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

The ISME Journal volume 16, pages 1798–1808 (2022)Cite this article

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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).

References

  1. Pollard W, Omelon C, Andersen D, McKay C. Perennial spring occurrence in the Expedition Fiord area of western Axel Heiberg Island, Canadian High Arctic. Can J Earth Sci. 1999;36:105–20.

    CAS  Article  Google Scholar 

  2. Andersen DT. Cold springs in permafrost on Earth and Mars. J Geophys Res. 2002;107:4–1-4-7.

    Article  Google Scholar 

  3. Niederberger TD, Perreault NN, Tille S, Lollar BS, Lacrampe-Couloume G, Andersen D, et al. Microbial characterization of a subzero, hypersaline methane seep in the Canadian High Arctic. ISME J. 2010;4:1326–39.

    CAS  PubMed  Article  Google Scholar 

  4. Goordial J, Lamarche-Gagnon G, Lay CY, Whyte L. Left out in the cold: life in cryoenvironments. In: Seckbach J, Oren A, Stan-Lotter H, editors. Polyextremophiles. New York: Springer; 2013. p. 335–64.

  5. Gilichinsky D, Rivkina E, Bakermans C, Shcherbakova V, Petrovskaya L, Ozerskaya S, et al. Biodiversity of cryopegs in permafrost. FEMS Microbiol Ecol. 2005;53:117–28.

    CAS  PubMed  Article  Google Scholar 

  6. Rivkina EM, Friedmann EI, McKay CP, Gilichinsky DA. Metabolic activity of permafrost bacteria below the freezing point. Appl Environ Microbiol. 2000;66:3230–3.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. Brown MV, Bowman JP. A molecular phylogenetic survey of sea-ice microbial communities (SIMCO). FEMS Microbiol Ecol. 2001;35:267–75.

    CAS  PubMed  Article  Google Scholar 

  8. Murray AE, Kenig F, Fritsen CH, McKay CP, Cawley KM, Edwards R, et al. Microbial life at -13 degrees C in the brine of an ice-sealed Antarctic lake. Proc Natl Acad Sci USA. 2012;109:20626–31.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Orosei R, Lauro SE, Pettinelli E, Cicchetti A, Coradini M, Cosciotti B, et al. Radar evidence of subglacial liquid water on Mars. Science. 2018;361:490–3.

    CAS  PubMed  Article  Google Scholar 

  10. Lauro SE, Pettinelli E, Caprarelli G, Guallini L, Pio Rossi A, Mattei E, et al. Multiple subglacial water bodies below the south pole of Mars unveiled by new MARSIS data. Nat Astron. 2021;5:63–70.

    Article  Google Scholar 

  11. Bishop JL, Yesilbas M, Hinman NW, Burton ZFM, Englert PAJ, Toner JD, et al. Martian subsurface cryosalt expansion and collapse as trigger for landslides. Sci Adv. 2021;7:1–13.

    Google Scholar 

  12. Allen CC, Oehler DZ. A case for ancient springs in Arabia Terra, Mars. Astrobiology. 2008;8:1093–112.

    CAS  PubMed  Article  Google Scholar 

  13. Battler MM, Osinski GR, Banerjee NR. Mineralogy of saline perennial cold springs on Axel Heiberg Island, Nunavut, Canada and implications for spring deposits on Mars. Icarus. 2013;224:364–81.

    CAS  Article  Google Scholar 

  14. Leask EK, Ehlmann BL. Evidence for deposition of chloride on Mars from small‐volume surface water events into the Late Hesperian‐Early Amazonian. AGU Adv. 2022;3:1–19.

    Article  Google Scholar 

  15. Howell SM, Pappalardo RT. NASA’s Europa Clipper-a mission to a potentially habitable ocean world. Nat Commun. 2020;11:1–4.

    Article  CAS  Google Scholar 

  16. Farley KA, Williford KH, Stack KM, Bhartia R, Chen A, de la Torre M, et al. Mars 2020 mission overview. Space Sci Rev. 2020;216:1–41.

    Article  Google Scholar 

  17. Kargel JS, Kaye JZ, Head JW, Marion GM, Sassen R, Crowley JK, et al. Europa’s crust and ocean: origin, composition, and the prospects for life. Icarus. 2000;148:226–65.

    CAS  Article  Google Scholar 

  18. Taubner RS, Pappenreiter P, Zwicker J, Smrzka D, Pruckner C, Kolar P, et al. Biological methane production under putative Enceladus-like conditions. Nat Commun. 2018;9:1–11.

    CAS  Article  Google Scholar 

  19. Lamarche-Gagnon G, Comery R, Greer CW, Whyte LG. Evidence of in situ microbial activity and sulphidogenesis in perennially sub-0 degrees C and hypersaline sediments of a high Arctic permafrost spring. Extremophiles. 2015;19:1–15.

    CAS  PubMed  Article  Google Scholar 

  20. Lay CY, Mykytczuk NC, Yergeau E, Lamarche-Gagnon G, Greer CW, Whyte LG. Defining the functional potential and active community members of a sediment microbial community in a high-arctic hypersaline subzero spring. Appl Environ Microbiol. 2013;79:3637–48.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. Menzel P, Ng KL, Krogh A. Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun. 2016;7:1–9.

    Article  CAS  Google Scholar 

  23. Gruber-Vodicka HR, Seah BKB, Pruesse E. phyloFlash: rapid small-subunit rRNA profiling and targeted assembly from metagenomes. mSystems. 2020;5:1–16.

    Article  Google Scholar 

  24. Li D, Liu CM, Luo R, Sadakane K, Lam TW. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31:1674–6.

    CAS  PubMed  Article  Google Scholar 

  25. Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:1–15.

    Article  CAS  Google Scholar 

  26. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. Chen IA, Chu K, Palaniappan K, Ratner A, Huang J, Huntemann M, et al. The IMG/M data management and analysis system v.6.0: new tools and advanced capabilities. Nucleic Acids Res. 2020;49:D751–D63.

    PubMed Central  Article  CAS  Google Scholar 

  28. Mukherjee S, Stamatis D, Bertsch J, Ovchinnikova G, Sundaramurthi JC, Lee J, et al. Genomes OnLine Database (GOLD) v.8: overview and updates. Nucleic Acids Res. 2020;49:D723–D733.

    PubMed Central  Article  CAS  Google Scholar 

  29. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics. 2019;36:1925–7.

    PubMed Central  Google Scholar 

  30. Schmieder R, Edwards R. Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS ONE. 2011;6:1–11.

    Article  CAS  Google Scholar 

  31. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. Kopylova E, Noe L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–7.

    CAS  PubMed  Article  Google Scholar 

  33. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31:166–9.

    CAS  PubMed  Article  Google Scholar 

  35. Royo-Llonch M, Sanchez P, Ruiz-Gonzalez C, Salazar G, Pedros-Alio C, Sebastian M, et al. Compendium of 530 metagenome-assembled bacterial and archaeal genomes from the polar Arctic Ocean. Nat Microbiol. 2021;6:1561–74.

    CAS  PubMed  Article  Google Scholar 

  36. Ghosh W, Dam B. Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol Rev. 2009;33:999–1043.

    CAS  PubMed  Article  Google Scholar 

  37. Boden R. Reclassification of Halothiobacillus hydrothermalis and Halothiobacillus halophilus to Guyparkeria gen. nov. in the Thioalkalibacteraceae fam. nov., with emended descriptions of the genus Halothiobacillus and family Halothiobacillaceae. Int J Syst Evol Microbiol. 2017;67:3919–28.

    CAS  PubMed  Article  Google Scholar 

  38. Sorokin DY, Abbas B, van Zessen E, Muyzer G. Isolation and characterization of an obligately chemolithoautotrophic Halothiobacillus strain capable of growth on thiocyanate as an energy source. FEMS Microbiol Lett. 2014;354:69–74.

    CAS  PubMed  Article  Google Scholar 

  39. Meier DV, Pjevac P, Bach W, Hourdez S, Girguis PR, Vidoudez C, et al. Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents. ISME J. 2017;11:1545–58.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. Headd B, Engel AS. Evidence for niche partitioning revealed by the distribution of sulfur oxidation genes collected from areas of a terrestrial sulfidic spring with differing geochemical conditions. Appl Environ Microbiol. 2013;79:1171–82.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. Preisig O, Zufferey R, Thoney-Meyer L, Appleby CA, Hennecke H. A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol. 1996;178:1532–8.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. Mikucki JA, Pearson A, Johnston DT, Turchyn AV, Farquhar J, Schrag DP, et al. A contemporary microbially maintained subglacial ferrous “ocean”. Science. 2009;324:397–400.

    CAS  PubMed  Article  Google Scholar 

  43. Ruff SE, Biddle JF, Teske AP, Knittel K, Boetius A, Ramette A. Global dispersion and local diversification of the methane seep microbiome. Proc Natl Acad Sci USA. 2015;112:4015–20.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. Lloyd KG, Lapham L, Teske A. An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments. Appl Environ Microbiol. 2006;72:7218–30.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  45. Maignien L, Parkes RJ, Cragg B, Niemann H, Knittel K, Coulon S, et al. Anaerobic oxidation of methane in hypersaline cold seep sediments. FEMS Microbiol Ecol. 2013;83:214–31.

    CAS  PubMed  Article  Google Scholar 

  46. Campen R, Kowalski J, Lyons WB, Tulaczyk S, Dachwald B, Pettit E, et al. Microbial diversity of an Antarctic subglacial community and high-resolution replicate sampling inform hydrological connectivity in a polar desert. Environ Microbiol. 2019;21:2290–306.

    PubMed  Article  Google Scholar 

  47. Cooper ZS, Rapp JZ, Carpenter SD, Iwahana G, Eicken H, Deming JW. Distinctive microbial communities in subzero hypersaline brines from Arctic coastal sea ice and rarely sampled cryopegs. FEMS Microbiol Ecol. 2019;95:1–15.

    Article  CAS  Google Scholar 

  48. Winkel M, Mitzscherling J, Overduin PP, Horn F, Winterfeld M, Rijkers R, et al. Anaerobic methanotrophic communities thrive in deep submarine permafrost. Sci Rep. 2018;8:1–13.

    CAS  Google Scholar 

  49. Lay CY, Mykytczuk NC, Niederberger TD, Martineau C, Greer CW, Whyte LG. Microbial diversity and activity in hypersaline high Arctic spring channels. Extremophiles. 2012;16:177–91.

    CAS  PubMed  Article  Google Scholar 

  50. Bhattarai S, Cassarini C, Lens PNL. Physiology and distribution of archaeal methanotrophs that couple anaerobic oxidation of methane with sulfate reduction. Microbiol Mol Biol Rev. 2019;83:1–31.

    Article  Google Scholar 

  51. Kleindienst S, Ramette A, Amann R, Knittel K. Distribution and in situ abundance of sulfate-reducing bacteria in diverse marine hydrocarbon seep sediments. Environ Microbiol. 2012;14:2689–710.

    CAS  PubMed  Article  Google Scholar 

  52. Timmers PH, Welte CU, Koehorst JJ, Plugge CM, Jetten MS, Stams AJ. Reverse methanogenesis and respiration in methanotrophic archaea. Archaea. 2017;2017:1–22.

    Article  CAS  Google Scholar 

  53. Leu AO, Cai C, McIlroy SJ, Southam G, Orphan VJ, Yuan Z, et al. Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae. ISME J. 2020;14:1030–41.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, et al. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature. 2013;500:567–70.

    CAS  PubMed  Article  Google Scholar 

  55. Cai C, Leu AO, Xie GJ, Guo J, Feng Y, Zhao JX, et al. A methanotrophic archaeon couples anaerobic oxidation of methane to Fe(III) reduction. ISME J. 2018;12:1929–39.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. Oshkin IY, Wegner CE, Luke C, Glagolev MV, Filippov IV, Pimenov NV, et al. Gammaproteobacterial methanotrophs dominate cold methane seeps in floodplains of West Siberian rivers. Appl Environ Microbiol. 2014;80:5944–54.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  57. Cabrol L, Thalasso F, Gandois L, Sepulveda-Jauregui A, Martinez-Cruz K, Teisserenc R, et al. Anaerobic oxidation of methane and associated microbiome in anoxic water of Northwestern Siberian lakes. Sci Total Environ. 2020;736:1–16.

    Article  CAS  Google Scholar 

  58. Orcutt B, Boetius A, Elvert M, Samarkin V, Joye SB. Molecular biogeochemistry of sulfate reduction, methanogenesis and the anaerobic oxidation of methane at Gulf of Mexico cold seeps. Geochim Cosmochim Acta. 2005;69:4267–81.

    CAS  Article  Google Scholar 

  59. Knittel K, Losekann T, Boetius A, Kort R, Amann R. Diversity and distribution of methanotrophic archaea at cold seeps. Appl Environ Microbiol. 2005;71:467–79.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Schubert CJ, Coolen MJ, Neretin LN, Schippers A, Abbas B, Durisch-Kaiser E, et al. Aerobic and anaerobic methanotrophs in the Black Sea water column. Environ Microbiol. 2006;8:1844–56.

    CAS  PubMed  Article  Google Scholar 

  61. Wang J, Hua M, Cai C, Hu J, Wang J, Yang H, et al. Spatial-temporal pattern of sulfate-dependent anaerobic methane oxidation in an intertidal zone of the East China Sea. Appl Environ Microbiol. 2019;85:1–15.

    Google Scholar 

  62. Dyksma S, Bischof K, Fuchs BM, Hoffmann K, Meier D, Meyerdierks A, et al. Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments. ISME J. 2016;10:1939–53.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. Perreault NN, Greer CW, Andersen DT, Tille S, Lacrampe-Couloume G, Lollar BS, et al. Heterotrophic and autotrophic microbial populations in cold perennial springs of the high Arctic. Appl Environ Microbiol. 2008;74:6898–907.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. Cordero PRF, Bayly K, Man Leung P, Huang C, Islam ZF, Schittenhelm RB, et al. Atmospheric carbon monoxide oxidation is a widespread mechanism supporting microbial survival. ISME J. 2019;13:2868–81.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. Nigro LM, Elling FJ, Hinrichs KU, Joye SB, Teske A. Microbial ecology and biogeochemistry of hypersaline sediments in Orca Basin. PLoS ONE. 2020;15:1–25.

    Article  CAS  Google Scholar 

  66. Rath KM, Fierer N, Murphy DV, Rousk J. Linking bacterial community composition to soil salinity along environmental gradients. ISME J. 2019;13:836–46.

    CAS  PubMed  Article  Google Scholar 

  67. Yoon JH, Lee MH, Kang SJ, Oh TK. Salegentibacter salinarum sp. nov., isolated from a marine solar saltern. Int J Syst Evol Microbiol. 2008;58:365–9.

    CAS  PubMed  Article  Google Scholar 

  68. Sangwan N, Xia F, Gilbert JA. Recovering complete and draft population genomes from metagenome datasets. Microbiome. 2016;4:1–11.

    Article  Google Scholar 

  69. Goordial J, Raymond-Bouchard I, Zolotarov Y, de Bethencourt L, Ronholm J, Shapiro N, et al. Cold adaptive traits revealed by comparative genomic analysis of the eurypsychrophile Rhodococcus sp. JG3 isolated from high elevation McMurdo Dry Valley permafrost, Antarctica. FEMS Microbiol Ecol. 2016;92:1–11.

    Google Scholar 

  70. Laso-Perez R, Wegener G, Knittel K, Widdel F, Harding KJ, Krukenberg V, et al. Thermophilic archaea activate butane via alkyl-coenzyme M formation. Nature. 2016;539:396–401.

    CAS  PubMed  Article  Google Scholar 

  71. Dombrowski N, Teske AP, Baker BJ. Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments. Nat Commun. 2018;9:1–13.

    CAS  Article  Google Scholar 

  72. Oren A. Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol. 2011;13:1908–23.

    CAS  PubMed  Article  Google Scholar 

  73. Gunde-Cimerman N, Plemenitas A, Oren A. Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations. FEMS Microbiol Rev. 2018;42:353–75.

    CAS  PubMed  Article  Google Scholar 

  74. Hechler T, Pfeifer F. Anaerobiosis inhibits gas vesicle formation in halophilic. Archaea Mol Microbiol. 2009;71:132–45.

    CAS  PubMed  Article  Google Scholar 

  75. Stokke R, Roalkvam I, Lanzen A, Haflidason H, Steen IH. Integrated metagenomic and metaproteomic analyses of an ANME-1-dominated community in marine cold seep sediments. Environ Microbiol. 2012;14:1333–46.

    CAS  PubMed  Article  Google Scholar 

  76. Wegener G, Krukenberg V, Riedel D, Tegetmeyer HE, Boetius A. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature. 2015;526:587–90.

    CAS  PubMed  Article  Google Scholar 

  77. Skennerton CT, Chourey K, Iyer R, Hettich RL, Tyson GW, Orphan VJ. Methane-fueled syntrophy through extracellular electron transfer: uncovering the genomic traits conserved within diverse bacterial partners of anaerobic methanotrophic archaea. mBio. 2017;8:1–14.

    Article  Google Scholar 

  78. Krukenberg V, Riedel D, Gruber-Vodicka HR, Buttigieg PL, Tegetmeyer HE, Boetius A, et al. Gene expression and ultrastructure of meso- and thermophilic methanotrophic consortia. Environ Microbiol. 2018;20:1651–66.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. Youssef NH, Rinke C, Stepanauskas R, Farag I, Woyke T, Elshahed MS. Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’. ISME J. 2015;9:447–60.

    CAS  PubMed  Article  Google Scholar 

  80. Castelle CJ, Brown CT, Anantharaman K, Probst AJ, Huang RH, Banfield JF. Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations. Nat Rev Microbiol. 2018;16:629–45.

    CAS  PubMed  Article  Google Scholar 

  81. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature. 2013;499:431–7.

    CAS  PubMed  Article  Google Scholar 

  82. Dombrowski N, Lee JH, Williams TA, Offre P, Spang A. Genomic diversity, lifestyles and evolutionary origins of DPANN archaea. FEMS Microbiol Lett. 2019;366:1–12.

    Article  CAS  Google Scholar 

  83. Wong HL, MacLeod FI, White RA 3rd, Visscher PT, Burns BP. Microbial dark matter filling the niche in hypersaline microbial mats. Microbiome. 2020;8:1–14.

    Article  CAS  Google Scholar 

  84. Schut GJ, Nixon WJ, Lipscomb GL, Scott RA, Adams MW. Mutational analyses of the enzymes involved in the metabolism of hydrogen by the hyperthermophilic archaeon Pyrococcus furiosus. Front Microbiol. 2012;3:1–6.

    Article  Google Scholar 

  85. Ruuskanen MO, Colby G, St. Pierre KA, St. Louis VL, Aris‐Brosou S, Poulain AJ. Microbial genomes retrieved from High Arctic lake sediments encode for adaptation to cold and oligotrophic environments. Limnol Oceanogr. 2020;65:S233–S247.

    CAS  Article  Google Scholar 

  86. Vigneron A, Cruaud P, Lovejoy C, Vincent WF. Genomic evidence of functional diversity in DPANN archaea, from oxic species to anoxic vampiristic consortia. ISME Commun. 2022;2:1–10.

    Article  Google Scholar 

  87. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil PA, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004.

    CAS  PubMed  Article  Google Scholar 

  88. Meheust R, Castelle CJ, Matheus Carnevali PB, Farag IF, He C, Chen LX, et al. Groundwater Elusimicrobia are metabolically diverse compared to gut microbiome Elusimicrobia and some have a novel nitrogenase paralog. ISME J. 2020;14:2907–22.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  89. Hahn CR, Farag IF, Murphy CL, Podar M, Elshahed MS, Youssef NH. Microbial diversity and sulfur cycling in an early earth analogue: from ancient novelty to modern commonality. mBio. https://doi.org/10.1128/mbio.00016-22. (in press).

  90. Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y. The I-TASSER Suite: protein structure and function prediction. Nat Methods. 2015;12:7–8.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  91. Rummel JD, Beaty DW, Jones MA, Bakermans C, Barlow NG, Boston PJ, et al. A new analysis of Mars "Special Regions": findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology. 2014;14:887–968.

    PubMed  Article  Google Scholar 

  92. Harris RL, Schuerger AC, Wang W, Tamama Y, Garvin ZK, Onstott TC. Transcriptional response to prolonged perchlorate exposure in the methanogen Methanosarcina barkeri and implications for Martian habitability. Sci Rep. 2021;11:1–16.

    Article  CAS  Google Scholar 

  93. Webster CR, Mahaffy PR, Atreya SK, Moores JE, Flesch GJ, Malespin C, et al. Background levels of methane in Mars’ atmosphere show strong seasonal variations. Science. 2018;360:1093–6.

    CAS  PubMed  Article  Google Scholar 

  94. Oehler DZ, Etiope G. Methane seepage on Mars: where to look and why. Astrobiology. 2017;17:1233–64.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. Marlow JJ, Larowe DE, Ehlmann BL, Amend JP, Orphan VJ. The potential for biologically catalyzed anaerobic methane oxidation on ancient Mars. Astrobiology. 2014;14:292–307.

    CAS  PubMed  Article  Google Scholar 

  96. Ji M, Greening C, Vanwonterghem I, Carere CR, Bay SK, Steen JA, et al. Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature. 2017;552:400–3.

    CAS  PubMed  Article  Google Scholar 

  97. Berg JS, Ahmerkamp S, Pjevac P, Hausmann B, Milucka J, Kuypers MMM. How low can they go? Aerobic respiration by microorganisms under apparent anoxia. FEMS Microbiol Rev. 2022;fuac006. https://doi.org/10.1093/femsre/fuac006.

  98. Berg JS, Pjevac P, Sommer T, Buckner CRT, Philippi M, Hach PF, et al. Dark aerobic sulfide oxidation by anoxygenic phototrophs in anoxic waters. Environ Microbiol. 2019;21:1611–26.

    CAS  PubMed  Article  Google Scholar 

  99. Stamenković V, Ward LM, Mischna M, Fischer WW. O2 solubility in Martian near-surface environments and implications for aerobic life. Nat Geosci. 2018;11:905–9.

    Article  CAS  Google Scholar 

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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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Authors and Affiliations

  1. Natural Resource Sciences, McGill University, Ste-Anne-de-Bellevue, QC, Canada

    Elisse Magnuson, Miguel Á. Fernández-Martínez, Ya-Jou Chen, Catherine Maggiori & Lyle G. Whyte

  2. School of Architecture, Civil and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland

    Ianina Altshuler

  3. School of Environmental Sciences, University of Guelph, Guelph, ON, Canada

    Jacqueline Goordial

Authors
  1. Elisse Magnuson
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  2. Ianina Altshuler
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  3. Miguel Á. Fernández-Martínez
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  4. Ya-Jou Chen
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  5. Catherine Maggiori
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  6. Jacqueline Goordial
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  7. Lyle G. Whyte
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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.

Corresponding author

Correspondence to Lyle G. Whyte.

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The authors declare no competing interests.

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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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