Swiss Federal Institute for Forest, Snow and Landscape Research WSL

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Understanding the impacts of climate change on Arctic, Antarctic and Alpine permafrost microbiomes (CRYOLINK)

Project lead

Beat Frey

Project staff

Beat Stierli
Joel Rüthi
Gilda Varliero

Project duration

2017 - 2023

Financing
Beim Graben von Permafrostproben in einer Bodentiefe von 160 cm am Muot da Barba Peider, Pontresina
Digging permafrost samples at a soil depth of 160 cm at Muot da Barba Peider, Pontresina. Photo: Beat Stierli

Cold habitats represent the majority of the Earth’s biomes and permafrost, defined as the part of the soil frozen for at least two consecutive years, are widely spread on land surfaces. The Alpine region with its glaciers and permafrost is particularly affected by climate change. Thawing of alpine permafrost and melting of glaciers are the result of persistently warm conditions during recent years. For a long time, permafrost in the Alpine region was considered as a "sterile ground" in which life can only exist to a limited extent. Nowadays, it is becoming increasingly evident that these areas constitute a unique niche for cold-adapted microorganisms and should be considered as sensitive ecosystems in view of their high susceptibility to global warming.

The interdisciplinary project CryoLink explores permafrost in the Alps, the Arctic and Antarctica as a refuge for microbial life forms. For the first time, samples from alpine permafrost and glacier ice were explored for viral and microbial life. The results were surprising: some like it cold! Up to 1000 different microorganisms and several hundreds of viruses were found in over 12'000 year-old permafrost, about many of which nothing or very little is known so far. It is still unclear how these cold-adapted microorganisms survive in permafrost, how the cells can metabolize and even reproduce. The permafrost microbiome has developed various adaptive strategies to survive under extreme conditions such as nutrient and energy scarcity, no sun light, permanent low temperatures, or low liquid water availability.

Permafrost areas are considered as an ‘extreme environment’ and harbour microorganisms with an ability to adapt, not only to sub-zero temperatures, but also to low water, carbon and nutrient availability. However, these habitats constitute a unique niche for cold-adapted microorganisms. Little information is available on the ecology of microorganisms in permafrost, despite their high importance in view of their high susceptibility to global change.

These microorganisms were trapped in the permafrost and ice for thousands of years. What will happen to them when they are awakened from their "slumber" by global warming? Thawing permafrost threatens to release biological and chemical materials that have been sequestered for tens to hundreds of thousands of years. As these constituents re-enter the environment, they have the potential to disrupt ecosystem function, reduce the populations of native organisms and endanger human health.

Permafrost is an unexploited habitat with many unknown taxa and has the potential to contain novel compounds (i.e., antimicrobials; enzymes for polymer degradation). This immeasurable treasure of unknown microorganisms in ice and permafrost needs to be explored now. Permafrost in the next hundred of years will disappear by climate warming. For this, we have set up an unique collection of microbial strains (Biobank). This collection preserves microorganisms from endangered regions such as the Swiss Alps and contains so far more than 3,000 specimens. Among the microbial life we hope to find microorganisms that could be of interest to medicine and both the pharmaceutical and cosmetics industries.

Many of the microorganisms isolated from permafrost may represent a potentially novel source for enzymes and bioactive compounds that benefit human medicine and biotechnology. Our Biobank consisting of several thousand permafrost-derived strains is, therefore, a valuable resource to examine the potential of natural product formation both via bioactivity assays and genome mining. Our combination of culture-independent microbiota profiling with large-scale bacterial isolation efforts of permafrost soils will allow us to tap into this unexplored treasure of newly chemical compounds which is endangered by increasing temperatures.

The CryoLink project was granted by the Swiss National Science Foundation, Swiss Polar Institute and Ernst-Göhner Foundation to Beat Frey and started 2017.

Projects

Long-term climate experiments to study the Alpine soil microbiome

Long-term climate experiments were established to document the response of the alpine soil microbiome and soil functions to climate change.

Alpine microorganisms and climate warming (AlpBioClimDiv)

The rapidly advancing climate change in the Swiss Alps is driving glacier retreat and thawing permafrost. We are investigating the effects of these drastic changes on Alpine biodiversity.

The glacier microbiome

We are researching glaciers as a refuge for microbial life forms in the Swiss Alps. These organisms have been living in the ice for thousands of years and are now reappearing due to global warming.

Publications

Perez-Mon C., Stierli B., Plötze M., Frey B. (2022) Fast and persistent responses of alpine permafrost microbial communities to in situ warming. Sci. Total Environ. 807, 150720 (15 pp.). https://doi.org/10.1016/j.scitotenv.2021.150720Institutional Repository DORA

Frey B., Varliero G., Qi W., Stierli B., Walthert L., Brunner I. (2022) Shotgun metagenomics of deep forest soil layers show evidence of altered microbial genetic potential for biogeochemical cycling. Front. Microbiol. 13, 828977 (18 pp.). https://doi.org/10.3389/fmicb.2022.828977Institutional Repository DORA

Hicks L.C., Frey B., Kjøller R., Lukac M., Moora M., Weedon J.T., Rousk J. (2022) Toward a function-first framework to make soil microbial ecology predictive. Ecology. 103(2), e03594 (9 pp.). https://doi.org/10.1002/ecy.3594Institutional Repository DORA

Robinson S.I., O’Gorman E.J., Frey B., Hagner M., Mikola J. (2022) Soil organic matter, rather than temperature, determines the structure and functioning of subarctic decomposer communities. Glob. Chang. Biol. 28(12), 3929-3943. https://doi.org/10.1111/gcb.16158 Institutional Repository DORA

Donhauser J., Qi W., Bergk-Pinto B., Frey B. (2021) High temperatures enhance the microbial genetic potential to recycle C and N from necromass in high-mountain soils. Glob. Chang. Biol. 27(7), 1365-1386. https://doi.org/10.1111/gcb.15492 Institutional Repository DORA

de Vries F.T., Thion C., Bahn M., Bergk Pinto B., Cécillon S., Frey B., … Bardgett R.D. (2021) Glacier forelands reveal fundamental plant and microbial controls on short-term ecosystem nitrogen retention. J. Ecol. 109(10), 3710-3723. https://doi.org/10.1111/1365-2745.13748 Institutional Repository DORA

Frey B., Walthert L., Perez-Mon C., Stierli B., Köchli R., Dharmarajah A., Brunner I. (2021) Deep soil layers of drought-exposed forests harbor poorly known bacterial and fungal communities. Front. Microbiol. 12, 674160 (21 pp.). https://doi.org/10.3389/fmicb.2021.674160Institutional Repository DORA

Perez-Mon C., Qi W., Vikram S., Frossard A., Makhalanyane T., Cowan D., Frey B. (2021) Shotgun metagenomics reveals distinct functional diversity and metabolic capabilities between 12 000-year-old permafrost and active layers on Muot da Barba Peider (Swiss Alps). Microb. Genom. 7(4), 000558 (13 pp.). https://doi.org/10.1099/mgen.0.000558Institutional Repository DORA

Adamczyk M., Rüthi J., Frey B. (2021) Root exudates increase soil respiration and alter microbial community structure in alpine permafrost and active layer soils. Environ. Microbiol. 23(4), 2152-2168. https://doi.org/10.1111/1462-2920.15383 Institutional Repository DORA

Frey B. (2021) Microbial ecology of mountain permafrost: the Alps. In S. Liebner & L. Ganzert (Eds.), Life in extreme environments: Vol. 7. Microbial life in the cryosphere and Its feedback on global change. Berlin: de Gruyter. 153-172. https://doi.org/10.1515/9783110497083-007 Institutional Repository DORA

Frossard A., De Maeyer L., Adamczyk M., Svenning M., Verleyen E., Frey B. (2021) Microbial carbon use and associated changes in microbial community structure in high-Arctic tundra soils under elevated temperature. Soil Biol. Biochem. 162, 108419 (11 pp.). https://doi.org/10.1016/j.soilbio.2021.108419Institutional Repository DORA

Adamczyk M., Perez-Mon C., Gunz S., Frey B. (2020) Strong shifts in microbial community structure are associated with increased litter input rather than temperature in High Arctic soils. Soil Biol. Biochem. 151, 108054 (14 pp.). https://doi.org/10.1016/j.soilbio.2020.108054Institutional Repository DORA

Donhauser J., Niklaus P.A., Rousk J., Larose C., Frey B. (2020) Temperatures beyond the community optimum promote the dominance of heat-adapted, fast growing and stress resistant bacteria in alpine soils. Soil Biol. Biochem. 148, 107873 (16 pp.). https://doi.org/10.1016/j.soilbio.2020.107873Institutional Repository DORA

Rüthi J., Bölsterli D., Pardi-Comensoli L., Brunner I., Frey B. (2020) The "plastisphere" of biodegradable plastics is characterized by specific microbial taxa of Alpine and Arctic soils. Front. Environ. Sci. 8, 562263 (23 pp.). https://doi.org/10.3389/fenvs.2020.562263Institutional Repository DORA

Perez-Mon C., Frey B., Frossard A. (2020) Functional and structural responses of Arctic and alpine soil prokaryotic and fungal communities under freeze-thaw cycles of different frequencies. Front. Microbiol. 11, 982 (14 pp.). https://doi.org/10.3389/fmicb.2020.00982Institutional Repository DORA

Pontes A., Ruethi J., Frey B., Aires A., Thomas A., Overy D., … Sampaio J.P. (2020) Cryolevonia gen. nov. and Cryolevonia schafbergensis sp. nov., a cryophilic yeast from ancient permafrost and melted sea ice. Int. J. Syst. Evol. Microbiol. 70(4), 2334-2338. https://doi.org/10.1099/ijsem.0.004040 Institutional Repository DORA

Wojcik R., Donhauser J., Frey B., Benning L.G. (2020) Time since deglaciation and geomorphological disturbances determine the patterns of geochemical, mineralogical and microbial successions in an Icelandic foreland. Geoderma. 379, 114578 (14 pp.). https://doi.org/10.1016/j.geoderma.2020.114578Institutional Repository DORA

Pushkareva E., Eckhardt K.U., Hotter V., Frossard A., Leinweber P., Frey B., Karsten U. (2020) Chemical composition of soil organic matter and potential enzyme activity in the topsoil along a moisture gradient in the High Arctic (Svalbard). Geoderma. 368, 114304 (9 pp.). https://doi.org/10.1016/j.geoderma.2020.114304Institutional Repository DORA

Luláková P., Perez-Mon C., Šantrůčková H., Ruethi J., Frey B. (2019) High-alpine permafrost and active-layer soil microbiomes differ in their response to elevated temperatures. Front. Microbiol. 10, 668 (16 pp.). https://doi.org/10.3389/fmicb.2019.00668Institutional Repository DORA

Adamczyk M., Hagedorn F., Wipf S., Donhauser J., Vittoz P., Rixen C., … Frey B. (2019) The soil microbiome of GLORIA mountain summits in the Swiss Alps. Front. Microbiol. 10, 1080 (21 pp.). https://doi.org/10.3389/fmicb.2019.01080Institutional Repository DORA

Kern R., Hotter V., Frossard A., Albrecht M., Baum C., Tytgat B., … Karsten U. (2019) Comparative vegetation survey with focus on cryptogamic covers in the high Arctic along two differing catenas. Polar Biol. 42(11), 2131-2145. https://doi.org/10.1007/s00300-019-02588-z Institutional Repository DORA

Mondini A., Donhauser J., Itcus C., Marin C., Perșoiu A., Lavin P., … Purcarea C. (2018) High-throughput sequencing of fungal communities across the perennial ice block of Scărișoara Ice Cave. Ann. Glaciol. 59(77), 134-146. https://doi.org/10.1017/aog.2019.6 Institutional Repository DORA

Donhauser J., Frey B. (2018) Alpine soil microbial ecology in a changing world. FEMS Microbiol. Ecol. 94(9), 099 (34 pp.). https://doi.org/10.1093/femsec/fiy099Institutional Repository DORA

Wojcik R., Donhauser J., Frey B., Holm S., Holland A., Anesio A.M., … Benning L.G. (2018) Linkages between geochemistry and microbiology in a proglacial terrain in the High Arctic. Ann. Glaciol. 59(77), 95-110. https://doi.org/10.1017/aog.2019.1 Institutional Repository DORA

Frey B., Rime T., Phillips M., Stierli B., Hajdas I., Widmer F., Hartmann M. (2016) Microbial diversity in European alpine permafrost and active layers. FEMS Microbiol. Ecol. 92(3), 018 (17 pp.). https://doi.org/10.1093/femsec/fiw018Institutional Repository DORA

Rime T., Hartmann M., Frey B. (2016) Potential sources of microbial colonizers in an initial soil ecosystem after retreat of an alpine glacier. ISME J. 10(7), 1625-1641. https://doi.org/10.1038/ismej.2015.238 Institutional Repository DORA

Rime T., Hartmann M., Stierli B., Anesio A.M., Frey B. (2016) Assimilation of microbial and plant carbon by active prokaryotic and fungal populations in glacial forefields. Soil Biol. Biochem. 98, 30-41. https://doi.org/10.1016/j.soilbio.2016.03.012 Institutional Repository DORA

Frasson D., Udovicic M., Frey B., Lapanje A., Zhang D.C., Margesin R., Sievers M. (2015) Glaciimonas alpina sp. nov. isolated from alpine glaciers and reclassification of Glaciimonas immobilis Cr9-12 as the type strain of Glaciimonas alpina sp. nov. Int. J. Syst. Evol. Microbiol. 65(6), 1779-1785. https://doi.org/10.1099/ijs.0.000174 Institutional Repository DORA

Rime T., Hartmann M., Brunner I., Widmer F., Zeyer J., Frey B. (2015) Vertical distribution of the soil microbiota along a successional gradient in a glacier forefield. Mol. Ecol. 24(5), 1091-1108. https://doi.org/10.1111/mec.13051 Institutional Repository DORA

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