Active and dormant microorganisms on glacier surfaces

Abstract

Glacier and ice sheet surfaces host diverse communities of microorganisms whose activity (or inactivity) influences biogeochemical cycles and ice melting. Supraglacial microbes endure various environmental extremes including resource scarcity, frequent temperature fluctuations above and below the freezing point of water, and high UV irradiance during summer followed by months of total darkness during winter. One strategy that enables microbial life to persist through environmental extremes is dormancy, which despite being prevalent among microbial communities in natural settings, has not been directly measured and quantified in glacier surface ecosystems. Here, we use a combination of metabarcoding and metatranscriptomic analyses, as well as cell-specific activity (BONCAT) incubations to assess the diversity and activity of microbial communities from glacial surfaces in Iceland and Greenland. We also present a new ecological model for glacier microorganisms and simulate physiological state-changes in the glacial microbial community under idealized (i) freezing, (ii) thawing, and (iii) freeze-thaw conditions. We show that a high proportion (>50%) of bacterial cells are translationally active in-situ on snow and ice surfaces, with Actinomycetota, Pseudomonadota, and Planctomycetota dominating the total and active community compositions, and that glacier microorganisms, even when frozen, could resume translational activity within 24 h after thawing. Our data suggest that glacial microorganisms respond rapidly to dynamic and changing conditions typical of their natural environment. We deduce that the biology and biogeochemistry of glacier surfaces are shaped by processes occurring over short (i.e., daily) timescales, and thus are susceptible to change following the expected alterations to the melt-regime of glaciers driven by climate change. A better understanding of the activity of microorganisms on glacier surfaces is critical in addressing the growing concern of climate change in Polar regions, as well as for their use as analogues to life in potentially habitable icy worlds.

Keywords: activity; dormancy; extremophiles; glacier; ice; microorganisms; snow.

FIGURE 1

Field sites. (a–c) Mittivakkat glacier in SE‐Greenland; (a) the transition from the snow to the ice surface; (b) the glacier surface, and (c) a close‐up of the ice surface. (d–g) Langjökull, Iceland, (d) as seen from Kaldadalsvegur (credit: Johann Dréo, CC BY‐SA 3.0); (e) the Langjökull glacier surface; and close‐ups of the (f) snow and (g) ice surface. The scale bars in c, f, and g represent 10 cm.

FIGURE 2

Conceptual model diagram. State variables: active biomass (B ₁ ), dormant biomass (B ₂ ), and dissolved organic carbon (DOC). Transfer functions: V _B1 represents the growth of active biomass, M _B1 and M _B2 represent the maintenance of active and dormant biomass, respectively (i.e., the transformation of DOC to CO ₂ by B ₁ and B ₂ ), D _B1 and D _B2 stand for the mortality of active and dormant biomass respectively, ξ is the de‐activation of active to dormant biomass, and ϵ is the activation of dormant biomass to active biomass.

FIGURE 3

Epifluorescence microscopy. Single‐cell visualization of translational activity observed for bacteria from the ice sample MIT5 from Mittivakkat glacier. Panels from top to bottom: (a) DAPI staining of DNA in blue; (b) protein synthesis‐active cells via BONCAT in green; and (c) an overlay showing active (green) and inactive (blue) cells.

FIGURE 4

Microbial activity in in‐situ 24‐h incubations and ex‐situ longer‐term laboratory incubations. The active fraction of bacteria (as determined via BONCAT) in (a) Mittivakkat ice samples, (b) Langjökull snow samples, and (c) Langjökull ice samples. Both in‐situ (i.e., on the glacier surface) incubations (in triplicate), and an ex‐situ time‐series of laboratory incubations at 2°C after thawing from ∼6 months storage at −20°C (in singlicate), are shown. Incubation time (days) represents the sum of the incubation period prior to the addition of HPG (“pre‐incubation”) and the 24‐h incubation with HPG (“HPG‐incubation”). The outer shape of the violin plot represents the kernel density distribution of the data, where wider sections indicate a higher density of data.

FIGURE 5

Microbial community composition and activity. Stacked bar‐plots showing (a) bacterial community composition (DNA, based on 16S rRNA gene relative abundance, %) and the active community (RNA, based on 16S rRNA gene expression from total RNA, %). The most abundant ASVs are shown. The remaining ASVs within one class are combined into phylum/class. ASVs within one class share broadly the same hue. (b) Eukaryotic community composition (DNA, based on 18S rRNA gene relative abundance) and the active community (RNA, based on 18S rRNA gene expression from total RNA, %).

FIGURE 6

Modelling of active and dormant microorganisms. Simulations of active (B ₁ , yellow) and dormant (B ₂ , lilac) biomass, and DOC concentration, during idealized (a) freeze, (b) thaw, and (c) freeze–thaw conditions on a glacier surface. Red and blue bars at the top of each panel indicate the frozen (−3.0°C, blue) or thawed (0.5°C, red) state of the simulated glacier surface environment.