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Open Access

Review

Microbial dynamics in rapidly transforming Arctic proglacial landscapes

Abstract

Arctic glacial environments are rapidly changing, as the Arctic warms at a rate three to four times faster than the global average (the phenomenon known as Arctic amplification). Microorganisms are uniquely adapted to extreme glacial environments and studying how ecological and climatic feedback loops affect the diversity of these communities is crucial to the characterisation of vulnerable Arctic habitats. Glacial landscapes span a wide range of habitats, from glacier ice to marine waters, and encompass terrestrial, aquatic, and interzonal systems. While glacier shrinkage has been the focus of scientific attention, auxiliary habitats are also impacted by rapid glacier retreat. Auxiliary habitats include terrestrial systems, such as outwash plains, vegetated periglacial environments, and aquatic systems, such as glacier-fed streams, lakes, and glacier-adjacent marine environments. Glacier recession drives high-impact changes in glacier-associated habitats: rising temperatures, increased light penetration of glacial streams, changes in nitrogen-to-phosphate ratios, and increases in availability of glacier-derived organic compounds. In turn, microbial systems in these habitats may experience changes in nutrient dynamics and shifts in community structures. The exposure of new lands by retreating glaciers may also result in increased dust and microbial dispersal into the atmosphere. Here, we discuss the effects of climate change on glacial microbiomes and the feedback loops between microbial community dynamics and the large-scale climatic processes in the Arctic. We characterise aspects of vulnerable microbial ecosystems and highlight the importance of preserving unseen microbial biodiversity. We then outline current capacities for microbial conservation, focusing on cryopreservation and biobanking. Lastly, we suggest future research directions and steps that academic and governmental institutions may take to foster research and collaboration with Indigenous communities.

Citation: Marsh G, Chernikhova D, Thiele S, Altshuler I (2024) Microbial dynamics in rapidly transforming Arctic proglacial landscapes. PLOS Clim 3(6): e0000337. https://doi.org/10.1371/journal.pclm.0000337

Editor: Sher Muhammad, ICIMOD: International Centre for Integrated Mountain Development, NEPAL

Published: June 25, 2024

Copyright: © 2024 Marsh et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

1. Introduction

The Arctic is a rapidly changing region as it warms nearly four times faster than the global average [1]. Climatic feedback loops play a central role in this Arctic amplification, contributing to increased air temperature, greater precipitation, Arctic greening, and decreased snow and ice cover [2]. Furthermore, Alaska, Arctic Canada and Greenland have experienced decreases in Arctic glacial ice mass balance since the 1980s, in addition to decreases in land ice mass balance in the Russian High Arctic [2]. The changing glacial landscapes of the Arctic have a significant impact on life inhabiting these extreme environments [3]. Microbial life, including bacteria, archaea, fungi, protists and viruses, process nutrients and mineral substrates, affect biogeochemical cycles, primary succession, and climatic feedback loops in glacial ecosystems [4,5]. As glaciers retreat, new terrestrial and freshwater habitats are formed [3,4]. Microbiota are at the forefront of soil formation in these newly exposed habitats and contribute to the weathering of rock substrates in addition to carbon and nitrogen cycling, establishing soil for the primary succession of lichens, mosses, macrofungi and plants [6]. Similarly, newly formed freshwater aquatic habitats, such as proglacial lakes, are colonised and transformed by microbial communities [3]. In these terrestrial and aquatic environments, biogeochemical interactions occur at both local and global scales, as atmospheric carbon and nitrogen sources are sequestered within the soils, streams, rivers, and lakes [7,8].

Exploring glacial microbial diversity and microbial interactions with climate change in the Arctic are essential to modelling future microbial and environmental dynamics in this region [9]. Microbial community analyses may also enable biomonitoring of ecosystem health, as community structures may shift with environmental changes [10]. However, this sensitivity also leaves microbial communities vulnerable to dysbiosis and potential loss of taxa, emphasising the importance of capturing this diversity before it is lost [9]. This may be achieved through utilisation of biobanks and cryopreservation of entire microbiomes, which are historically focused on agriculture and human microbiome applications [11–13]. Collections of Arctic microbiota may also act as sources of raw material for biotechnological research. Arctic microbiota have unique adaptations to extreme oligotrophic and cold environments that are of interest for bioprospecting [14,15]. For example, cold-adapted enzymes are useful catalysts at low temperatures, and are applied in various industries including food technology, where products are treated at low temperatures to reduce food spoilage [16,17]. Other applications include bioremediation of cold environments, such as degradation of oil contaminates by cold-adapted lipases [16], further stressing the need of preserving such specialised microbiomes for future utilisation [14,15,18].

However, microbial research in the Arctic is challenging given the remoteness and relative inaccessibility of the region. This limits sample collection, preservation and in situ analysis, with further limitations surrounding the nature of extremophilic organisms, which are generally challenging to culture and isolate [14,19]. Genetic approaches are widely used for studying Arctic microbiomes, with amplicon analysis providing insight into community composition and species abundance, while metagenomics and metatranscriptomics further characterise the functional potential and active microbial members [20]. In addition, the rise of multi-omics analysis is seen in the combination of these techniques with others such as metaproteomics and meta-metabolomics, creating a multi-layered picture of biological systems [20]. However, there is considerable lack of these types of studies employing multi-omics tools in glacier-associated environments [20,21].

We outline the current knowledge of microbial diversity and dynamics in Arctic glacier-associated environments and the interaction of these microbiomes with climate change. While we briefly discuss supraglacial, englacial and subglacial systems, the scope of this review specifically focuses on microbial dynamics in proglacial terrestrial and aquatic habitats; these include glacial outwash plains, glacial aeolian dust, proglacial streams and lakes, and the immediate marine coast [4,22]. We explore the current limitations of Arctic microbial research and suggest the next steps forward to investigate changes in this region.

2. Glacial environments

Glaciers consist of diverse ecosystems ranging from the glacial surface (supraglacial), to the internal glacial ice mass (englacial), and the region of the glacier in contact with the underlying substrate (subglacial) [23] (Fig 1). Life in these extreme environments is limited by the availability of liquid water, nutrients, electron donor/acceptors, light, oxygen, and low temperatures [19,23]. Microbial communities inhabit surface ice, cryoconite holes, glacial snow, and englacial and subglacial habitats [19,23].

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Fig 1. Ecosystem dynamics in warming glacial Arctic environments.

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2.1 Supraglacial zone

Glacial microbial research has largely focused on supraglacial habitats which are readily accessible on the glacier surface [23]. The supraglacial zone is exposed to the atmosphere and is vulnerable to immediate climatic perturbations and solar radiation [19]. The zone contains niche environments for microbial life, such as cryoconite holes [24]. Specifically, cryoconite holes are water-filled depressions that form on the glacial surface and are sites of nutrient accumulation [23,24]. The formation of these habitats is often initiated by deposition of inorganic and organic dust particles, from sources including proglacial dust, bird nesting sites and marine aerosols, which reduce surface albedo and cause localised ice melt [24–27]. The microbial composition of cryoconite holes varies to that of glacier surface ice with a larger relative abundance of prokaryotes than eukaryotes [28]. Studies suggest the existence of core cryoconite microbiomes that may be distinct and location-specific [26,27,29]. Cryoconite holes host diverse communities of microorganisms including photosynthetic algae (eg. Raphidonema and Ancylonema genera) and cyanobacteria (eg. Oscillatoriales and Nostocales orders) which can build up organic carbon and support growth of heterotrophic bacteria, fungi, predatory protists, and higher trophic level consumers, such as tardigrades [25,28,30–33]. Microbial activity and growth further decrease surface albedo in the cryoconite microenvironments, creating a positive feedback loop of accelerated melting [34].

Red snow is another phenomenon contributing to the accelerated surface melting via surface albedo reduction from microbial darkening [35]. Red snow describes the algae and associated microbial communities that grow in snow melt and are found across the Arctic [35]. The snow algae may appear red on the snow surface, due to the production of photoprotective pigments such as the carotenoid astaxanthin, and have also been observed in a variety of other colours, including green, golden-brown, pink, orange, and purple-grey [36–38]. Snow algae members of the genus Chlamydomonas and Raphidonema are prevalent across geographic regions, although it is only recently that species have been distinguished through genetic analysis [35,37]. Bacteria are commonly found alongside these algae and include Cyanobacteria, Pseudomonadota (prev. Proteobacteria), and Bacteroidota (prev. Bacteriodetes) phyla. These taxa are known to inhabit snow environments, with community compositions that are specific to geographic regions in the Arctic [35].

2.2 Englacial zone

Below the supraglacial zone the glacier grows more inhospitable with limited solar radiation, increased pressure, reduced liquid water availability and limited interstitial space within the ice interior [19]. Studies of microbial diversity in the englacial zone are restricted to ice coring techniques, with factors such as contamination posing a greater risk to results due to low microbial biomass [19]. The microorganisms in these habitats are thought to represent the historical communities deposited in the snow that formed the glacier [19]. Ice cores from Arctic glaciers and the Greenland Ice Sheet were found to consist of Cyanobacteria, Alphaproteobacteria, Actinobacteria, Bacteroidetes, WPS-2, Firmicutes, Acidobacteria, Gammaproteobacteria and Armatimonadetes [3,39]. However, detection of excess gases such as carbon dioxide, methane, and nitrous oxide in glacial ice cores has suggested the possibility of active microbial metabolism within the ice or recent microbial deposition through meltwater channels, implying that the microbiome composition may have changed from the initial deposited community [40–42]. This corroborates with the recovery of viable isolates from glacial ice cores, dated over 750,000 years old, in the Tibetan plateau [43]. Interestingly, a large proportion of supraglacial meltwater enters the englacial and subglacial regions which can cause altered temperatures [44] and potentially provide additional nutrients that stimulate microbial activity. Englacial meltwater channels present as cloudy ice when frozen and exhibit microbial communities less associated with glacial cold-adapted microbial taxa than communities from clear englacial ice, indicating the effect of local conditions on microbial diversity within the englacial zone [26,42].

2.3 Subglacial zone

The basal ice found in the deepest layer of the glacier, the subglacial zone, hosts an accumulation of nutrients transported through the preceding glacial layers by water flow [19]. The subglacial zone encompasses the basal ice of the glacier and the bedrock it grinds below, in addition to the water created from this friction, geothermal heat, and pressure [31]. This environment is predominantly anoxic, hosting methanogens and chemolithotrophs such as anaerobic nitrate reducers and sulphate reducers, while aerobic chemoheterotrophs have also been successfully cultivated from subglacial habitats [45,46]. Predominately Proteobacteria, Gracilibacteria, Bacteroidetes, Actinobacteria and Parcubacteria were identified from the subglacial environment via sampling of naled ice bodies in the glacier forefield [47]. Zdanowski et al. (2017) investigated the deposition of supraglacial cryoconites into the subglacial habitat and identified increased abundance of anaerobic cryoconite species [31]. The study suggests that with increased climate warming, cryoconite inhabiting taxa can establish within the englacial and subglacial zones as they are flushed through the glacier [31]. Cryoconite microbial migration into the subglacial habitat is yet to be explored further but may have interesting consequences for subglacial microbial diversity.

3. Proglacial environments

Glaciers exist as part of larger landscapes and interact with the surrounding terrestrial and aquatic habitats [4,22] (Figs 1 and 2). Investigating the effects of climate change on glacial microbiomes and microbiomes influenced by deglaciation requires a holistic approach that addresses the exchange of nutrients and microorganisms between atmospheric, terrestrial, and aquatic spheres. Here we focus on the changing microbiomes of the terrestrial and aquatic proglacial environments that encompass the region beyond the glacial terminus, including the glacial outwash plains, moraines, proglacial lakes and streams, and downstream marine environments [4,22] (Fig 3).

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Fig 2. Features of a typical glacial outwash plain, Kiattuut Sermiat, Narsarsuaq, Greenland Base map available at: https://www.arcgis.com/home/item.html?id=7ec08e5438304dbfa1e26181503e6fa8.

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Fig 3. Proglacial microbial studies in the Arctic.

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3.1 Terrestrial environments

3.1.1 Glacial outwash plains.

Glacial outwash plains are created from the sediment exposed as glaciers recede [4]. This sediment has been crushed by the weight of the glacier as it moves and contains limited nutrients, thus creating challenging conditions for life [4]. Despite this, microorganisms are capable of colonising this newly exposed oligotrophic environment [48]. Initial microbial colonisation of glacial outwash plains is derived from atmospheric sources and also extends to organisms originating from the adjacent supraglacial and subglacial environments [7], potentially from ephemeral fluvial connections. Glacial outwash plains provide a spatial study of microbial succession, known as a chronosequence, as newly exposed sediment at the glacier terminus transitions to more developed soils [49]. Colonisation by autotrophs and chemolithotrophs initiates soil development, and with time the microbial community shifts to include heterotrophic members [4,7,49]. The colonising microbes create nutrient stocks of available carbon and nitrogen, providing a mechanism of soil development, in addition to physical and chemical weathering of the exposed sediment [50]. Nitrogen fixing bacteria such as Geobacter, Frankia, Nostoc, Polaromonas, Bradyrhizobium, Rivularia, Pseudoanabaena and Rhodobacter were identified in Arctic glacier forefields [49,51]. These diazotrophs are important during early succession and can be found closer to the glacier terminus [7,49]. Overtime, this early primary succession can facilitate plant growth [52] and glacier outwash plains may become carbon sinks due to microbial and plant autotrophy resulting in accumulation of soil carbon stocks [4,53]. Further, multiple studies have identified increased methane uptake by aerobic methane-oxidising bacteria in older soils of Alpine and sub-Arctic glacier forefields, suggesting a possible methane sink in proglacial environments [54–56].

Microbial diversity and abundance tend to increase in more developed soils containing higher amounts of bioavailable nutrients [48]. Pessi et al. (2018) identified that cyanobacteria (predominantly filamentous) increased in abundance with soil age in multiple glacier forelands of Svalbard across the chronosequence [57]. Filamentous cyanobacteria function in soil stabilisation and can develop biological soil crusts [57]. Soil crusts have been found to facilitate initial plant establishment and are associated with greater plant density, suggesting soil stabilisation by microbial communities which aids primary succession [52,57]. While few studies focus on plant—arbuscular mycorrhizal (AM) fungi associations in the Arctic [58–61], some pioneer plants that colonize soils exposed by retreating glaciers have been found to associate with ectomycorrhizal fungi [58,62]. Studies suggest that these fungal communities in Arctic forelands will undergo taxonomic shifts with climate change [58,62].

Importantly, the diversity of microbial communities and underlying biogeochemical processes in developing outwash plains remains largely unexplored in relation to Arctic warming. Mateos-Rivera et al. (2016) determined that increases in surface temperature of sub-Arctic glacier forefield soils resulted in a more diverse microbial community that shifted from psychrophilic to psychrotolerant members [63]. Further, Bárcena et al. (2011) identified increased methane consumption in sub-Arctic glacier foreland soil incubated at 22°C compared to 10°C, indicating increased temperature influencing microbial function and highlighting the importance of investigating temperature effects in Arctic proglacial regions [56].

In addition, rapidly changing fluvial systems shape Arctic glacial outwash plains into a dynamic environment for life, an aspect which has not been explored in the literature. Of particular interest are glacier flooding events known as jökulhlaups, which are caused by geothermal or volcanic activity under the glacier or from the bursting of an ice-dammed supraglacial lake [64]. The ensuing flood passes around or through the glacier to the outwash plain where water levels are greatly increased for the span of a few days and large amounts of sediment are transported [64]. The flooding events can cause significant morphological changes to the proglacial landscape but currently the effects on terrestrial and aquatic biology are unknown. As jökulhlaup flooding events are becoming more frequent in regions such as Greenland, as a consequence of warmer temperatures [64], the effects of these floods on soil development and outflow forefield microbiomes warrants investigation.

3.1.2 Glacial aeolian dust.

The fine sediments of glacial outwash plains can be emitted into the atmosphere as dust containing bioaerosols which may be transported across large distances through atmospheric dispersal [5,65]. Proglacial environments are a significant source of dust at high latitudes and contribute to dust deposition on glacial surfaces, which reduces albedo and drives increased melt [66]. The dust can include viable cells and spores which in turn can potentially colonise new areas despite exposure to intense UV, low nutrients and extreme temperatures during atmospheric transport [67]. Few studies have focused on aerial microbial diversity in the Arctic specifically, with a study in Svalbard by Cuthbertson et al. (2017) observing predominantly Pseudomonadota, Actinobacteria, and Firmicutes in accordance with findings from other aerial bacterial studies in both polar and nonpolar regions [67,68].

Further, bioaerosols in aeolian dust can have ice nucleating properties by initiating water crystallisation at higher temperatures [5]. This phenomenon is observed in gram-negative bacteria from Gammaproteobacteria (e.g. Pseudomonas), and less commonly in gram-positive bacteria from certain species of Lysinibacillus [69,70]. The biologically induced freezing is attributed to ice nucleating activity (INA) proteins which bind water molecules in a specific structure favourable to ice crystallisation [69]. The ability of bacteria to induce freezing at higher temperatures may have developed as a way to cause frost damage to plants, resulting in the release of plant nutrients [71]. While the role of ice nucleation in bacterial species originating from the Arctic is largely unknown, it likely plays a role in reducing atmospheric residence time via precipitation [72,73].

Increased glacial dust from newly exposed proglacial outwash plains has climatic ramifications as ice nucleation from bioaerosols encourages cloud formation via glaciation of low-level clouds [5]. Specifically, Arctic mixed-phase clouds can form, which contribute to warming effects through cloud forcing [74]. Warming occurs as long-wave radiation emitted by the Earth is absorbed by mixed-phase clouds and partly emitted back to the Earth surface [74]. Cloud forcing takes place at high latitudes, including the Arctic, where incoming solar (short-wave) radiation is reduced [74]. Hence, the ice nucleating activity of glacially sourced bioaerosols can contribute to the changing climate of the Arctic.

3.2 Aquatic environments

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].

3.2.2 Marine environments.

Glacial meltwater is not only released into terrestrial environments, but also shed into marine systems, thus transporting nutrients, sediment, freshwater, and microorganisms into the coastal ocean with effects for the marine bacterial and archaeal communities and potential downstream impacts on higher trophic levels [110,111]. These glacial runoff influxes are more pronounced in the melting season and might increase with ongoing climate warming, while affecting the water column and pelagic ecosystem structure within fjords [110–112]. The transport of macro- and micro- nutrients from both land and marine terminating glaciers can include nitrogen, phosphorus, silicic acid, manganese and bioessential iron; these can increase marine productivity, and therefore zooplankton and downstream ecosystem dynamics [113–117]. Though for marine terminating glaciers, the nutrient influx dynamics into the marine photic zone depends on the glacier grounding line depth and induced upwelling of deeper nutrient-rich marine water [113,118].

The glacial runoff also creates gradients in salinity and turbidity, with turbidity sometimes causing decreases in phytoplankton productivity and tipping the system to net heterotrophy in the inner fjord compared to coastal shelf waters [119,120]. During high influx times, the microbial communities found in glacial meltwater persist in the freshwater layer and mix with marine communities, which continues until mixing and eventual lower influx lead to a homogenisation of the marine community and a disappearance of glacial derived microbiota [120]. Dissolved organic carbon (DOC) transported with the glacial meltwater may stimulate bacterial and archaeal production, while nutrients can stimulate phytoplankton production, which may have a secondary effect on the bacterial and archaeal community by additional carbon source availability [76,121,122]. However, the stimulation of phytoplankton growth again seems to be largely dependent on the turbidity of the water [121,122]. The origin of the water, whether directly from the glacier or from glacier influenced terrestrial sources, seems to be a key factor for the influx of nutrients and sediments [76]. With increased melt, the high influx of sediments with glacial runoffs can lead to a burial of glacial stream bacteria in the marine sedimentation zones [123,124]. This burial can then have implications for the oxygenation and consequently the sulfur- and iron cycling in the glacial influenced marine sediments [123,124].

4. Future perspectives

Overall research on microbiomes in Arctic glacial forefields is generally limited to phylogenetic identification [6,85,102], although some recent studies are expanding upon this with greater metagenomic insights [7,8,51]. While there are Arctic centric studies that utilise multi-omics, these are not focused on proglacial environments [21,125]. Therefore, it would be beneficial to analyse microbial function and active taxa through combinations of multi-omic technologies, including metagenomics, metatranscriptomics, metaproteomics and meta-metabolomics [20], to better understand microbial dynamics and succession in developing proglacial environments. Furthermore, while there is evidence for future carbon sequestration in proglacial terrestrial and aquatic environments [7,126], there is a lack of nuanced understanding of microbially mediated production and sequestration of greenhouse gases (carbon dioxide, methane, and nitrous dioxide) in Arctic proglacial fields. Recent innovations regarding in situ metagenomic analysis will aid the study of these extreme environments [127–129], for example metagenomic analysis was demonstrated in the field using a Nanopore MinION device and flow cell in a solar powered offline system, across a remote Icelandic ice cap [129].

While there is hydrological, nutrient, and microbial interconnectivity between supra-, en-, and sub-glacial zones [3,26,45,78,98,130], few studies approach this in a holistic way. For example, glacial microbiomes interact with the microbial systems in groundwater [95], glacier-fed streams, and lakes [78,86] –ecosystems with direct impacts on the human communities in the Arctic. Thus, research to gain better understanding of those interactions is a priority to establish baselines for future monitoring [10]. For example, future research could focus on interconnectedness of these environments (e.g. proglacial fields and cryoconites) in relation to seasonality, biogeochemical cycles, and climate change-related disturbances.

As Indigenous communities are the key stakeholders in Arctic research, researchers working in Indigenous lands should strive to avoid colonial parachute science, and work in partnerships with local communities [131]. For meaningful collaborations, it is important to consider the historical interactions of western science initiatives in the Arctic, and to ensure equitable benefit sharing between stakeholders [132]. Collaborative research can be co-productive or Indigenous-led [133], where all parties participate in writing research proposals, project planning, selection of priorities, local training (skill sharing), iterative co-managing, and co-assessing [134,135] (reference). Co-production is an inherently interdisciplinary paradigm that lends itself well to ecosystem-centred science [133,136]. These community partnerships should extend beyond the data gathering–community members should be acknowledged in publications and study results delivered back to the community. Moreover, Arctic communities have already developed recommendations for researchers to meaningfully engage with indigenous communities (e.g. ScIQ framework) [137] and online resources/databases of existing community-based monitoring (CBM) and Indigenous Knowledge (IK) projects [138,139]. Lastly, involving indigenous communities in research can also be a more sustainable approach with potential decrease in field work-associated carbon footprint [140].

As Arctic environments are rapidly changing it is important to preserve samples of current microbial diversity as baselines for future studies, environmental monitoring, conservation management and restoration of biomes, and as a bioprospecting resource for future industrial and medical applications [14,141,142]. Future basic environmental research would also benefit from reliable preservation, archival, and sharing of raw environmental samples (reference specimens) and samples in preservation solutions (e.g. ethanol, DNA/RNA ShieldTM, RNAlater®) [141,143]. This may be especially true for Arctic studies with challenging and expensive campaigns that rely on non-reproducible samples from a limited set of locations and timepoints [28,144]. Furthermore, availability of samples for reanalysis with novel techniques would facilitate reproducibility and new avenues of inquiry that were not part of the original focus (for example looking at the virome of a proglacial soil sample that was previously used solely for prokaryotic analysis) [143].

Database collections of multi-omic data are useful resources for research, lend themselves well to public access (e.g. NCBI) [145], and allow comparison between different studies. However, as sequencing and molecular techniques continue to advance, it may become increasingly difficult to compare newly generated research with older studies without access to the original source material [143,146]. Microbial domain biological resource centres (mBRCs), also known as culture collections, store and distribute microorganisms and replicable genetic and viral material, with ~790 mBRCs worldwide, holding over three million strains [147]. Government-supported initiatives to interlink mBRCs and other biodiversity archives are building international networks to support research and democratise access [148,149]. Cryopreservation can maintain bacterial diversity in phylogenetically complex samples [150]. Two common temperature options are -80°C and -196°C [151,152]. For long-term storage (over 5 years), preservation in liquid nitrogen at -196°C is recommended to avoid degradation [152–154]. Cryopreservation damage may be assessed with viability PCR, utilising the DNA-binding dye propidium monoazide (PMA) to prevent amplification of extracellular (from dead cells) and relic DNA [155]. Cryopreservation also allows mBRCs to efficiently hold large microbial inventories, which can be recovered upon thaw, and reduces the risks of genetic drift inherent in long-term sub-culturing [151–153,156]. However, most mBRC collections are confined to culturable axenic isolates and do not generally include whole microbiomes, which limits environmental microbiome research [13]. Hence, there are calls for the creation of biobanks (based on adapted mBRC infrastructure) of cryopreserved complex microbial communities, representing whole ecological microbiomes [13,141,147,157], as done for medical stool biobanks, which may aid environmental research [13]. However, more research is needed on cryopreservation protocols, to optimise microbial survival and preservation of community structures [143].

As oligotrophic Arctic samples have low microbial biomass, microbiome molecular analysis is susceptible to contamination during sample gathering and transport, and from extraction kits which can be contaminated with oligotrophic and extremophile taxa [19,142]. This can be mediated with the use of cryopreserved reference samples that can be standardised and included across different studies to enhance reproducibility and reduce impact of contaminants. Additionally, a PMA-treated field sample aliquot (immediately after collection and before cryopreserving) can help identify contaminants introduced during downstream processing [158]. Publicly funded repositories could be a future source of these shared reference samples and their associated metadata, processing history, and storage protocols [13,159,160].

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