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Microbial dynamics in rapidly transforming Arctic proglacial landscapes [1]

['Grace Marsh', 'École Polytechnique Fédérale De Lausanne', 'Sion', 'Darya Chernikhova', 'University Of Iceland', 'Reykjavík', 'Stefan Thiele', 'University Of Bergen', 'Bergen', 'Ianina Altshuler']

Date: 2024-07

Besides influencing the surrounding terrestrial environments, glacial retreat also affects a variety of proglacial freshwater and marine habitats [75,76]. Freshwater environments include both proglacial streams/rivers, which are formed by glacial meltwater release into the glacier forefield, as well as proglacial lakes, which can be formed when glacial meltwater is dammed by moraines or the bedrock [22]. Furthermore, freshwater from proglacial streams, lakes, and direct glacial run offs can reach the ocean and influence marine environments [76–78]. Warming in the Arctic increases glacial melting, leading to changes in water volume, flow velocity, turbidity, sediment and microbial transport, nutrient concentrations, salinity, and temperature, all of which influence the bacterial and archaeal communities in glacial streams, lakes, and the connected marine environments [79–82].

3.2.1 Freshwater proglacial streams and lakes.

Proglacial freshwater environments can consist of interconnected networks of glacial meltwater streams/rivers and proglacial lakes [3]. As there are few studies on microbial dynamics in Arctic proglacial freshwater ecosystems, currently knowledge is also supplemented with mid-latitude Alpine systems [83]. Glacial streams originate from glacial meltwater and are variable in their geochemical and geographical settings, which influences the bacterial and archaeal community of these environments, resulting in endemism [83]. Due to the low salinity, the communities found in glacial streams mostly consist of freshwater associated taxa and are often similar but distinct to those found in glaciers [78,84]. The main phyla found in glacial streams in various Arctic environments including Svalbard, Greenland, and Alaska, are Pseudomonadota, Bacteroidia, and Actinobacteria, with lower abundances of Verrucomicrobia, Acidobacteria, Planktomycetota [78,83,85,86]. While the common genera in these environments are Polaromonas, Methylotenera, Methylophilus, Nitrotoga, and Rhodoferax, this is variable between different environments [83,85,87]. The initial community of such streams is seeded mostly from the subglacial run off [77,88]. However, diversity of the community often increases downstream, which in a space-for-time approach may imply that glacial retreat and changes in the physicochemical parameters is followed by a succession in the bacterial and archaeal community, based on their metabolic capabilities and preferences, as an effect of climate change or from increased connectivity with the surrounding terrestrial environments [84,87]. The microbial communities in downstream areas of proglacial rivers are likely more influenced by the surrounding soils (e.g. Actinobacteria) and groundwater [86] compared to upstream areas closer to the glacier source [84,88,89]. This increased influence of the surrounding soil microbiota on the glacial river microbiome is also true for glacial rivers with larger catchment sizes compared to smaller ones [87]. In benthic biofilms of proglacial streams, Pseudomonadota and Bacteroidia, together with Patescibacteria and Planctomycetota, are the most dominant phyla [90,91]. While Cyanobacteria can be found in stream biofilms and microbial mats, their abundance and photosynthesis rates partially depend on the outflow volume and turbidity of glacial discharge, due to the effect of shear forces on light permeability [82,84,92]. The similarity of benthic biofilm communities to the glacial stream water communities might be due to the constant mixing of sediment particles into the water and the corresponding dispersal of microbes [93].

Groundwater microbiomes are the least studied of glacial-associated ecosystems [86]. These microbiomes are influenced by glacial runoff, specifically, community compositions depend on the type of aquifer, the source of the water, flow dynamics, and the distance to the glacier [86,94,95]. Importantly, groundwater provides an interphase between surface water and surrounding soil microbiomes [86], however this dynamic may be altered with increased glacial melt causing a shift from confined to unconfined aquifers [95]. While the groundwater and glacial river are hydrologically interconnected, they host distinct microbial communities [86,96]. Purkamo et al. (2022) found a dominance of Burkholderiales and Pseudomonadales in Icelandic glacial groundwater, but relatively low abundance of Candidatus Yanofskybacteria in comparison to glacial river water [86]. Bacterial and archaeal diversity were greater in groundwater sites with increasing distance from the river, indicating the influence of the unique environmental pressures between these glacial sub-habitats [86,96]. While no archaea were detected in the river, the groundwater archaeal communities were dominated by Woesearchaeales, highlighting the distinction between interconnected groundwater and river microbiomes [86]. Furthermore, presence of anaerobic microorganisms in groundwater was supported by Bomberg et al (2019), who detected methanogenic archaea and iron reducing bacteria in deeper groundwater [96]. However, seasonal environmental conditions impact the dynamics between shallow and deep groundwater ecosystems [97]. For example, in the summer, shallow oxygenated groundwater mixes with deeper anaerobic groundwater, driving seasonal microbial methane oxidation [97,98]. In the winter, this dynamic shifts, shallow groundwater freezes while deeper methane-rich groundwater remains active, potentially resulting in greater methane emissions [97,98]. This is corroborated by identification of methanogens in deep anaerobic groundwater (such as Bathyarchaeota) [96].

Proglacial lakes reside in the glacial forefield and are formed by, in-contact with, or directly influenced by the glacier ice margin and glacial meltwater [22]. Proglacial lakes are variable in physicochemical characteristics (although generally characterised by oligotrophy) and microbial diversity, as they often depend on the influx of glacial streams and meltwater [8,22,78]. Consequently, the microbial taxa often found in glacial lakes are similar to those in streams, characterised by the presence of Pseudomonadota, Bacteroidia, Actinobacteria, Planctomycetes, Verrucomicrobia, Chloroflexi, and at times Acidobacteria, Patescibacteria, Elusimicrobia, and Cyanobacteria, as well as microalgae and diatoms, in addition to overall low abundances of archaea [78,99–104].

Arctic proglacial lakes are increasing in numbers and extent as glaciers retreat [105]. These proglacial lakes can interrupt the delivery of meltwater and sediment to oceans and potentially act as partial freshwater reserves in place of glaciers [22]. Microbial succession in Arctic proglacial fluvio-lacustrine systems depends on gradients of environmental conditions acting on the microorganisms originating from the glacier, as well as new colonisation from the surrounding habitats (e.g., soils) [84,88,100]. While there is interconnection and sourcing of microbial taxa across the glacier and the proglacial freshwater environments, there appears to be strong taxonomic sorting across the habitats despite hydrological connectivity across environments [77,78,100]. For example, the study by Girard et al. (2023) demonstrated that while the surface of glacial ice was dominated by Cyanobacteria, the adjacent proglacial lake was dominated by an assemblage of Chloroflexi, Actinobacteriota, and Planctomycetota [78]. Interestingly, this study detected Polaromonas, a psychrophilic bacteria, across all sampled habitats (e.g. glacial and lake ice, proglacial lake and stream waters) but with unique phylotype assemblages in each habitat [78], suggesting strong sorting even at lower taxonomic levels.

Distance from the glacier and age of the proglacial lakes appear to be driving factors in microbial abundance and diversity, although without a consistent pattern. The study by Górniak et al. (2016) in an Arctic fluvio-lacustrine system (Svalbard) demonstrated that shifts in physicochemical parameters result in selective pressure on microorganisms across the proglacial field chronosequence, with higher diversity but lower biomass in the younger colder lake, closer to the glacier, compared to an older warmer downstream lake [100,106]. This was followed by increased abundance of Actinobacteria and Bacteroidota and decreased abundance of Alphaproteobacteria [100]. A similar pattern of reduced diversity with distance from the glacier was demonstrated in sediments of Icelandic proglacial lakes, Lamsters et al. (2020) showed that the oldest, least oligotrophic, furthest lake from the glacier had a considerably different community assemblage and lower taxonomic diversity compared to the younger lake that was still hydrologically connected to the glacier [102]. Contrary to these studies, a more recent analysis of five proglacial chronosequences demonstrated an increase in both bacterial cell number and diversity in older lakes, further from the glacier [8], suggesting no universal trend in proglacial lake succession. However, this could be due to differences in hydrological connectivity of the lakes or the influences of bird-driven nutrient fertilization and pH changes across the different studies [8]. Hydrological connectivity across the glacier habitats in the context of increased melt can also be important in the context of viral control of ecological dynamics. Viruses originating from glacier cryoconite holes are able to infect microbiota in downstream proglacial ponds, with increased viral abundance associated with higher host availability and higher temperatures in proglacial ponds [107].

Based on Alpine systems, turbidity seems to be a main driving factor for the bacterial and archaeal community, and the loss of turbidity due to climate change in glacial streams and connected lakes may lead to a shift in the autotrophic and heterotrophic bacterial diversity [108]. These differences between glacier fed and disconnected proglacial lakes suggest that with increased glacial retreat the proglacial lake communities may shift from chemoheterotrophic processes in connected lakes to photoautotrophy in disconnected lakes, which can result in shifts of ecosystem functions [109].

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[1] Url: https://journals.plos.org/climate/article?id=10.1371/journal.pclm.0000337

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