice. Gaps in knowledge and testable hypotheses are identified for future research.

Figure 1

Dependence of brine volume fraction (a) and brine salinity (b) on sea-ice temperature, according to phase equations from Cox and Weeks [21]. Contour lines in (a) indicate the effect of different bulk salinities on brine volume fraction. Brine salinity (b) is independent of bulk ice salinity, conventionally determined only by temperature; we suggest, by the shadowing of the line, that the presence of extracellular polymeric substances (EPS) produced by sea-ice organisms may influence brine salinity in as yet unpredictable ways (see Section 3.3).

Figure 2

Schematic diagram of seasonal (fall through winter) processes influencing microorganisms in sea ice, including transport mechanisms (orange arrows) and some of the microbial adaptive responses (italics). During sea-ice formation, larger organisms ascend with rising frazil ice crystals; smaller bacteria and archaea likely attach to algae, particles or ice crystals. Once entrained in the ice, microorganisms inhabit a network of brine channels where they experience low temperature (T), high brine salinity (S) and reduced living space, but are protected from fluctuations in air temperature by the insulating properties of snow and ice. As sea ice consolidates, brines are expelled into the ocean (desalination) and onto the surface; a fraction of the microorganisms, EPS and other components of the brine are expelled, too. Surface-expelled brines and their contents form a skim layer that can be incorporated into frost flowers and snow, prone to wind dispersal. The skim layer and frost flowers, directly exposed to the atmosphere, experience more extreme fluctuations in temperature and brine salinity and, as the sun rises in late winter, greater UV exposure. From remaining areas of open water, including leads, wind can transport marine microorganisms in aerosols. Airborne microorganisms (including terrestrial bacteria) can nucleate snow and return to the ice/snow surface.

Figure 3

Temperature recorded at the Mass Balance Observatory Site (Barrow, AK, USA) during 2011 (days of year 25–158) at different depths above and below the ice surface. Dashed lines mark seasonal transitions. Spring equinox was on day 79, summer solstice on day 171.

Figure 4

Brine salinity estimated from temperature data in Figure 3. Depths and dashed lines as in Figure 3. Brine salinity calculated using air temperature represents the extreme situation in which expelled sea-ice brines are directly exposed to the atmosphere and in thermal equilibrium with it.

Figure 5

Absorption spectra for pEPS solution concentrated from surface samples of winter first year ice (open circles, 13 mg glu-eq mL⁻¹) and saline snow (filled circles, 9.3 mg glu-eq mL⁻¹). Samples were collected offshore Barrow, Alaska, in February 2010, filtered onto 0.4 µm polycarbonate filters as described by Ewert and collaborators [48], kept frozen in the dark at −20 °C for 20 months, and resuspended in 1.5 mL of distilled water for analysis.

Figure 6

Conductometric titration of polysaccharide solutions with CaCl₂ (0.05 M). Each data point shows the effect of increasing concentration of CaCl₂ on preexisting solutions of polysaccharide (0.5 g L⁻¹). Value in parentheses is the slope of the titration curve. Slopes were calculated using linear regressions, all of which have R > 0.99 and p value < 0.001. Experiments were performed at room temperature, with less than 1 degree difference among treatments (blank, 22.0 °C ± 0.1; dextran, 22.1 °C ± 0.1; xanthan 22.0 °C ± 0.1; 34H EPS, 22.9 °C ± 0.1). Cell-free EPS from strain 34H was extracted by centrifugation and precipitation with ethanol as in [111], followed by freeze-drying.