Icy worlds in the solar system and beyond have attracted a remarkable attention as possible habitats for life. The current consideration about whether life exists beyond Earth is based on our knowledge of life in terrestrial cold environments. On Earth, glaciers and ice sheets have been considered uninhabited for a long time as they seemed too hostile to harbor life. However, these environments are unique biomes dominated by microbial communities which maintain active biochemical routes. Thanks to techniques such as microscopy and more recently DNA sequencing methods, a great biodiversity of prokaryote and eukaryote microorganisms have been discovered. These microorganisms are adapted to a harsh environment, in which the most extreme features are the lack of liquid water, extremely cold temperatures, high solar radiation and nutrient shortage. Here we compare the environmental characteristics of icy worlds, and the environmental characteristics of terrestrial glaciers and ice sheets in order to address some interesting questions: (i) which are the characteristics of habitability known for the frozen worlds, and which could be compatible with life, (ii) what are the environmental characteristics of terrestrial glaciers and ice sheets that can be life-limiting, (iii) What are the microbial communities of prokaryotic and eukaryotic microorganisms that can live in them, and (iv) taking into account these observations, could any of these planets or satellites meet the conditions of habitability? In this review, the icy worlds are considered from the point of view of astrobiological exploration. With the aim of determining whether icy worlds could be potentially habitable, they have been compared with the environmental features of glaciers and ice sheets on Earth. We also reviewed some field and laboratory investigations about microorganisms that live in analog environments of icy worlds, where they are not only viable but also metabolically active.

Glaciers are populated by a large number of microorganisms including bacteria, archaea and microeukaryotes. Several factors such as solar radiation, nutrient availability and water content greatly determine the diversity and abundance of these microbial populations, the type of metabolism and the biogeochemical cycles. Three ecosystems can be differentiated in glaciers: supraglacial, subglacial and englacial ecosystems. Firstly, the supraglacial ecosystem, sunlit and oxygenated, is predominantly populated by photoautotrophic microorganisms. Secondly, the subglacial ecosystem contains a majority of chemoautotrophs that are fed on the mineral salts of the rocks and basal soil. Lastly, the englacial ecosystem is the least studied and the one that contains the smallest number of microorganisms. However, these unknown englacial microorganisms establish a food web and appear to have an active metabolism. In order to study their metabolic potentials, samples of englacial ice were taken from an Antarctic glacier. Microorganisms were analyzed by a polyphasic approach that combines a set of -omic techniques: 16S rRNA sequencing, culturomics and metaproteomics. This combination provides key information about diversity and functions of microbial populations, especially in rare habitats. Several whole essential proteins and enzymes related to metabolism and energy production, recombination and translation were found that demonstrate the existence of cellular activity at subzero temperatures. In this way it is shown that the englacial microorganisms are not quiescent, but that they maintain an active metabolism and play an important role in the glacial microbial community.

Global warming is having a great impact on the Arctic region, due to the change of air temperature and precipitation. As a consequence, the glacial ice melts and englacial materials are being transported into the ocean. These substances can constitute a source of nutrients in food webs or, on the contrary, a source of contaminants. In this research seven marine Svalbard glaciers and their tidewater tongues were focused. This survey provides a first attempt comparing microbial communities from coastal and tidewater glaciers that reveal a hitherto unknown microbial diversity. A wider diversity was found in glaciers than in seawater samples. Glacier microorganisms mainly corresponded to the phylum Proteobacteria (48.8%), Bacteroidetes (29.1%) and Cyanobacteria (16.3%) (Figure 3A). Seawater microorganisms belonged to Bacteroidetes (40.3%), Actinobacteria (31.7%) and Proteobacteria (25.4%). Other phyla found such as Firmicutes, Thermi, Gemmatimonadetes, Verrucomicrobia, Nitrospirae, Chloroflexi, Planctomycetes, and Chlamydiae were less abundant. The distribution of microbial communities was affected in different extent by the concentration of nutrients (nitrogen nutrients, dissolved organic carbon and soluble reactive phosphorus) and by environmental parameters such as salinity. Nevertheless, the environmental variables did not influence in the distribution of the microbial communities as much as the concentration of nutrients did. Our results demonstrate an interchange between glacier and coastal microbial populations as well as the presence of some indicator species (i.e., Hymenobacter) as possible sentinels for bacterial transport between glaciers and their downstream seawaters. The consequence of this process could be the alteration of the water composition of the fiords producing serious consequences throughout the marine ecosystem and in the cycling of globally important elements.

Mountain glaciers have generally experienced an accelerated retreat over the last 3 decades as a rapid response to current global warming. However, the response to previous warm periods in the Holocene is not well-described for glaciers of the southern Europe mountain ranges, such as the Pyrenees. The situation during the Medieval Climate Anomaly (900–1300 CE) is particularly relevant since it is not certain whether the southern European glaciers just experienced significant ice loss or whether they actually disappeared. We present here the first chronological study of a glacier located in the Central Pyrenees (NE Spain), Monte Perdido Glacier (MPG), carried out by different radiochronological techniques and a comparison with geochemical proxies from neighbouring palaeoclimate records. The chronological model evidences that the glacier persisted during the Roman period and the Medieval Climate Anomaly. The apparent absence of ice in the past ∼ 600 years suggests that any ice accumulated during the Little Ice Age has since ablated. This interpretation is supported by measured concentrations of anthropogenic metals, including Zn, Se, Cd, Hg and Pb, which have concentrations well below those typical of industrial-age ice measured at other glaciers in Europe. This study strengthens the general understanding that warming of the past few decades has been exceptional for the past 2 millennia.

Heat shock protein 90 (HSP90) is a conserved molecular chaperone that functions as part of complexes in which different client proteins target it to diverse sets of substrates. In this paper, HSP90 complexes were investigated in γ-proteobacteria from mild (Shewanella oneidensis) and cold environments (Shewanella frigidimarina and Psychrobacter frigidicola), to determine changes in HSP90 interactions with client proteins in response to the adaptation to cold environments. HSP90 participation in cold adaptation was determined using the specific inhibitor 17-allylamino-geldanamycin. Then, HSP90 was immunoprecipitated from bacterial cultures, and the proteins in HSP90 complexes were analyzed by two-dimensional gel electrophoresis and identified by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. According to HSP90-associated protein analysis, only 15 common proteins were found in both species from the same genus, S. oneidensis and S. frigidimarina, whereas a significant higher number of common proteins were found in both psychrophilic species S. frigidimarina and P. frigidicola 21 (p < 0.001). Only two HSP90-interacting proteins, the chaperone proteins DnaK and GroEL, were common to the three species. Interestingly, some proteins related to energy metabolism (isocitrate lyase, succinyl-CoA synthetase, alcohol dehydrogenase, NAD(+) synthase, and malate dehydrogenase) and some translation factors only interacted with HSP90 in psychrophilic bacteria. We can conclude that HSP90 and HSP90-associated proteins might take part in the mechanism of adaptation to cold environments, and interestingly, organisms living in similar environments conserve similar potential HSP90 interactors in opposition to phylogenetically closely related organisms of the same genus but from different environments.