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Active lithoautotrophic and methane-oxidizing microbial community in an anoxic, sub-zero, and hypersaline High Arctic spring

Abstract

Lost Hammer Spring, located in the High Arctic of Nunavut, Canada, is one of the coldest and saltiest terrestrial springs discovered to date. It perennially discharges anoxic (<1 ppm dissolved oxygen), sub-zero (~−5 °C), and hypersaline (~24% salinity) brines from the subsurface through up to 600 m of permafrost. The sediment is sulfate-rich (1 M) and continually emits gases composed primarily of methane (~50%), making Lost Hammer the coldest known terrestrial methane seep and an analog to extraterrestrial habits on Mars, Europa, and Enceladus. A multi-omics approach utilizing metagenome, metatranscriptome, and single-amplified genome sequencing revealed a rare surface terrestrial habitat supporting a predominantly lithoautotrophic active microbial community driven in part by sulfide-oxidizing Gammaproteobacteria scavenging trace oxygen. Genomes from active anaerobic methane-oxidizing archaea (ANME-1) showed evidence of putative metabolic flexibility and hypersaline and cold adaptations. Evidence of anaerobic heterotrophic and fermentative lifestyles were found in candidate phyla DPANN archaea and CG03 bacteria genomes. Our results demonstrate Mars-relevant metabolisms including sulfide oxidation, sulfate reduction, anaerobic oxidation of methane, and oxidation of trace gases (H2, CO2) detected under anoxic, hypersaline, and sub-zero ambient conditions, providing evidence that similar extant microbial life could potentially survive in similar habitats on Mars.

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Fig. 1: Taxonomic diversity and novelty in MAGs and SAGs.
Fig. 2: Key metabolic genes expressed in the LH spring sediment.
Fig. 3: Metabolic potential and gene expression in high-quality MAGs and medium-quality SAGs.
Fig. 4: Percent relative expression by phylum, including both genes in MAGs and SAGs and unbinned genes classified by JGI.
Fig. 5: Metabolic reconstruction of ANME-1 SAGs.
Fig. 6: Model for a hypothetical Martian methane cycle, adapted and reproduced with permission from Harris et al. [92].

Data availability

Sequencing reads, metagenome, MAGs, and SAGs are in NCBI under BioProject PRJNA699472. JGI metagenome and SAG annotations are available under GOLD Study ID Gs0135943 (SAG IDs in Table S4).

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Acknowledgements

We thank the Bigelow Single Cell Genomics Center for cell sorting services and support. EM was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) doctoral award (funding reference number CGSD2-534189-2019), Fonds de recherche du Québec—Nature et technologies (FRQNT) doctoral award (funding reference number 272792), and the Northern Scientific Training Program. This research was also supported by the Canada Research Chair Program, the NSERC Discovery and Northern Research Supplement Programs, and the Polar Continental Shelf Project (Arctic logistical support). Field work was carried out with appropriate licensing obtained from the territory of Nunavut and the Nunavut Research Institute (Nunavut Scientific Research License Nos. 02 043 17R-M and 02 051 19N-M).

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Contributions

LGW conceived and supervised the study. EM, IA, and LGW designed the experiments. EM, IA, and CM conducted field work. EM and IA conducted laboratory experiments and sequencing. EM, IA, MAF, YJC, JG, and LGW analyzed and interpreted the data. EM and IA prepared figures. EM, MAF, and LGW wrote the paper. All authors reviewed and edited the paper.

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Correspondence to Lyle G. Whyte.

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Magnuson, E., Altshuler, I., Fernández-Martínez, M.Á. et al. Active lithoautotrophic and methane-oxidizing microbial community in an anoxic, sub-zero, and hypersaline High Arctic spring. ISME J 16, 1798–1808 (2022). https://doi.org/10.1038/s41396-022-01233-8

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  • DOI: https://doi.org/10.1038/s41396-022-01233-8

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