Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic

Abstract

The physical properties of Arctic sea ice determine its habitability. Whether ice-dwelling organisms can change those properties has rarely been addressed. Following discovery that sea ice contains an abundance of gelatinous extracellular polymeric substances (EPS), we examined the effects of algal EPS on the microstructure and salt retention of ice grown from saline solutions containing EPS from a culture of the sea-ice diatom, Melosira arctica. We also experimented with xanthan gum and with EPS from a culture of the cold-adapted bacterium Colwellia psychrerythraea strain 34H. Quantitative microscopic analyses of the artificial ice containing Melosira EPS revealed convoluted ice-pore morphologies of high fractal dimension, mimicking features found in EPS-rich coastal sea ice, whereas EPS-free (control) ice featured much simpler pore geometries. A heat-sensitive glycoprotein fraction of Melosira EPS accounted for complex pore morphologies. Although all tested forms of EPS increased bulk ice salinity (by 11-59%) above the controls, ice containing native Melosira EPS retained the most salt. EPS effects on ice and pore microstructure improve sea ice habitability, survivability, and potential for increased primary productivity, even as they may alter the persistence and biogeochemical imprint of sea ice on the surface ocean in a warming climate.ice algae | permeability | polysaccharides | saline ice O ver the past few decades, the extent and thickness of Arctic sea ice have undergone significant climate-driven reductions that show no abatement (1-3). Current polar ecosystems depend on sea ice as a platform for foraging and reproduction by marine organisms and as a porous matrix that supports extensive blooms of ice algae. In the Arctic, these blooms account for a seasonally early and dominant fraction of total spring primary production (4). With continued reductions in areal extent of summer sea ice, however, phytoplankton activity in open waters is expected to dominate total primary production (5), leading to shifts away from ecosystems supported by fluxes of ice-algal material to the seafloor (6) toward pelagic ecosystems characteristic of lower latitudes (7). Predictions of reduced ice-algal production, however, do not consider the possibility that changes to sea ice microstructure and physical properties may stimulate primary productivity in the remaining ice.Here we reframe the question of how large-scale losses of Arctic sea ice will impact ecosystems and ask instead whether organisms-in particular sea-ice algae-have evolved means to alter ice physical properties to their benefit, mitigating impacts of climate change. The mechanism we consider derives from the biological production of extracellular polysaccharide substances (EPS)-organic materials of high surface area and complex behavior in aqueous solution (8)-observed microscopically in the brine inclusions of sea ice, where they are thought to function as cryoprotectants (9) and osmoprotectants (10). Do these substances also alter the microstructure of the...

Bacterial genome replication at subzero temperatures in permafrost

“…One possible mechanism to account for the differential temperature response in our experimental microcosms is the change in solute concentrations in the remaining liquid water surrounding the soil particles that occur with decreasing temperatures. Increases in both the production of extracellular polymeric substances (acting as cryoprotectants) and in bacterial abundance under similar subzero temperature conditions have been observed in brine channels from sea ice and frost flowers (Krembs et al, 2002;Collins et al, 2008;Meiners et al, 2008;Bowman and Deming 2010;Krembs et al, 2011). This hypothesis is further supported by recent evidence that permafrost isolates have thermohaline-dependent responses for both polysaccharide and fatty acid composition (Ponder et al, 2005) as well as for gene expression patterns (Mykytczuk et al, 2013).…”

A Unique Capsular Polysaccharide Structure from the Psychrophilic Marine Bacterium Colwellia psychrerythraea 34H That Mimics Antifreeze (Glyco)proteins

“…22 The synthesis of extracellular polysaccharides appears to be important to cold-adaptation of this strain, especially in subfreezing environments. 12,17,23,24 Data reported here unravel the structure of a capsular polysaccharide surrounding individual cells of C. psychrerythraea 34H (Figure 1), which in turn defines the organism's interface with its environment. The results of chemical and spectroscopic analyses of the purified capsular material revealed a structure new among bacterial polysaccharides: a linear tetrasaccharide repeating unit containing two amino sugars and two uronic acids, of which one is amidated by a threonine (Figure 4).…”

Broad-scale predictability of carbohydrates and exopolymers in Antarctic and Arctic sea ice

“…1). dCHO are concentrated from sea ice DOC by dialysis (>8 kDa), with subsequent treatment allowing the definition of four subcomponents of the total dCHO pool: (i) dissolved uronic acids (dUA), produced by ice diatoms and ice bacteria (14-16), that confer strong cross-linkages between polymer chains (8), forming low solubility EPS complexes within brine channels (8,14,17); (ii) dEPS, produced by sea ice algae (9,12,18,19) and isolated from dCHO by 70% (vol/vol) alcohol precipitation; (iii) a low solubility fraction of dEPS obtained by 30% (vol/vol) alcohol precipitation, containing complex EPS molecules (dEPS complex ), often produced by algae with reduced biological activity or when under physiological stress (9, 13, 19); and (iv) a fraction of highly soluble carbohydrates that are not considered EPS (dCHO non-EPS ), do not precipitate in alcohol, and are produced by many actively growing ice algae (9, 14).The bacteria and algae that successfully colonize sea ice habitats have mechanisms that enable them to survive temperatures less than −20°C and salinities >100 in the sea ice brines (17,20). However, there is increasing evidence that the processes of seawater freezing can be biologically mediated by ice-binding proteins and EPS secreted by bacteria and algae.…”

“…However, there is increasing evidence that the processes of seawater freezing can be biologically mediated by ice-binding proteins and EPS secreted by bacteria and algae. These compounds can alter ice structure (14,15,(21)(22)(23)(24)(25)(26) and, in the case of EPS, also form physico-chemical buffers between the organisms and the surrounding brines and ice matrix (9,14,17).When sea ice melts, its dissolved and particulate constituents are released into the surface waters (27, 28), contributing to the microbial dynamics in both the melting ice and melt waters (19,(29)(30)(31). Physical aggregation of EPS in seawater to form larger particles may promote the sinking of particulate organic matter from the surface waters (19, 32), or produce EPS foams that are Significance Many marine microalgae and bacteria secrete polysaccharide gels (exopolymers) in response to environmental stresses, such as the freezing temperatures and salt concentrations that organisms experience when in sea ice.…”