Comparative genomics of the extremophile Cryomyces antarcticus and other psychrophilic Dothideomycetes

Authors: GOMEZ, SANDRA - Purdue University; SIC, WILY - Purdue University; HARIDAS, SAJEET - Department Of Energy Joint Genome; LABUTTI, KURT - Department Of Energy Joint Genome; EICHENBURGER, JOANNE - Department Of Energy Joint Genome; KAUR, NAVNEET - Department Of Energy Joint Genome; LIPZEN, ANNA - Department Of Energy Joint Genome; BARRY, KERRIE - Department Of Energy Joint Genome; Goodwin, Stephen - Steve; GRIBSKOV, MICHAEL - Purdue University; GRIGORIEV, IGOR - Department Of Energy Joint Genome

Submitted to: Frontiers in Fungal Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/12/2024
Publication Date: 9/6/2024
Citation: Gomez-Gutierrez, S.V., Sic-Hernandez, W., Haridas, S., Labutti, K., Eichenburger, J., Kaur, N., Lipzen, A., Barry, K., Goodwin, S.B., Gribskov, M., Grigoriev, I.V. 2024. Comparative genomics of the extremophile Cryomyces antarcticus and other psychrophilic Dothideomycetes. Frontiers in Fungal Biology. https://doi.org/10.3389/ffunb.2024.1418145.
DOI: https://doi.org/10.3389/ffunb.2024.1418145

Interpretive Summary: Cryomyces antarcticus is a fungus that inhabits rock outcrops in Antarctica, where it is exposed to extremes of cold, humidity and solar radiation in one of the least habitable environments on Earth; due to its growth in the most extreme environments it has been suggested as an organism that could survive on Mars. However, the mechanisms it uses to survive such environments are not known. To identify modifications that might help this fungus survive extreme environments, its genome sequence was compared to those of 51 other fungi from a range of extremes plus moderate environments for comparison. The analysis identified families of genes that were expanded or contracted in cold-loving fungi compared to the others and could help to explain their evolutionary adaptations. Genes in cold-loving fungi had a higher frequency of bases that could stabilize DNA, which might help explain their ability to survive extreme conditions. The C. antarcticus genome also had characteristics that could indicate it has a sexual cycle, which had not been known previously. These results will be of interest to fungal biologists and ecologists trying to understand adaptations of organisms to extreme environments and to space biologists who will want to learn what might be required for life to survive on Mars.

Technical Abstract: Cryomyces antarcticus is an endolithic fungus that inhabits rock outcrops in Antarctica. It survives extremes of cold, humidity and solar radiation in one of the least habitable environments on Earth. This fungus is unusual because it produces heavily melanized, meristematic growth and is thought to be haploid and asexual. Due to its growth in the most extreme environment it has been suggested as an organism that could survive on Mars. However, the mechanisms it uses to achieve its extremophilic nature are not known. Over a billion years of fungal evolution has enabled representatives of this kingdom to populate almost all parts of planet Earth and to adapt to some of its most uninhabitable environments including extremes of temperature, salinity, pH, water, light, or other sources of radiation. Comparative genomics can provide clues to the processes underlying biological diversity, evolution, and adaptation. This effort has been greatly facilitated by the 1000 Fungal Genomes project and the JGI MycoCosm portal where sequenced genomes have been assembled into phylogenetic and ecological groups representing different projects, lifestyles, ecologies, and evolutionary histories. Comparative genomics within and between these groups provides insights into fungal adaptations, for example to extreme environmental conditions. Here, we analyze two Cryomycetes genomes in the context of additional psychrophilic fungi, as well as non-psychrophilic fungi with diverse lifestyles selected from the MycoCosm database. This analysis identifies families of genes that are expanded and contracted in Cryomyces and other psychrophiles, and may explain their extremophilic lifestyle. Higher GC contents of genes and of bases in the third positions of codons may help to stabilize DNA under extreme conditions. Numerous smaller scaffolds in C. antarcticus suggest the presence of an alternative haplotype that could indicate that the sequenced isolate is diploid or dikaryotic. These analyses provide a first step to unraveling the secrets of the extreme lifestyle of C. antarcticus.