Ice formed in the subglacial environment can contain some of the highest
concentrations of solutes, nutrients, and microbes found in glacier systems, which can be released to downstream freshwater and marine ecosystems and
glacier forefields. Despite the potential ecological importance of basal
ice, our understanding of its spatial and temporal biogeochemical
variability remains limited. We hypothesize that the basal thermal regime
of glaciers is a dominant control on subglacial biogeochemistry because it
influences the degree to which glaciers mobilize material from the
underlying substrate and controls the nature and extent of biogeochemical
activity that occurs at glacier beds. Here, we characterize the solutes,
nutrients, and microbes found in the basal regions of a cold-based glacier
and three polythermal glaciers and compare them to those found in overlying
glacier ice of meteoric origin. Compared to meteoric glacier ice, basal ice
from polythermal glaciers was consistently enriched in major ions, dissolved
organic matter (including a specific fraction of humic-like fluorescent
material), and microbes and was occasionally enriched in dissolved
phosphorus and reduced nitrogen (
Glaciers form by the compression and metamorphism of snow and slowly deform
and flow under their own weight. A considerable portion of a glacier's ice
is of meteoric origin and receives chemical and biological inputs primarily
from the atmosphere. However, subglacial processes, including melt–freeze
events and erosion, can result in the production of basal ice near the bed.
This basal ice is typically characterized by relatively high concentrations
of solutes that are dominated by
Subglacial processes and the composition of basal ice can dramatically impact the biogeochemistry of meltwater and sediments exported from glaciers in a warming world. For example, in glaciers where surface-derived meltwater drains through the subglacial environment and comes into contact with basal ice, subglacial water, and sediments, its geochemistry (Tranter et al., 2002), nutrient content (Hawkings et al., 2014; Wadham et al., 2016), and microbial community composition (Dubnick et al., 2017) are dramatically altered. Direct links have recently been established between subglacial biogeochemical signatures and impacts on downstream environments, including downstream freshwater (Sheik et al., 2015) and fjord ecosystems (Gutiérrez et al., 2015). Similarly, during glacial retreat, the biogeochemical material contained in basal ice is released to the terrestrial landscape. These materials have been directly linked to the nutrient dynamics of glacier forefields (Kazemi et al., 2016; Mindl et al., 2007; Sattin et al., 2010) and form the basis of the soils from which many postglacial landscapes evolve (Kastovská et al., 2005).
Despite the relatively high concentration and/or unique composition of solutes, nutrients, and microbes often found in subglacial systems, as well as their potential to impact glacier forefields and downstream ecosystems, our understanding of the controls on subglacial biogeochemical processes and products remains limited. We hypothesize that the basal thermal regime plays an important role in defining the physical and biogeochemical characteristics and variability of basal ice. Since warm ice deforms more easily than cold ice and subglacial water promotes basal sliding (Iken, 1981; Iken and Bindschadler, 1986), we expect basal ice that forms and persists in fast-flowing glaciers to experience relatively “warm” conditions and have distinct biogeochemistries from basal ice that forms and persists in the relatively “cold” conditions of slow-flowing glaciers. To evaluate how the basal thermal regime affects the biogeochemical materials that glaciers mobilize from the substrate or produce and cycle within subglacial environments, we explore the solutes, nutrients, and microbes found in the basal regions of three fast-flowing polythermal outlet glaciers and the slow-flowing western margin of the Devon Ice Cap (DIC, Devon Island, Nunavut, Canada).
The Devon Ice Cap (DIC) covers an area of approximately 14 400 km
Study site indicating the geology of the surrounding substrate and flow velocity of the Devon Ice Cap. Samples were collected from three polythermal glaciers with relatively fast-flowing ice that are surrounded by Archean bedrock and two locations along the relatively slow-flowing cold-based section of the western margin.
We sampled basal ice as well as overlying meteoric glacier ice from the
Devon Ice Cap (Fig. 1). We identified basal ice near the glacier bed as an
ice facies with high debris content and an anisotropic structure that
incorporated features such as discontinuous layers, lenses, and pods of
varying size (Hubbard and Sharp, 1989;
Knight, 1997). In contrast, glacier ice is typically white, bubbly, and
horizontally stratified. Ice samples were collected from marginal ice cliff
faces, ice rubble at the base of cliff faces, and the walls of subglacial
meltwater channels. All ice samples were collected using sterile (furnaced
at 500
Prior to analysis, samples were removed from the freezer and melted at 4
All filtration equipment was rinsed three times with sample, and a minimum of 5 mL of sample was passed through each filter paper before the sample was
filtered for analysis. Glassware was acid-washed (10 % HCl for
Determinations
of soluble reactive phosphorus (SRP;
Dissolved organic carbon was
quantified using a Shimadzu TOC-5000A Total Organic Carbon Analyzer
(Shimadzu, Japan) equipped with a high-sensitivity platinum catalyst using
US EPA method no. 415.1. Five standards between 0 and 2 ppm were used
for calibration (
We used three-dimensional excitation
emission matrices (EEMs) derived from total fluorescence scans to broadly
characterize dissolved organic matter (DOM) into humic-like and protein-like
fractions and to correlate specific fluorophores with those previously
identified in the literature. DOM fluorescence was measured in ratio mode
(
Anions were quantified
using a Dionex DX-600 ion chromatograph (Dionex, USA) and methods outlined
by US EPA method no. 300.1. Cations were measured using inductively coupled
plasma – optical emission spectroscopy (ICP-OES; Thermo Scientific iCAP
6300, Cambridge, UK) and US EPA method no. 200.7. Detection limits were as follows:
50 mL of unfiltered, melted ice
was placed in a pre-weighed 50 mL dish and dried at 50
DNA was extracted from filter
papers using MO BIO's PowerSoil® DNA isolation kit following
the manufacturer's protocol but with several modifications to maximize the
efficiency of the extraction, as follows: (1) at step 14, solution C4 was
added for a total of 4 mL instead of 1200
The concentration of
Parallel factor analysis (PARAFAC) was used to decompose the complex EEMs into discrete components using the drEEM toolbox in MATLAB 2018a and methods developed by Murphy et al. (2013). Corrections were applied for instrument spectral bias and for inner filter effects, and Raman scatter was normalized to daily Raman scans (Murphy et al., 2013). The scatter region for each EEM was excised and smoothed, and EEMs were normalized to unit variance. PARAFAC was completed using non-negativity constraints, and the EEM normalization was reversed after modeling. Although the modelled components cannot be identified as specific organic compounds, they were characterized using the OpenFluor database (Murphy et al., 2014) and comparisons with previous literature. To summarize the DOM composition of each sample, the fluorescent intensity of each component was normalized to its mean and variance across the dataset and a PCA was completed.
Paired-end reads were assembled using PANDAseq (Masella et al., 2012) and analyzed using Quantitative Insights Into Microbial Ecology (QIIME, Caporaso et al., 2010), managed by the automated exploration of microbial diversity v1.5 (AXIOME, Lynch et al., 2013). Sequences were clustered with UPARSE (Edgar, 2013) into unique operational taxonomical units (OTUs) with 97 % similarity. OTUs were assigned to taxonomy via the Ribosomal Database Project (RDP) (Wang et al., 2007) with a confidence threshold of 0.8. The number of reads ranged from 7608 to 188 117 per sample so that reads were rarefied to the lowest read count (7608). The microbial assemblages in each sample were summarized by completing non-metric multidimensional scaling (NMDS) of Bray–Curtis distance measures, statistical significance between groups was determined using multi-response permutation procedure (MRPP) and multiple linear regressions to fit environmental vectors onto the NMDS (using the vegan toolbox in R).
Glacier ice and cold basal ice had relatively low solute concentrations
(
Summary of
Number, mean, and standard deviation of measures of major ions,
inorganic nutrients, and DOM components in glacier ice, warm basal ice, and
cold basal ice, and statistical tests between warm basal ice and cold basal and
glacier ice. The
n/a – not applicable.
While warm basal ice did not contain significantly more dissolved inorganic
nutrients than glacier ice, including nitrogen (TDN,
Relative abundance and range in concentrations of major ions
(top row), organic nutrients (middle row), and inorganic nutrients (bottom row) in basal
ice and glacier ice. Data were scaled to the interval 0–1. Boxplots
indicate the median, 25th, and 75th percentiles; whiskers indicate the
most extreme datapoints that are not considered outliers; and outliers are indicated
with a “
A five-component PARAFAC model explained 98.6 % of the variability in the
spectrofluorescence dataset. Two of these components were similar to
protein-like fluorescence and three were similar to humic-like fluorescence,
as described in other studies (Table 2). DOC concentrations in warm basal
ice were not significantly different from those in glacier ice (
Excitation and emission maxima for the five-component PARAFAC model, including the identification of each component.
Cold basal ice had significantly higher DOC concentrations
(
A total of 3555 OTUs were identified across the rarefied dataset. Microbial
assemblages in warm basal ice and glacier ice formed two distinct groups
(Fig. 2). A total of 76 % of the OTUs observed in warm basal ice were absent from
glacier ice (Fig. 4), suggesting that a large portion of the microbial
assemblage in warm basal ice was sourced from the subglacial environment.
Microbial assemblages in warm basal ice were also highly variable –
Venn diagrams showing overlap in membership between the microbial assemblages observed in warm basal ice, glacier ice, and cold basal ice samples. Numbers represent the number of operational taxonomic units (OTUs) that are unique to each environment or shared between environments.
The microbial assemblages in cold basal ice were broadly similar to those in glacier ice (Fig. 2). Cold basal ice shared most (73 %) OTUs with glacier ice (Fig. 4). Of the shared OTUs between cold basal ice and glacier ice, many (37 %) were absent from the warm basal ice samples. Thus, the microbial assemblages in cold basal ice remained remarkably similar to those in meteoric glacier ice, despite the potential for interactions with the substrate.
Glacier ice originates as snow in the accumulation zones of glaciers/ice caps. This ice is of meteoric origin and receives chemical and biological inputs primarily from the atmosphere, experiences consistently sub-freezing temperatures and is likely to host low rates of biogeochemical activity in the englacial system (Price and Sowers, 2004). Surface melt routed through the subglacial system, or subglacially, produced meltwater formed by geothermal and frictional heat sources may refreeze to form basal ice beneath temperate and polythermal glaciers. The interactions between ice or water and the overridden substrate can mobilize particulates and solutes and incorporate them into the base of the glacier during the formation of warm basal ice (Hubbard et al., 2009). Relatively warm temperatures (i.e. near the pressure melting point) beneath the glacier may also promote biogeochemical activity by increasing both the availability of liquid water, the rates of chemical weathering, and the metabolic rates of micro-organisms (Price and Sowers, 2004).
The subglacial conditions in cold-based glaciers differ considerably from those in temperate and polythermal glaciers because temperatures are below the pressure melting point. The modes of formation of cold basal ice can vary between glaciers and are generally poorly understood. Thus, interpretations of the environments in (and processes by) which such ice is formed are often ambiguous, making our understanding of the biogeochemistry of cold basal ice even more limited. The formation of cold basal ice is often described by the “apron entrainment model” that invokes the production of basal ice by the overriding and reworking of apron material (snow, ice blocks, refrozen melt water, and debris) along an advancing margin (Shaw, 1977). However, the dark, largely bubble-free ice and absence of coarse-grained debris in the western margin basal ice facies suggests that the apron entrainment model may not describe its mode of formation. Case studies have demonstrated that basal ice in cold-based systems can also be produced by subglacial processes including the deformation and entrainment of subglacial permafrost (Fitzsimons et al., 2008), the overriding of ice marginal lakes (Lorrain et al., 1999), and the refreezing of water produced in warm thermal zones or high-pressure zones at the glacier bed that then flows into cold thermal zones or low-pressure zones downstream, where it refreezes (Knight, 1997; Wettlaufer et al., 1996) and entrains debris and excludes gases as it accretes to the glacier sole (Gilpin, 1979; Walder, 1986).
Warm basal ice from fast-flowing glaciers was consistently enriched in
rock-derived solutes, including
Both warm and cold basal ice showed some evidence of inorganic nutrient
acquisition in the subglacial environment. The cold basal ice had relatively
high concentrations of TDP and TDN (particularly
Both warm and cold basal ice contained higher average DOC concentrations
(0.49 and 0.40 ppm, respectively) than glacier ice (0.15 ppm) (Table 1)
suggesting a potential source of DOC in subglacial systems, as observed in
Greenland
(O'Donnell et al.,
2016) and Antarctica (Wadham et al.,
2012). Compared to glacier ice, the DOM in warm and cold basal ice had
higher and more variable proportions of humic-like fluorescent material (C3
and C5) but no significant differences in the presence of C1, C2 or C4
protein-like fluorescent material (Tables 1, 2, Fig. 3). Humic DOM, and
humic-like C3 and C5 fluorescence are commonly associated with soils and
vegetation
(Cory and McKnight, 2005; Osburn et al., 2016; Stedmon et al., 2003), thus it is
possible that both the fast- and slow-flowing glaciers acquired these
compounds by direct (via abiotic leaching) and indirect (via microbial
cycling) of material from the substrate. Similar observations were made for
low molecular weight DOC compounds in previous studies of basal ice from
Greenland (O'Donnell et al.,
2016). In polythermal glaciers, high rates of mechanical weathering and
meltwater contact with the underlying substrate could facilitate the
acquisition of humic-like DOM from the substrate. While this is unlikely the
case for cold basal ice where mechanical weathering and meltwater is
limited, the sedimentary rocks near or underlying the western margin support
well-developed soils and vegetation. Therefore, even limited interaction
with the substrate could have resulted in the acquisition of significant
humic-like DOM in this cold-based system if this material was abundant in
the substrate. Previous studies have also associated humic-like C3 and C5
fluorescence with microbial processing of organic matter (Table 2),
suggesting basal ice may have acquired these components via heterotrophic
microbial activity in subglacial environments or in supraglacial or ice
marginal material that was transported into the subglacial system by
meltwater. The positive correlation between DOC concentrations in warm basal
ice and tyrosine-like C1 fluorescence (
The microbial assemblages contained in the cold basal ice were remarkably
similar to those in meteoric glacier ice; cold basal ice shared most (i.e.
73 %) OTUs with glacier ice, of which many (37 %) were unique to only
cold basal ice and meteoric glacier ice (Fig. 4). Like glacier ice, the
microbial assemblages observed in cold basal ice included Proteobacteria
(
In contrast, the microbial assemblages in warm basal ice were distinct from
those in glacier ice (Figs. 2, 4, MRPP,
Although sample location did not affect the major ion chemistry, nutrient, or organic composition of basal ice, it was an important influence on the composition of the microbial assemblages in warm basal ice. We observed that microbial assemblages in basal ice samples from the same glacier were more similar to each other than were assemblages in basal ice from different glaciers. Inter-glacier differences in basal microbial assemblages were resolved over relatively small distances (less than 100 km) and between glaciers with similar basal thermal regimes and underlying substrates (Fig. 1). Geographic location has previously been identified as an important determinant of microbial assemblages across various spatial scales, from metres (Lear et al., 2014) to global (Fuhrman et al., 2008), and within other polar environments including Antarctic and Arctic terrestrial and aquatic habitats (Comte et al., 2016; Yergeau et al., 2007), as well as on glacier surfaces (Cameron et al., 2016) and in subglacial discharge (Zarsky et al., 2018). Basal ice in different glaciers can be particularly isolated from each other, so microbial dispersal between systems is probably very limited. Furthermore, although residence times of warm basal ice within a system are difficult to estimate, they may be long enough to allow stochastic processes, such as random extinction, chance colonization, drift, and priority effects (Chase and Myers, 2011; Vellend and Agrawal, 2010), to play important roles in shaping the structure of microbial assemblages in basal ice. In contrast, basal processes within a system, including ice deformation and melt–freeze effects, would provide some degree of intra-glacial mixing of microbial assemblages and may explain the higher degree of similarity between assemblages in basal ice from the same system.
We investigated the biogeochemical properties of warm basal ice from three
polythermal glaciers that drain a region of the Devon Ice Cap that is
underlain by metasedimentary rocks and gneiss. We found samples of basal ice
from their subglacial environments to be consistently enriched in solutes
(i.e.
While basal ice in warm subglacial systems appear to have acquired abundant solutes, microbes, and nutrients from the underlying substrate, basal ice produced in cold-based systems acquired few biogeochemical characteristics from the underlying substrate. The cold basal ice explored in this study may have acquired some inorganic and organic nutrients from the substrate, but acquisition of other solutes or microbes appears to be limited. This cold basal ice acquired few solutes and microbes even though the local substrate, composed of sandstone, dolomite, limestone, and relatively well-developed soils, would have been more reactive than the metasedimentary and gneiss substrate beneath the warm-based systems. It remains unknown whether the intricacies of the biogeochemical characteristics that were observed in the cold basal ice in this study result from (i) specific characteristics of the underlying or surrounding substrate, (ii) specific glaciological and hydrological processes that occurred during the formation of the cold basal ice, or (iii) the effects of biogeochemical processes that occur in situ in cold basal ice. Further research is required to define how the cold basal ice at the western margin of the DIC developed and to better characterize the biogeochemical processes that occur in subglacial environments where liquid water is limited. Nevertheless, findings from this study suggest that basal temperature play important roles in controlling subglacial biogeochemistry and the suite of solutes, nutrients, and microbes that are either mobilized from the substrate or produced within subglacial systems.
Sequences were submitted to the National Center for Biotechnology Information Sequence Read Archive (accession number PRJNA564341). Other data from this paper are available upon request to the corresponding author.
AD conceptualized the study, AD and BD designed and completed the fieldwork, AM completed the DNA extractions in the laboratory, and AD completed the formal analysis and wrote the manuscript with reviews and edits from all authors.
The authors declare that they have no conflict of interest.
We thank the Nunavut Research Institute and the communities of Grise Fjord and Resolute Bay for permission to conduct research on Devon Island. We also thank the staff at the BASL Laboratory for chemical analyses, Chad Cuss at the SWAMP Laboratory for assistance with DOM/PARAFAC analyses, Brian Lanoil for providing laboratory facilities for completing DNA extractions, the Neufeld lab at the University of Waterloo for DNA sequencing, and past field crews on the Devon Ice Cap for accumulating such a valuable wealth of knowledge about the ice cap. We sincerely thank Maria Cavaco, Maya Bhatia, Dave Burgess, and Andy Hodson for comments and conversation that helped develop this paper and the three reviewers for providing comments that improved this paper.
This research has been supported by the Natural Sciences and Engineering Research Council of Canada (Discovery grant no. 05234-2015 and Graduate Scholarship CGSD3-475559-2015), Polar Knowledge Canada (the Northern Scientific Training Program), The W. Garfield Weston Foundation (award for Northern Research), and the Polar Continental Shelf Program (grant nos. 604-16 and 620-17).
This paper was edited by Tom J. Battin and reviewed by Marek Stibal and two anonymous referees.