Exopolymer particles: microbial hotspots of enhanced bacterial activity in Arctic fast ice (Chukchi Sea)

Abstract

Sea ice is an important structuring element of Arctic marine ecosystems and provides a vast low-temperature habitat for ice-associated bacteria. While it is now known that sea ice sequesters large amounts of extracellular polymeric substances (EPS) contributing significantly to its particulate organic carbon pool, the ecological role of EPS in sea ice is poorly understood. Using in situ incubations combined with a newly developed triple-staining method (Alcian Blue, DAPI, CTC), we determined the number of CTC-reducing (i.e. actively respiring) sea-ice bacteria living freely or attached to gel-like exopolymer particles. Samples were collected at 6 depths from Chukchi Sea coastal fast ice in April, May and June 2003. Concentrations of exopolymer particles ranged between 1.8 × 10 6 and 149.1 × 10 6 particles l -1 (average 4.7 × 10 6 particles l -1) and showed strong vertical gradients with maximum concentrations at the ice-water interface. Total bacterial numbers (TBN) ranged from 0.18 × 10 9 to 8.48 × 10 9 cells l -1 with an average fraction of 7.4% of actively respiring cells (range 3.0 to 17.2% of TBN). The attached bacterial fraction (range 4.6 to 28.5%, average 15.0% of TBN) showed a significantly, approximately 4 times higher proportion of actively respiring cells (average 19.6%, range 7.8 to 37.6%) when compared to the free-living fraction that had an average of 5.4% (range 1.1 to 11.2%) of actively respiring cells. In conclusion, exopolymer particles in sea ice are microbial hotspots of increased bacterial activity able to foster enhanced biogeochemical cycling.

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).…”

Role of sea ice in global biogeochemical cycles: emerging views and challenges

“…Tedesco et al [2010], using a more advanced biogeochemical component (two algal species, varying nutrient quotas in algal cells), showed that so-called survivors, i.e., single algal cells surviving adverse environmental conditions, can significantly contribute to ice algal production. Furthermore, no model at this stage includes organic matter, while organic matter storage in sea ice is quite large, with important consequences for nutrient remineralization [Meiners et al, 2008]. Finally, a 1D representation of gas dynamics in sea ice has been applied to Ar, underlining the important role of bubbles [Moreau et al, in revision], but has not yet been applied to other climatically significant biogases.…”

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

“…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.…”

“…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…”

“…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.…”