Metagenomic insights into novel microbial lineages with distinct ecological functions in the Arctic glacier foreland ecosystems.

Land-terminating glaciers are retreating globally, resulting in the expansion of the ice-free glacier forelands (GFs). These GFs act as a natural laboratory to study microbial community succession, soil formation, and ecosystem development. Here, we have employed gene-centric and genome-resolved metagenomic approaches to disseminate microbial diversity, community structure, and their associated biogeochemical processes involved in the carbon, nitrogen, and sulfur cycling across three GF ecosystems. Here, we present a compendium of draft Metagenome Assembled Genomes (MAGs) belonging to bacterial (n = 899) and archaeal (n = 4) domains. These MAGs were reconstructed using a total of 27 shotgun metagenomic datasets obtained from three different GFs, including Midtre Lovénbreen glacier (Svalbard), Russell glacier (Greenland), and Storglaciaren (Sweden). The taxonomic classification revealed that 98% of MAGs remained unclassified at species levels, suggesting the presence of novel microbial lineages. The abundance of metabolic genes associated with carbon, nitrogen, and sulfur cycling pathways varied between and within the samples collected across the three GF ecosystems. Our findings indicate that MAGs from different GFs share close phylogenetic relationships but exhibit significant differences in abundance, distribution patterns, and metabolic functions. This compendium of novel MAGs, encompassing autotrophic, phototrophic, and chemolithoautotrophic microbial groups reconstructed from GF ecosystems, represents a valuable resource for further studies.

Contrasting early successional dynamics of bacterial and fungal communities in recently deglaciated soils of the maritime Antarctic.

Although microorganisms are the very first colonizers of recently deglaciated soils even prior to plant colonization, the drivers and patterns of microbial community succession at early-successional stages remain poorly understood. The successional dynamics and assembly processes of bacterial and fungal communities were compared on a glacier foreland in the maritime Antarctic across the ~10-year soil-age gradient from bare soil to sparsely vegetated area. Bacterial communities shifted more rapidly than fungal communities in response to glacial retreat; species turnover (primarily the transition from glacier- to soil-favouring taxa) contributed greatly to bacterial beta diversity, but this pattern was less clear in fungi. Bacterial communities underwent more predictable (more deterministic) changes along the soil-age gradient, with compositional changes paralleling the direction of changes in soil physicochemical properties following deglaciation. In contrast, the compositional shift in fungal communities was less associated with changes in deglaciation-induced changes in soil geochemistry and most fungal taxa displayed mosaic abundance distribution across the landscape, suggesting that the successional dynamics of fungal communities are largely governed by stochastic processes. A co-occurrence network analysis revealed that biotic interactions between bacteria and fungi are very weak in early succession. Taken together, these results collectively suggest that bacterial and fungal communities in recently deglaciated soils are largely decoupled from each other during succession and exert very divergent trajectories of succession and assembly under different selective forces.

Climate warming could increase recruitment success in glacier foreland plants.

BACKGROUND AND AIMS: Glacier foreland plants are highly threatened by global warming. Regeneration from seeds on deglaciated terrain will be crucial for successful migration and survival of these species, and hence a better understanding of the impacts of climate change on seedling recruitment is urgently needed to predict future plant persistence in these environments. This study presents the first field evidence of the impact of climate change on recruitment success of glacier foreland plants. METHODS: Seeds of eight foreland species were sown on a foreland site at 2500 m a.s.l., and at a site 400 m lower in altitude to simulate a 2·7 °C increase in mean annual temperature. Soil from the site of origin was used to reproduce the natural germination substrate. Recruitment success, temperature and water potential were monitored for 2 years. The response of seed germination to warming was further investigated in the laboratory. KEY RESULTS: At the glacier foreland site, seedling emergence was low (0 to approx. 40 %) and occurred in summer in all species after seeds had experienced autumn and winter seasons. However, at the warmer site there was a shift from summer to autumn emergence in two species and a significant increase of summer emergence (13-35 % higher) in all species except two. Survival and establishment was possible for 60-75 % of autumn-emerged seedlings and was generally greater under warmer conditions. Early snowmelt in spring caused the main ecological factors enhancing the recruitment success. CONCLUSIONS: The results suggest that warming will influence the recruitment of glacier foreland species primarily via the extension of the snow-free period in spring, which increases seedling establishment and results in a greater resistance to summer drought and winter extremes. The changes in recruitment success observed here imply that range shifts or changes in abundance are possible in a future warmer climate, but overall success may be dependent on interactions with shifts in other components of the plant community.

Chronological distribution and potential sources of persistent toxic substances in soils from the glacier foreland of Midtre Lovénbreen, Svalbard.

Despite its reputation as one of the cleanest regions globally, recent studies have identified the presence of various persistent toxic substances (PTSs) in the environmental matrices collected from Svalbard. This study investigated the chronological distribution and potential sources of 81 PTSs in soils from the glacier foreland of Midtre Lovénbreen. Soil samples (n = 45) were categorized by age based on exposure to the atmosphere due to glacier retreat in July 2014 into five age groups: 80-100 years (n = 7), 60-80 years (n = 12), 40-60 years (n = 16), 20-40 years (n = 7), and <20 years (n = 3). Concentrations of polychlorinated biphenyls (PCBs, n = 32) in soils varied with age, ranging from 0.29 to 0.74 ng g-1 dw. In addition, the concentrations of polycyclic aromatic hydrocarbons (PAHs, n = 28), perylene, and alkyl-PAHs (n = 20) in soils ranged from 21 to 80 ng g-1 dw, 2.9-62 ng g-1 dw, and 73-420 ng g-1 dw, respectively. The concentrations of PTSs were observed to be greater in older soils. Principal component analysis revealed that PCBs in soils originated from various product sources. Positive matrix factorization modeling estimated the association of PAHs in soils with potential origins, such as diesel emissions, petroleum and coal combustion, and coal. Potential sources of PAHs were mainly coal in younger soils and diesel emissions and petroleum combustion in older soils. Alkyl-PAH compositions in the soil were similar to those of bituminous coal, with a noteworthy degree of weathering observed in older soils. The accumulation rate and flux of PTSs in soils exhibited compound-specific patterns, reflecting factors such as long-range transport, fate, origin, and recent inputs. These findings can serve as baseline data for protecting and preserving polar environments.

Methylocystis dominates methane oxidation in glacier foreland soil at elevated temperature.

Methane-oxidizing bacteria (methanotrophs) play an important role in mitigating methane emissions in various ecological environments, including cold regions. However, the response of methanotrophs in these cold environments to extreme temperatures above the in-situ temperature has not been thoroughly explored. Therefore, this study collected soil samples from Longxiazailongba (LXZ) and Qiangyong (QY) glacier forelands and incubated them with 13CH4 at 35°C under different soil water conditions. The active methanotroph populations were identified using DNA stable isotope probing (DNA-SIP) and high throughput sequencing techniques. The results showed that the methane oxidation potential in LXZ and QY glacier foreland soils was significantly enhanced at an unusually high temperature of 35°C during microcosm incubations, where abundant substrate (methane and oxygen) was provided. Moreover, the influence of soil water conditions on this potential was observed. Interestingly, Methylocystis, a type II and mesophilic methanotroph, was detected in the unincubated in-situ soil samples and became the active and dominant methanotroph in methane oxidation at 35°C. This suggests that Methylocystis can survive at low temperatures for a prolonged period and thrive under suitable growth conditions. Furthermore, the presence of mesophilic methanotrophs in cold habitats could have potential implications for reducing greenhouse gas emissions in warming glacial environments.

Distinct responses of soil methanotrophy in hummocks and hollows to simulated glacier meltwater and temperature rise in Tibetan glacier foreland.

Glacier foreland soils are known to be essential methane (CH4) consumers. However, global warming and increased glacier meltwater have turned some foreland meadows into swamp meadows. The potential impact of this change on the function of foreland soils in methane consumption remains unclear. Therefore, we collected Tibetan glacier foreland soils in the non-melting season from typical microtopography in swamp meadows (hummock and hollow). Three soil moisture conditions (moist, saturated, and submerged) were set by adding glacier runoff water. Soil samples were then incubated in the laboratory for two weeks at 10 °C and 20 °C. About 5 % of 13CH4/12CH4 was added to the incubation bottles, and daily methane concentrations were measured. DNA stable isotope probing (DNA-SIP) and high-throughput sequencing were combined to target the active methanotroph populations. The results showed that type Ia methanotrophs, including Crenothrix, Methylobacter, and an unclassified Methylomonadaceae cluster, actively oxidized methane at 10 °C and 20 °C. There were distinct responses of methanotrophs to soil moisture rises in hummock and hollow soils, resulting in different methane oxidation potentials. In both hummock and hollow soils, the methane oxidation potential was positively correlated with temperature. Furthermore, saturated hummock soils exhibited the highest methane oxidation potential and methanotroph populations, while submerged hollow soils had the lowest. This suggests that the in-situ hummock soils, generally saturated with water, are more essential than in-situ hollows, typically submerged in water, for alleviating the global warming potential of swamp meadows in the Tibetan glacier foreland during the growing season.

Changes in Diversity and Abundance of Ammonia-Oxidizing Archaea and Bacteria along a Glacier Retreating Chronosequence in the Tianshan Mountains, China.

Glaciers retreating due to global warming create important new habitats, particularly suitable for studying ecosystem development where nitrogen is a limiting factor. Nitrogen availability mainly results from microbial decomposition and transformation processes, including nitrification. AOA and AOB perform the first and rate-limiting step of nitrification. Investigating the abundance and diversity of AOA and AOB is essential for understanding early ecosystem development. The dynamics of AOA and AOB community structure along a soil chronosequence in Tianshan No. 1 Glacier foreland were analyzed using qPCR and clone library methods. The results consistently showed low quantities of both AOA and AOB throughout the chronosequence. Initially, the copy numbers of AOB were higher than those of AOA, but they decreased in later stages. The AOB community was dominated by "Nitrosospira cluster ME", while the AOA community was dominated by "the soil and sediment 1". Both communities were potentially connected to supra- and subglacial microbial communities during early stages. Correlation analysis revealed a significant positive correlation between the ratios of AOA and AOB with soil ammonium and total nitrogen levels. These results suggest that variations in abundance and diversity of AOA and AOB along the chronosequences were influenced by ammonium availability during glacier retreat.

[QMEC-based Analysis of the Soil Microbial Functional Potentials across Different Tibetan Plateau Glacier Forelands].

Soil microorganisms dominate the biogeochemical cycles of elements in glacier forelands, which continue to expand due to the climate warming. We analyzed the soil microbial functional characteristics among three types of glacier forelands on the Tibetan Plateau: Yulong Glacier (Y), a temperate glacier; Tianshan Urumqi Glacier No.1 (T), a sub-continental glacier; and Laohugou Glacier No.12 (L), a continental glacier. Here, soil microbial functional genes were quantified using quantitative microbial element cycling technology (QMEC). We found that, in the three glacier forelands, the abundances of soil microbial functional genes related to hemicellulose degradation and reductive acetyl-CoA pathway were highest compared with other carbon-related functional genes. The main nitrogen cycling genes were involved in ammonification. The functional genes of the phosphorus cycle and sulfur cycle were related to organic phosphate mineralization and sulfur oxidation. Furthermore, the soils of the temperate glacier foreland with better hydrothermal conditions had the most complex microbial functional gene structure and the highest functional potentials, followed by those of the soils of continental glacier foreland with the driest environment. These significant differences in soil microbial functional genes among the three types of glacier forelands verified the impacts of geographic difference on microbial functional characteristics, as well as providing a basis for the study of soil microbial functions and biogeochemical cycles in glacier forelands.

Sink or Source: Alternative Roles of Glacier Foreland Meadow Soils in Methane Emission Is Regulated by Glacier Melting on the Tibetan Plateau.

Glacier foreland soils have long been considered as methane (CH4) sinks. However, they are flooded by glacial meltwater annually during the glacier melting season, altering their redox potential. The impacts of this annual flooding on CH4 emission dynamics and methane-cycling microorganisms are not well understood. Herein, we measured in situ methane flux in glacier foreland soils during the pre-melting and melting seasons on the Tibetan Plateau. In addition, high-throughput sequencing and qPCR were used to investigate the diversity, taxonomic composition, and the abundance of methanogenic archaea and methanotrophic bacteria. Our results showed that the methane flux ranged from -10.11 to 4.81 µg·m-2·h-1 in the pre-melting season, and increased to 7.48-22.57 µg·m-2·h-1 in the melting season. This indicates that glacier foreland soils change from a methane sink to a methane source under the impact of glacial meltwater. The extent of methane flux depends on methane production and oxidation conducted by methanogens and methanotrophs. Among all the environmental factors, pH (but not moisture) is dominant for methanogens, while both pH and moisture are not that strong for methanotrophs. The dominant methanotrophs were Methylobacter and Methylocystis, whereas the methanogens were dominated by methylotrophic Methanomassiliicoccales and hydrogenotrophic Methanomicrobiales. Their distributions were also affected by microtopography and environmental factor differences. This study reveals an alternative role of glacier foreland meadow soils as both methane sink and source, which is regulated by the annual glacial melt. This suggests enhanced glacial retreat may positively feedback global warming by increasing methane emission in glacier foreland soils in the context of climate change.

Glacier retreat in the High Arctic: opportunity or threat for ectomycorrhizal diversity?

Climate change causes Arctic glaciers to retreat faster, exposing new areas for colonization. Several pioneer plants likely to colonize recent deglaciated, nutrient-poor areas depend on fungal partners for successful establishment. Little is known about general patterns or characteristics of facilitating fungal pioneers and how they vary with regional climate in the Arctic. The High Arctic Archipelago Svalbard represents an excellent study system to address these questions, as glaciers cover ∼60% of the land surface and recent estimations suggest at least 7% reduction of glacier area since 1960s. Roots of two ectomycorrhizal (ECM) plants (Salix polaris and Bistorta vivipara) were sampled in eight glacier forelands. Associated ECM fungi were assessed using DNA metabarcoding. About 25% of the diversity was unknown at family level, indicating presence of undescribed species. Seven genera dominated based on richness and abundance, but their relative importance varied with local factors. The genus Geopora showed surprisingly high richness and abundance, particularly in dry, nutrient-poor forelands. Such forelands will diminish along with increasing temperature and precipitation, and faster succession. Our results support a taxonomical shift in pioneer ECM diversity with climate change, and we are likely to lose unknown fungal diversity, without knowing their identity or ecological importance.

Organic carbon accumulation in the glacier forelands with regard to variability of environmental conditions in different ecogenesis stages of High Arctic ecosystems.

Recently deglaciated surfaces of glacier forelands are subjected to a variety of biotic and abiotic factors that lead to continuous soil formation. Until now, no attempt has been taken to analyse multiple factors that might affect soil development in the Arctic forelands. The main aim of this research was to determine the factors that influence soil development in the eight forelands of Svalbard. Moreover, the effects of both habitat type (glacier foreland and mature tundra) and geographical location on environmental variables treated as potential factors influencing soil formation were tested. In 2017, at each location a series of 1 m2 plots was established; all 168 plots were investigated in terms of soil properties, spatial data, biological soil crusts (BSCs) properties, percent cover of BSCs and vascular plants. Stepwise multiple linear regression analysis using forward variable selection showed that soil development was significantly associated with six of fifteen analysed factors, i.e. BSC cover, carbon and nitrogen content in BSCs, soil pH, Topographic Wetness Index and foreland location. Two-way analysis of variance followed by Tukey's test revealed significant differences in studied environmental variables between habitat types and studied locations, showing that foreland soils still retain particular initial characters to differentiate them from tundra soil.

Combined effects of glacial retreat and penguin activity on soil greenhouse gas fluxes on South Georgia, sub-Antarctica.

The effects of soil succession after glacial retreat and fertilisation by marine animals are known to have major impacts on soil greenhouse gas (GHG) fluxes in polar terrestrial ecosystems. While in many polar coastal areas retreating glaciers open up new ground for marine animals to colonise, little is known about the combination of both factors on the local GHG budget. We studied the magnitude of GHG fluxes (CO2, CH4 and N2O) on the combined effect of glacial retreat and penguin-induced fertilisation along a transect protruding into the world's largest King Penguin (Aptenodytes patagonicus) colony at Saint Andrews Bay on sub-Antarctic South Georgia. GHG production and consumption rates were assessed based on laboratory incubations of intact soil cores and nutrients and water additional experimental incubations. The oldest soils along the transect show significant higher contents of soil carbon, nutrients and moisture and were strongly influenced by penguin activity. We found a net CH4 consumption along the entire transect with a marked decrease within the penguin colony. CO2 production strongly increased along the transect, while N2O production rates were low near the glacier front and increased markedly within the penguin colony. Controlled applications of guano resulted in a significant increase in CO2 and N2O production, and decrease in CH4 consumption, except for sites already strongly influenced by penguin activity. The results show that soil microbial activity promptly catalyses a turnover of soil C and atmospheric methane oxidation in de-glaciated forelands. The methane oxidizers, however, may increase relatively slowly in their capacity to oxidise atmospheric CH4. Results show also that the increase of nutrients by penguins reduces CH4 oxidation whereas N2O production is greatly increased. A future expansion of penguins into newly available ice-free polar coastal areas may therefore markedly increase the local GHG budget.

Primary Succession of Nitrogen Cycling Microbial Communities Along the Deglaciated Forelands of Tianshan Mountain, China.

Structural succession and its driving factors for nitrogen (N) cycling microbial communities during the early stages of soil development (0-44 years) were studied along a chronosequence in the glacial forelands of the Tianshan Mountain No.1 glacier in the arid and semi-arid region of central Asia. We assessed the abundance and population of functional genes affiliated with N-fixation (nifH), nitrification (bacterial and archaeal amoA), and denitrification (nirK/S and nosZ) in a glacier foreland using molecular methods. The abundance of functional genes significantly increased with soil development. N cycling community compositions were also significantly shifted within 44 years and were structured by successional age. Cyanobacterial nifH gene sequences were the most dominant N fixing bacteria and its relative abundance increased from 56.8-93.2% along the chronosequence. Ammonia-oxidizing communities shifted from the Nitrososphaera cluster (AOA-amoA) and the Nitrosospira cluster ME (AOB-aomA) in younger soils (0 and 5 years) to communities dominated by soil and sediment 1 (AOA-amoA) and Nitrosospira Cluster 2 Related (AOB-aomA) in older soils (≥17 years). Most of the denitrifers closest relatives were potential aerobic denitrifying bacteria, and some other types of denitrifying bacteria (like autotrophic nitrate-reducing, sulfide-oxidizing bacteria and denitrifying phosphorus removing bacteria) were also detected in all soil samples. The regression analysis showed that N cycling microbial communities were dominant in younger soils (0-5 years) and significantly correlated with soil total carbon, while communities that were most abundant in older soils were significantly correlated with soil total nitrogen. These results suggested that the shift of soil C and N contents during the glacial retreat significantly influenced the abundance, composition and diversity of N cycling microbial communities.

Soil fungal community assembly in a primary successional glacier forefront ecosystem as inferred from rDNA sequence analyses.

• Soil fungal community assembly in nonvegetated areas on the forefront of a receding glacier was analyzed by cloning of the PCR-amplified partial small subunit (18S) of the ribosomal RNA genes (rDNA) from soil DNA samples. • Fungal sequences obtained from areas adjacent to the present glacier terminus (young substrate) represented three fungal phyla, whereas those obtained adjacent to the terminal moraine (old substrate) were distributed among Ascomycetes and Hymenomycetes. The cloned sequences from both substrates represented mainly filamentous ascomycetes or basidiomycetes with a likely affinity to Agaricales. Unexpected biotrophic fungi with affinities to Taphrinomycetes, Urediniomycetes (the rust fungi) and Ustilaginomycetes (the smut fungi) plus an unknown, likely chytridiomycetous group were detected exclusively in the young substrates. • These observations of biotrophic fungi are attributed to an aerially deposited, dormant spore bank, which may also be present in the older substrate but is masked by larger active mycelial biomass. • This study underlines the importance of stochastic events and airborne spore deposition in the assembly of early fungal communities.