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Microalgae growing on the underside of sea ice are key primary producers in polar marine environments. Their nutritional status, determined by their macromolecular composition, contributes to the region’s biochemistry and the unique temporal and spatial characteristics of their growth makes them essential for sustaining polar marine food webs. The importance of sea ice microalgae as primary producers in polar marine ecosystems means that ongoing research into climate-change driven macromolecular phenotyping is critical to understanding the implications for the regions biochemical cycling and carbon transfer.
- sea ice
- sympagic microalgae
- trophic transfer
- sea ice microalgae
- polar
- arctic
- antarctic
1. Introduction
Ice-covered seas account for approximately 10% of the global ocean surface area (34 × 106 km2) annually, with the seasonal formation and decay of sea ice playing a key role in global ocean turnover. Sea ice forms during the dark winter months reaching its maximum extent as spring commences. Therefore, in the Arctic, the maximum extent of sea ice (~15.2 × 106 km2) occurs in March, while in the Antarctic, sea ice extent reaches a maximum (~18.5 × 106 km2) in September [1] (Figure 1). Despite their asynchrony, combined, these two regions form a significant biome, providing essential habitat for many marine organisms, including diverse communities of bacteria, protists, and meiofuana [2][3][2,3].
Figure 1. Sea ice zones in both polar regions. Stippled lines indicate the maximum (SI-Max) and minimum (SI-Min) extent of sea ice in the Arctic (top left) and Southern Ocean (top right). Black open circles indicate the poles. Schematic of the spatial and temporal evolution and decay of sea ice in polar marine ecosystems. Arrows indicate seasonal changes in salinity from brine extrusion and freshwater melt, as well as light attenuation, solar angle, and mixing depth. The entrainment of microalgae into the sea ice as it forms, its proliferation and re-release into the water column during melt is also shown. I0 = percent incident irradiance.
The organisms that thrive in these vast expanses of frozen seawater, underpin polar marine biodiversity and biochemistry. In particular, photosynthetic microalgae, which become engrained into the ice as it forms (Figure 1), support polar marine food webs, and, together with heterotrophic bacteria, are principal players in the biochemical cycling of elements within the marine and sea ice environments [2]. Sea ice primary productivity and nutrient cycling is important for understanding the dynamics of seawater biochemistry, as the biomolecular composition of sea ice microalgae and the cycling of nutrients that occurs within sea ice microbial communities influences the biochemistry of seawater [4][5][4,5]. However, biochemical components can be sensitive to physical processes, including photooxidation from UV, which is determined by ice thickness or mixing depth [6][7][6,7], potentially reshaping the biochemical signature of the seawater [8][9][8,9].
The ecological importance of sea ice microalgae is attributed to their role in primary production during the frozen winter and in spring as the ice begins to melt. During the early spring, sea ice microalgae grow within the brine channel network under very low irradiances [10][11][10,11], and as the solar angle increases, spring blooms commence, marked by an increase in biomass on the underside of the ice [10][11][10,11]. The total biomass that accumulates depends on the amount of light transmitted and therefore the thickness of the ice and snow cover, as well as the duration of the growth season, with substratum melt and ice breakup ultimately forcing the end of the sea ice algae growth season [12][13][12,13].
Sea ice microalgal communities can make significant contributions to primary production in polar regions, accounting for up to 25% of total primary production in seasonally ice-covered waters and up to ~60% in perennially ice-covered Arctic waters [14][15][16][17][14,15,16,17]. However, their precise contribution to primary production varies depending on time of year and geographic location. For example, sea ice algae contributed as little as <1% to primary production in Young Sound, Greenland in 2002 [18] yet contributed ~70% of primary production in Barrow, Alaska in 2003 [19]. Whilst the contribution of sea ice microalgae to total primary productivity is generally less than that of pelagic phytoplankton, the divergence in their timing and distribution means that the sea ice microalgae subsist as an important source of nutrients and energy to the marine food web [17][20][17,20].
As primary producers, sea ice microalgae convert solar energy into carbon via photosynthesis, making light a principal driver of sea ice productivity. Photosynthates are converted into a variety of biochemical components including proteins, lipids, and carbohydrates; biomolecules that make up the majority of the cell biomass. The allocation of the photosynthetically derived carbon is largely determined by environmental conditions and is therefore dynamic, whereby the biomolecular composition of the microalgal cell reflects its physiological status [21][34]. Shifts in biochemical composition in response to environmental conditions, while important for the physiology and nutritional status of the sea ice microalgae itself, also strongly influence the productivity and nutritional value of primary consumers. For example, sea ice microalgae have been shown to contribute up to ~146% of the energy budget of Antarctic krill during the winter [22][35]. Similarly, adequate lipid supply has been shown to be critical to the survival and reproduction of zooplankton [23][24][36,37]. Over winter, large lipid reserves are particularly important for zooplankton when pelagic primary production is low [25][26][27][38,39,40]. The biomolecular stores of primary producers are therefore the cornerstone of productive marine ecosystems, and changes in the partitioning of these critical biomolecules contained in microalgae inevitably alters the supply of energy and essential compounds to higher trophic levels.
Planetary warming is causing polar environments to change rapidly [28][41], and the significant decline in sea ice is of major ecological concern [1][29][1,42]. For the past four decades, the most profound and consistent sea ice decline has been measured in the Arctic [1][28][30][1,41,43], which has experienced a decline in average September sea ice extent of ~10.1% per decade [31][32][44,45]. Concomitant with the decline in extent is a dramatic loss of thicker multi-year ice, increasing the expanse of open water in summer, with predictions of sea ice-free summers within decades [30][33][34][43,46,47]. The situation in the Antarctic is more nuanced, as the southern hemisphere sea ice extent experienced a gradual rate of increase between 1981 and 2014, after which it has been experiencing a precipitous rate of decline [35][48] amounting to a 27% reduction between 2010 and 2017 [32][45]. Given that the growing season for sea ice microalgae is already constrained to within a few months each year and seems likely to be further shortened as oceans warm and ice extent continues to decline [12][30][36][12,43,49], it is probable that in the future we will see reduced accumulation of biomass, disrupting the critical early-season food supply for the region’s primary consumers. Furthermore, as polar regions warm, light climate under the sea ice is expected to change, influencing productivity. A reduction in snow cover and declining sea ice thickness would result in higher under-ice light intensity [11]; conversely, where precipitation is expected to increase (more snow), light transmission may decline. In addition, sea surface temperatures are rising [37][50], polar oceans are acidifying [28][38][41,51], and there is an increase in freshwater input due to glacial retreat and run off [39][52]. These shifts in ecosystem condition will influence future community composition [40][41][53,54] and biomolecular partitioning of sea ice microalgae [42][43][44][45][46][47][55,56,57,58,59,60]. Therefore, accurate assessment of the direction and magnitude of these cellular changes is necessary to better understand the impact on marine biogeochemistry and carbon transfer through the polar marine food web.
2. Biomolecular Composition of Sea Ice Algae from Polar Regions
Microalgae are the primary source of biomolecules (protein, lipids, and carbohydrates) in marine ecosystems. In cells, proteins play a key role in all enzymatic processes and growth, while lipids and carbohydrates are essential components of cell membranes and form important energy reservoirs [21][25][48][34,38,61]. Particular to sea ice microalgae, lipids and antifreeze amino acids such as proline have been important evolutionary adaptations to tolerating the freezing and hypersaline conditions of the ice matrix [49][50][62,63]. The biomolecular composition of sea ice microalgae in both absolute amounts and relative proportions vary between species, making community composition a strong determinant of overall nutritional status of primary producers. Lipids are the most energy-rich biomolecules and, as such, contain much of the energy that is transferred among trophic levels [25][38]. Carbohydrates, which contribute less to energy transfer [25][38], have an important role in supplying the cellular carbon pool [51][64], and are integral for protein synthesis [52][65]. Proteins are the predominant source of amino acids [53][66] and form a cellular nitrogen reservoir [48][61]. They are a key source of nutrition for higher trophic levels [25][38]. In terms of carbon transfer through trophic webs, proteins have the highest relative efficiency [21][54][55][34,67,68], thus making protein rich species of potentially greater value in supporting secondary production. However, specific to polar regions, microalgae with high lipid content have been shown to be important for zooplankton fecundity [56][57][58][25,26,69]. Investigations into the biochemical composition of pelagic phytoplankton from the two polar regions have revealed differences in biomolecular characteristics, with Arctic waters shown to be dominated by lipid-rich cells [59][60][70,71], possibly a result of low nitrogen status. In contrast, Antarctic phytoplankton are generally found to be rich in protein [61][62][63][72,73,74]. The high protein production by these primary producers, is likely supported by the high nitrogen concentrations in the seawater [64][65][75,76], resulting in a nitrogen-rich food source for primary consumers and thus able to support a highly productive ecosystem. One study however, found high concentrations of carbohydrates during a summer bloom in the Amundsen Sea [66][77]. This was attributed to high densities of the haptophyte Phaeocystis antarctica, which is a common bloom-forming species in Antarctic waters [66][67][77,78]. It is important to note, however, that while these patterns highlight differences between the Arctic and Antarctic, these general trends for pelagic phytoplankton are derived from only a few studies, representing low temporal and spatial coverage, and thus may not capture any potential seasonal and spatial variability. While numerous studies have investigated the biomolecular composition of sea ice microalgae from both polar regions (Table 1), to date, no similar overall patterns have been observed for sea ice microalgae. However, given the propensity for sea ice microalgae to seed pelagic blooms, similar differences in key biochemical characteristics may exist for the ice communities from the two regions.Table 1. Compilation of studies that have measured biomolecules in sea ice microalgae in the Arctic and Antarctic.
| Study | Taxa | Location | Latitude, Longitude | Sampling Date | Biomolecules Investigated | ||
|---|---|---|---|---|---|---|---|
| Antarctica | An et al., 2013 | Chlamydomonas | sp. ICE-L | Zhongshan Research Station | 69° S, 77° E | N/A | Fatty acids |
| Cade-Menun & Paytan 2010 | Fragilariopsis curta, Fragilariopsis cylindrus, Nitzschia subcurvata, Phaeocystis Antarctica, Thalassiosira weissflogii, Dunaliella tertiolecta, Synechoccus sp. | Culture | N/A | N/A | Lipid, protein, carbohydrate |
||
| Gleitz & Kirst 1991 | Diatom-dominated mixed community, primarily Nitzschia sp., Chaetoceros sp., Navicula sp., Corethron sp., Rhizosolenia sp., Amphiprora sp., Dactyliosolen sp., Synedropsis sp., Tropidoneis and Phaeocystis pouchetii | Weddell Sea | 58–63° S, 55–45° W |
1988/1989 | Lipid, amino acid, carbohydrate | ||
| Mock & Kroon 2002a | Fragilariopsis curta, Navicula gelida var.-antarctica, Nitzschia medioconstricta | Weddell Sea | 70°02′ S, 06°00′ W |
March–May 1999 | Lipid, protein | ||
| Mock & Kroon 2002b | Fragilariopsis curta, Navicula gelida var.-antarctica, Nitzschia medioconstricta | Weddell Sea | 70°02′ S, 06°00′ W |
March–May 1999 | Lipid, protein | ||
| Palmisano & Sullivan 1985 | Diatom-dominated mixed community, primarily Pleurosigma sp., Nitzschia stellata, Berkeleya sp., Amphiprora kuferathii, Phaeocystis sp. and small centrics. | McMurdo Sound | 77° S, 166° W |
November–December 1983 |
Lipid, protein, polysaccharide | ||
| Teoh et al., 2004 | Chlamydomonas sp. and Navicula sp. | Windmill Islands | 66°17′ S, 110°29′ E |
N/A | Lipid, protein, carbohydrate, fatty acids | ||
| Sackett et al., 2013 | Fragilariopsis cylindrus, Chaetoceros simplex and Pseudo-nitzschia subcurvata | Southern Ocean and Prydz Bay | 66° S, 147° E, 68° S, 73° E |
N/A | Lipid, protein, carbohydrate, fatty acids, amino acids | ||
| Xu et al., 2014 | Chlamydomonas sp. ICE-L | Zhongshan Research Station | 69° S, 77° E | N/A | Lipid, fatty acids | ||
| Arctic | Lee et al., 2008a | Mixed community dominated by large chain-forming diatoms | Barrow, Alaska | 71°20′ N, 156°39′ W |
April–June 2003 | Lipid, protein, polysaccharide | |
| Lee et al., 2008b | Mixed community dominated by large chain-forming diatoms | Barrow, Alaska | 71°20′ N, 156°39′ W |
February–June 2003 |
Lipid, protein, polysaccharide | ||
| Leu et al., 2006b | Thalassiosira antarctica var. borealis | Ny-Ålesund, Svalbard | 78°55′ N, 11°56′ E |
May–June 2004 | Fatty acids | ||
| Leu et al., 2010 | Diatom-dominated mixed community, primarily Nitzschia frigida, Navicula septentrionalis and Fragilariopsis cylindrus. | Ripfjorden, Svalbard | 80° N, 22° E |
March–July 2007 | Fatty acids | ||
| Lund-Hansen et al., 2020 | Mixed diatom-dominated community. Primarily Nitzschia frigida, Nitzschia longissima and Thalassiosira sp. | Kangerlussuaq West Greenland | 66°57′ N, 50°57′ W | March 2016 | Fatty acids | ||
| Mock & Gradinger 2000 | Mixed community dominated by Nitzschia sp., Fragilariopsis sp. and Chaetoceros sp. | Barents Sea | 77°10′ N, 34°04′ E |
May–June 1997 | Lipid, protein, polysaccharides | ||
| Pogorzelec et al., 2017 | Nitzschia frigida, pennate ribbon colonies and Attheya sp. | Dease Strait, Nunavut, Canada | 69°1′ N, 105°19′ W |
March–May 2014 | Lipid, protein | ||
| Smith et al., 1987 | Mixed community | Resolute Passage, Canada | 74°41′ N, 95°50′ W |
April–June 1985 | Lipid, protein, polysaccharides | ||
| Smith et al., 1989 | Diatom-dominated mixed community, primarily Nitzschia frigida and Nitzschia grunowii | Central Canadian Arctic | 74°40′ N, 94°54′ W |
April–May 1985; 1986 | Lipid, protein, amino acid, polysaccharide | ||
| Smith et al., 1993 | Diatom-dominated mixed community | Resolute Passage, Canada | 74°41′ N, 95°50′ W |
March–June 1989 | Lipid | ||
| Smith & Herman 1992 | Diatom-dominated mixed community | Resolute Passage, Canada | 74°41′ N, 95°50′ W |
May 1987, May–June 1988 |
Lipid, protein, polysaccharide | ||
| Søreide et al., 2010 | Diatom-dominated mixed community | Ripfjorden, Svalbard | 80°27′ N, 22°29′ E |
March–July 2007 | Fatty acids | ||
| Torstensson et al., 2013 | Nitzschia lecointei | Amundsen Sea | N/A | January 2011 | Fatty acids | ||
| Torstensson et al., 2019 | Nitzschia lecointei | Amundsen Sea | N/A | N/A | Lipid, protein carbohydrate, fatty acids |
One of the strongest determinants of biomolecular composition is taxonomic composition. Phylogenetically distinct microalgal groups have been shown to vary in their proportional allocation of biomolecules. Diatoms (Orcophyta: Bacillariophyceae), for example, generally have higher lipid and lower carbohydrate content than other microalgal phyla, such as the Chlorophytes and Haptophytes [48][61]. More specifically, pennate diatoms within the sea ice have been shown to have higher lipid, fatty acid, and carbohydrate content than the centric diatoms from the same community [47][60]. Similarly, diatoms with a smaller cell volume (such as pennate diatoms) have been shown to have higher carbohydrate content than larger volume diatoms [68][79]. At the taxonomic level of species, differentiation is more subtle, but nevertheless has been shown [44][47][69][70][57,60,80,81]. However, by far most knowledge on species-specific biomolecular profiles is derived from single-species culture studies, providing a poor representation of what may be true for natural mixed communities. It is therefore important that studies on natural communities start to discriminate biomolecular profiles of individual taxa within a community if we are to improve our understanding of taxonomic biomolecular diversity.
3. Environmental Factors That Influence Bioomolecular Composition
Temperature: At the ice–water interface, temperature generally remains around −1.8 °C throughout spring, however as sea surface temperatures rise with the onset of ocean warming [37][50], it is possible that warmer temperatures will alter the biochemical composition of the algae, drive an earlier ice melt, and ultimately inhibit sea ice microalgal growth completely [11][30][11,43]. Limited work has been completed on the effects of temperature on the biochemical composition of sea ice algae, but from these few studies some patterns have emerged. Extreme subzero temperatures (−20 °C) have been associated with a decline in fatty acids, especially PUFA content [71][88]. A decline in fatty acids has been observed also under moderate temperature increases (from −1.8 °C to 3 °C), as well as in temperature increases well beyond the natural range (~15 °C) [72][71][73][74][86,88,89,90] (Figure 2A). In several Antarctic sea-ice diatoms, an increase in relative protein content and decrease in carbohydrate content have been observed with exposure to warmer (up to 3 °C) temperatures [74][90], including temperatures well above (~20 °C) the natural range for sea ice microalgae [72][86].
Figure 2. Schematic showing the direction of change (increase or decrease) in biomolecules in sea ice microalgae exposed to variations in (A) temperature, (B) salinity, (C) irradiance, (D) nitrogen concentration, and (E) pCO2. Changes are not indicative of magnitude. The different biomolecules are coded by color and line type as described in the legend. Shaded areas indicate where results from studies have revealed both a change and no change with environmental perturbation. Data were obtained from the studies listed in Table 1.
Salinity: Salinity within sea ice follows a steep gradient, from hyper-saline conditions within the brine channels (>70 ppt) to seawater and meltwater (~30 ppt) salinity levels at the ice–water interface. In hypersaline environments, such as sea ice brine channels, lipid and amino acid content have been shown to be higher than at lower salinity (~35 ppt) [44]. On the other hand, decreasing salinity (i.e., 10–20 ppt, compared to ambient levels) have resulted in increased protein [75], amino acid [44], fatty acid [74], and carbohydrate content [74] (
Salinity: Salinity within sea ice follows a steep gradient, from hyper-saline conditions within the brine channels (>70 ppt) to seawater and meltwater (~30 ppt) salinity levels at the ice–water interface. In hypersaline environments, such as sea ice brine channels, lipid and amino acid content have been shown to be higher than at lower salinity (~35 ppt) [57]. On the other hand, decreasing salinity (i.e., 10–20 ppt, compared to ambient levels) have resulted in increased protein [82], amino acid [57], fatty acid [90], and carbohydrate content [90] (
Figure 2
B).
Light: It has been shown repeatedly to determine the nutritional quality in sea ice microalgae, although the direction of change in biomolecular composition varies depending on the magnitude of change in light intensity (
Figure 2C). Primarily, a seasonally relevant change in light intensity as a result of low and high snow cover [46][76][77] and through naturally manipulated light levels [78], have been found to increase lipid synthesis over the duration of the spring bloom [19][79][80][81], with one study finding no significant correlation [82]. On the other hand, light intensity beyond the expected natural range (>100 µmol m
C). Primarily, a seasonally relevant change in light intensity as a result of low and high snow cover [59,106,116] and through naturally manipulated light levels [123], have been found to increase lipid synthesis over the duration of the spring bloom [19,83,99,100], with one study finding no significant correlation [98]. On the other hand, light intensity beyond the expected natural range (>100 µmol m
−2
s
−1) has been found to cause a decrease in lipid content [75][83] possibly due to photoinhibition limiting photosynthetic energy production and thereby biomolecular synthesis. In contrast to the general overall lipid response, PUFAs have consistently been found to decline with increasing light intensity (
) has been found to cause a decrease in lipid content [82,107] possibly due to photoinhibition limiting photosynthetic energy production and thereby biomolecular synthesis. In contrast to the general overall lipid response, PUFAs have consistently been found to decline with increasing light intensity (
Figure 2
C).
Changes in irradiance have also been shown to influence protein, amino acid, and carbohydrate content (
Figure 2
C). In mixed microalgae communities, protein and amino acids have generally been found to decrease with increasing light intensity over a realistic spring light range (3.5–40 µmol m
−2
s
−1), largely concomitant with an increase in lipid content [19][82][80][76][78]. Declines in protein have also been observed at light levels exceeding those expected in situ (40–100 µmol m
), largely concomitant with an increase in lipid content [19,98,99,106,123]. Declines in protein have also been observed at light levels exceeding those expected in situ (40–100 µmol m
−2
s
; [82]); however, at higher light levels (125–250 µmol m
−2
s
), protein allocation has been shown to increase [107].
Nutrient limitation: Nutrient limitation is less of a problem at the ice–water interface, where nutrients are continually replenished from the seawater. However, nitrogen limitation, which is a defining constraint on growth and development [11][84][85][11,126,127] and is expected to intensify with increasing ocean stratification [86][87][128,129], commonly leads to increased lipid and decreased protein content in microalgae (e.g., [88][89][90][91][130,131,132,133])
pH: Elevated pCO2 levels (~1000 μatm) over a period of ≥14 days resulted in reduced lipid [92][91] and fatty acid content [73][89], whilst shorter exposure (6 days) at the same pCO2 levels was found to have no significant effect on protein, fatty acid, or carbohydrate content [74][90], suggesting that length of exposure influences physiological response (Figure 2E). A recent study on Antarctic coastal diatoms found that high pCO2 levels resulted in a decrease in lipid content for the two largest taxa and an increase in protein content across all five taxa investigated [70][81]. Although conducted on polar pelagic algae, this study indicates that species-specific responses likely exist within sea ice communities, which has the potential to affect food web dynamics and carbon transfer in polar regions.
