Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Anaerobic carboxydotrophy in sulfur-respiring haloarchaea from hypersaline lakes

The ISME Journal volume 16, pages 1534–1546 (2022)Cite this article

Subjects

Abstract

Anaerobic carboxydotrophy is a widespread catabolic trait in bacteria, with two dominant pathways: hydrogenogenic and acetogenic. The marginal mode by direct oxidation to CO2 using an external e-acceptor has only a few examples. Use of sulfidic sediments from two types of hypersaline lakes in anaerobic enrichments with CO as an e-donor and elemental sulfur as an e-acceptor led to isolation of two pure cultures of anaerobic carboxydotrophs belonging to two genera of sulfur-reducing haloarchaea: Halanaeroarchaeum sp. HSR-CO from salt lakes and Halalkaliarchaeum sp. AArc-CO from soda lakes. Anaerobic growth of extremely halophilic archaea with CO was obligatory depended on the presence of elemental sulfur as the electron acceptor and yeast extract as the carbon source. CO served as a direct electron donor and H2 was not generated from CO when cells were incubated with or without sulfur. The genomes of the isolates encode a catalytic Ni,Fe-CODH subunit CooS (distantly related to bacterial homologs) and its Ni-incorporating chaperone CooC (related to methanogenic homologs) within a single genomic locus. Similar loci were also present in a genome of the type species of Halalkaliarchaeum closely related to AArc-CO, and the ability for anaerobic sulfur-dependent carboxydotrophy was confirmed for three different strains of this genus. Moreover, similar proteins are encoded in three of the four genomes of recently described carbohydrate-utilizing sulfur-reducing haloarchaea belonging to the genus Halapricum and in two yet undescribed haloarchaeal species. Overall, this work demonstrated for the first time the potential for anaerobic sulfur-dependent carboxydotrophy in extremely halophilic archaea.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Phylogenomic placement of carboxydotrophic sulfur-reducing isolates AArc-CO and HSR-CO among their nearest relatives based on maximum likelihood inference and concatenated partial amino acid sequences of 122 archaeal single copy conserved marker proteins.
Fig. 2: Anaerobic growth kinetics of carboxydotrophic sulfur-reducing haloarchaea grown at 4.0 M total Na+/pH 7/37 °C (HSR-CO) or pH 9.5/30 °C (AArc-CO) with 0.5 g l−1 yeast extract as the carbon source, CO as the electron donor and elemental sulfur as the electron acceptor.
Fig. 3: Sulfidogenic activity of resting cells of carboxydotrophic haloarchaea grown anaerobically with CO and sulfur.
Fig. 4: Phylogeny of the CooS catalytic subunit from haloarchaeal Ni,Fe-CODH based on maximum likelihood inference.
Fig. 5: Hypothetical scheme of electron transport from CooS to PsrABC in two anaerobic carboxydotrophic haloarchaea (based on genomic content).
Fig. 6: Maximum likelihood phylogenetic tree of catalytic subunit A of molybdopterin oxidoreductases, members of the Complex iron-sulfur molybdoenzyme (CISM) superfamily according to Duval et al. [67].

References

  1. Ragsdale SW. Life with carbon monoxide. Crit Rev Biochem Mol Biol. 2004;39:165–95.

    Article  CAS  PubMed  Google Scholar 

  2. Svetlitchnyi V, Peschel C, Acker G, Meyer O. Two membrane-associated NiFeS-carbon monoxide dehydrogenases from the anaerobic carbon-monoxide-utilizing eubacterium Carboxydothermus hydrogenoformans. J Bacteriol. 2001;183:5134–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Techtmann SM, Lebedinsky AV, Colman AS, Sokolova TG, Woyke T, Goodwin L, et al. Evidence for horizontal gene transfer of anaerobic carbon monoxide dehydrogenases. Front Microbiol. 2012;3:132.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Inoue M, Nakamoto I, Omae K, Oguro T, Ogata H, Yoshida T, et al. Structural and phylogenetic diversity of anaerobic carbon-monoxide dehydrogenases. Front Microbiol. 2020;9:3353.

    Article  Google Scholar 

  5. Jeoung J-H, Martins BM, Dobbek H Carbon monoxide dehydrogenases. In: Hu Y (ed.), Metalloproteins: Methods and Protocols. Methods in Molecular Biology. 2019; 1876:37–54.

  6. King GM, Weber CF. Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol. 2007;5:107–18.

    Article  CAS  PubMed  Google Scholar 

  7. Robb FT, Techtmann SM Life on the fringe: microbial adaptation to growth on carbon monoxide. F1000Research. 2018:7. https://doi.org/10.12688/f1000research.16059.1.

  8. King GM. Carbon monoxide as a metabolic energy source for extremely halophilic microbes: Implications for microbial activity in Mars regolith. Proc Nat Ac Sci USA. 2015;112:4465–70.

    Article  CAS  Google Scholar 

  9. Sokolova TG, Henstra AM, Sipma J, Parshina SN, Stams AJM, Lebedinsky AV. Diversity and ecophysiological features of thermophilic carboxydotrophic anaerobes. FEMS Microbiol Ecol. 2009;68:131–41.

    Article  CAS  PubMed  Google Scholar 

  10. Diender M, Stams AJM, Sousa DZ. Pathways and bioenergetics of anaerobic carbon monoxide fermentation. Front Microbiol. 2015;6:1275.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hoeft SE, Switzer Blum J, Stolz JF, Tabita FR, Witte B, King GM, et al. Alkalilimnicola ehrlichii sp. nov., a novel arsenite-oxidizing, haloalkaliphilic gammaproteobacterium capable of chemoautotrophic or heterotrophic growth with nitrate or oxygen as the electron acceptor. Int J Syst Evol Microbiol. 2007;57:504–12.

    Article  CAS  PubMed  Google Scholar 

  12. Sorokin DY, Kovaleva OL, Tourova TP, Kuenen JG, Muyzer G. Aerobic carboxydotrophy at extremely haloalkaline conditions in Alkalispirillum/Alkalilimnicola strains isolated from soda lakes. Microbiol (SGM). 2010;156:819–27.

    Article  CAS  Google Scholar 

  13. Myers MR, King GM. Perchlorate-coupled carbon monoxide (co) oxidation: evidence for a plausible microbe-mediated reaction in Martian brines. Front Microbiol. 2017;8:2571.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Jensen A, Finster K. Isolation and characterization of Sulfurospirillum carboxydovorans sp. nov., a new microaerophilic carbon monoxide oxidizing epsilonproteobacterium. Antonie van Leeuwenhoek. 2005;87:339–53.

    Article  CAS  PubMed  Google Scholar 

  15. Parshina SN, Sipma J, Henstra AM, Stams AJM Carbon monoxide as an electron donor for the biological reduction of sulphate. Int J Microbiol. 2010;2010:319527.

  16. Fukuyama Y, Omae K, Yoneda Y, Yoshida T, Sako Y. Insight into energy conservation via alternative carbon monoxide metabolism in Carboxydothermus pertinax revealed by comparative genome analysis. Appl Environ Microbiol. 2018;84:e00458–18.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Alves JI, Visser M, Arantes AL, Nijsse B, Plugge CM, Alves MM, et al. Effect of sulfate on carbon monoxide conversion by a thermophilic syngas-fermenting culture dominated by a Desulfofundulus species. Front Microbiol. 2020;11:588468.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Henstra AM, Dijkema C, Stams AJ. Archaeoglobus fulgidus couples CO oxidation to sulfate reduction and acetogenesis with transient formate accumulation. Environ Microbiol. 2007;9:1836–41. 18

    Article  CAS  PubMed  Google Scholar 

  19. Kozhevnikova DA, Taranov EA, Lebedinsky AV, Bonch-Osmolovskaya EA, Sokolova TG. Hydrogenogenic and sulfidogenic growth of Thermococcus archaea on carbon monoxide and formate. Microbiol (Mosc, Engl Translation). 2016;85:400–10.

    Article  CAS  Google Scholar 

  20. Oger P, Sokolova TG, Kozhevnikova DA, Chernyh NA, Bartlett DH, Bonch-Osmolovskaya EA, et al. Complete genome sequence of the hyperthermophilic archaeon Thermococcus sp. strain AM4, capable of organotrophic growth and growth at the expense of hydrogenogenic or sulfidogenic oxidation of carbon monoxide. J Bacteriol. 2011;193:7019–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Benvenuti M, Meneghello M, Guendon C, Jacq-Bailly A, Jeoung J-H, Dobbek H, et al. The two CO-dehydrogenases of Thermococcus sp. AM4. Biochim Biophys Acta. 2020;1861:148188.

    Article  CAS  Google Scholar 

  22. Wu GJ, Schut FLP, Haja DK, Adams MWW. Characterization of membrane-bound sulfane reductase: A missing link in the evolution of modern day respiratory complexes. J Biol Chem. 2018;293:16687–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Allen TD, Caldwell ME, Lawson PA, Huhnke RL, Tanner RS. Alkalibaculum bacchi gen.nov., sp.nov., a CO-oxidizing, ethanol-producing acetogen isolated from livestock-impacted soil. Int J Syst Evol Microbiol. 2010;60:2483–2489.

    Article  CAS  PubMed  Google Scholar 

  24. Liu K, Atiyeh HK, Tanner RS, Wilkins MR, Hahnke RL. Fermentative production of ethanol from syngas using moderately alkaliphilic strains of Alkalibaculum bacchi. Bioresour Technol. 2012;104:336–41.

    Article  CAS  PubMed  Google Scholar 

  25. Khomyakova MA, Merkel AY, Petrova DA, Bonch-Osmolovskaya EA, Slobodkin AI. Alkalibaculum sporogenes sp. nov., isolated from a terrestrial mud volcano and emended description of the genus Alkalibaculum. Int J Syst Evol Microbiol. 2020;70:4914–4919.

    Article  CAS  PubMed  Google Scholar 

  26. Sorokin DY, Diender M, Merkel AY, Koenen M, Bale NJ, Pabst M, et al. Natranaerofaba carboxydovora gen. nov., sp. nov., an extremely haloalkaliphilic CO-utilizing acetogen from a hypersaline soda lake representing a novel deep phylogenetic lineage in the class “Natranaerobiia”. Environ Microbiol. 2021;23:3460–76.

    Article  CAS  PubMed  Google Scholar 

  27. Sorokin DY, Makarova KS, Abbas B, Ferrer M, Golyshin PN, Galinski EA, et al. Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis. Nat Microbiol. 2017;2:17081.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sorokin DY, Kublanov IV, Gavrilov SN, Rojo D, Roman P, Golyshin PN, et al. Elemental sulfur and acetate can support life of a novel strictly anaerobic haloarchaeon. ISME J. 2016;10:240–252.

    Article  CAS  PubMed  Google Scholar 

  29. Sorokin DY, Kublanov IV, Yakimov MM, Rijpstra WI, Sinninghe Damsté JS. Halanaeroarchaeum sulfurireducens gen. nov., sp. nov., the first obligately anaerobic sulfur-respiring haloarchaeon, isolated from a hypersaline lake. Int J Syst Evol Microbiol. 2016;66:2377–81.

    Article  CAS  PubMed  Google Scholar 

  30. Sorokin DY, Yakimov MM, Kublanov IV, Oren A Halanaeroarchaeum. In: Whitman WB (ed). Bergey’s Manual of Systematic of Bacteria and Archaea. John Wiley & Sons, Ltd. 2017; https://doi.org/10.1002/9781118960608.gbm01496.

  31. Sorokin DY, Messina E, Smedile F, Roman P, Sinninghe Damsté JS, Ciordia S, et al. Discovery of anaerobic lithoheterotrophic haloarchaea, ubiquitous in hypersaline habitats. ISME J. 2017;11:1245–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Sorokin DY, Yakimov MM Genus Halodesulfuriarchaeum. In: Whitman WB (ed.). Bergey’s Manual of Systematic of Bacteria and Archaea. John Wiley & Sons, Ltd. 2018. https://doi.org/10.1002/9781118960608.gbm01528. 32

  33. Sorokin DY, Messina E, La Cono V, Ferrer M, Ciordia S, del Carmen Mena, et al. Sulfur respiration in a group of facultatively anaerobic natronoarchaea ubiquitous in hypersaline soda lakes. Front Microbiol. 2018;9:2359.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Sorokin DY, Yakimov MM, Messina E, Merkel AY, Bale NJ, Sinninghe Damsté JS. Natronolimnobius sulfurireducens sp. nov., and Halalkaliarchaeum desulfuricum gen. nov., sp. nov., the first sulfur-respiring alkaliphilic haloarchaea from hypersaline alkaline lakes. Int J Syst Evol Microbiol. 2019;69:2662–73.

    Article  CAS  PubMed  Google Scholar 

  35. Sorokin DY, Merkel AY, Messina E, Yakimov MM, Itoh T, Mesbah NM, et al. Reclassification of the genus Natronolimnobius: proposal of two new genera, Natronolimnohabitans gen. nov. to accommodate Natronolimnobius innermongolicus and Natrarchaeobaculum gen. nov. to accommodate Natronolimnobius aegyptiacus and Natronolimnobius sulfurireducens. Int J Syst Evol Microbiol. 2020;70:3399–405.

    Article  CAS  PubMed  Google Scholar 

  36. Sorokin DY, Merkel AY, Yakimov MM, Oren A. Halalkaliarchaeum. In: Whitman WB (ed.). Bergey’s Manual of Systematics of Archaea and Bacteria. John Wiley & Sons, Ltd. 2020. https://doi.org/10.1002/9781118960608.gbm01943.

  37. Sorokin DY, Messina E, Smedile F, La Cono V, Hallsworth JE, Yakimov MM. Carbohydrate-dependent sulfur respiration in halo(alkali)philic euryarchaea from hypersaline lakes. Environ Microbiol. 2021;23:3779–808. 37

    Article  Google Scholar 

  38. Sorokin DY, Yakimov MM, Messina E, Merkel AY, Koenen M, Bale NJ, et al. Halapricum desulfuricans sp. nov., carbohydrate-utilizing sulfur-reducing haloarchaea from hypersaline lakes. Syst Appl Microbiol. 2021;44:126249.

    Article  CAS  PubMed  Google Scholar 

  39. Pfennig N, Lippert KD. Über das Vitamin B12-Bedürfnis phototropher Schwefelbakterien. Arch Mikrobiol. 1966;55:245–56.

    Article  CAS  Google Scholar 

  40. Plugge CM. Anoxic media design, preparation, and considerations. Methods Enzymol. 2005;397:3–16.

    Article  CAS  PubMed  Google Scholar 

  41. Trüper HG, Schlegel HG. Sulfur metabolism in Thiorhodaceae. 1. Quantitative measurements on growing cells of Chromatium okenii. Antonie van Leeuwenhoek. 1964;30:225–38.

    Article  Google Scholar 

  42. Rinke C, Chuvochina M, Mussig AJ, Chaumeil P-A, Davín AA, Waite DW, et al. A standardized archaeal taxonomy for the Genome Taxonomy Database. Nat Microbiol. 2021;6:946–59.

    Article  CAS  PubMed  Google Scholar 

  43. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol Biol Evol. 2020;37:1530–1534.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.

    Article  CAS  PubMed  Google Scholar 

  45. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol. 2006;55:539–52.

    Article  PubMed  Google Scholar 

  46. Nakamura T, Yamada KD, Tomii K, Katoh K. Parallelization of MAFFT for large­scale multiple sequence alignments. Bioinformatics 2018;34:2490–2492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haesele A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2019;14:587–589.

    Article  Google Scholar 

  48. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009;25:1972–1973.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Kamyshny A, Goifman A, Rizkov D, Lev O. Formation of carbonyl sulfide by the reaction of carbon monoxide and inorganic polysulfides. Environ Sci Technol. 2003;37:1865–72.

    Article  CAS  PubMed  Google Scholar 

  50. Zeer-Wanklyn CJ, Zamble DB. Microbial nickel: cellular uptake and delivery to enzyme centers. Curr Opin Chem Biol. 2017;37:80–88.

    Article  CAS  PubMed  Google Scholar 

  51. Alfano M, Pérard J, Carpentier P, Basset C, Zambelli B, Timm J, et al. The carbon monoxide dehydrogenase accessory protein CooJ is a histidine-rich multidomain dimer containing an unexpected Ni(II)-binding site. J Biol Chem. 2019;294:7601–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Rowinska-Zyrek M, Zakrzewska-Czerwinska J, Zawilak-Pawlik A, Kozlowski H. Ni2+ chemistry in pathogens - a possible target for eradication. Dalton Trans. 2014;43:8976–89.

    Article  CAS  PubMed  Google Scholar 

  53. Sorokin DY. Microbial utilization of glycine betaine in hypersaline soda lakes. Microbiol (Mosc). 2021;90:567–75.

    Google Scholar 

  54. Elling FJ, Becker KW, KönnekeM, Schröder JM, Kellermann MY, Thomm M, et al. Respiratory quinones in Archaea: phylogenetic distribution and application as biomarkers in the marine environment. Environ Microbiol. 2016;18:692–707.

    Article  CAS  PubMed  Google Scholar 

  55. Buckel W, Thauer RK. Flavin-based electron bifurcation, ferredoxin, flavodoxin, and anaerobic respiration with protons (Ech) or NAD+ (Rnf) as electron acceptors: a historical review. Front Microbiol. 2018;9:401.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Buckel W, Thauer RK. Flavin-based electron bifurcation, a new mechanism of biological energy coupling. Chem Rev. 2018;118:3862–86.

    Article  CAS  PubMed  Google Scholar 

  57. Tian L, Lo J, Shao X, Zheng T, Olson DG, Lynda LR. Ferredoxin:NAD oxidoreductase of Thermoanaerobacterium saccharolyticum and its role in ethanol formation. Appl Environ Microbiol. 2016;82:7134–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Friedrich T, Scheide D. The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane bound multisubunit hydrogenases. FEBS Lett. 2000;479:1–5.

    Article  CAS  PubMed  Google Scholar 

  59. Grimaldi S, Schoepp-Cothenet B, Ceccaldi P, Guigliarelli B, Magalon A. The prokaryotic Mo/W-bisPGD enzymes family: A catalytic workhorse in bioenergetic. Biochim Biophys Acta. 2016;1827:1048–85.

    Article  Google Scholar 

  60. Duarte AG, Barbosa ACC, Ferreira D, Manteigas G, Domingos RM, Pereira IAC. Redox loops in anaerobic respiration - The role of the widespread NrfD protein family and associated dimeric redox module. Biochim Biophys Acta. 2021;1862:148416.

    Article  CAS  Google Scholar 

  61. Ledbetter RN, Garcia Costas AM, Lubner CE, Mulder DW, Tokmina-Lukaszewska M, Artz JH, et al. The electron bifurcating FixABCX protein complex from Azotobacter vinelandii: generation of low-potential reducing equivalents for nitrogenase catalysis. Biochemistry. 2017;56:4177–4190. 60

    Article  CAS  PubMed  Google Scholar 

  62. Schut GJ, Mohamed-Raseek N, Tokmina-Lukaszewska M, Mulder DW, Nguyen DMN, Lipscomb GL. The catalytic mechanism of electron-bifurcating electron transfer flavoproteins (ETFs) involves an intermediary complex with NAD+. J Biol Chem. 2019;294:3271–83.

    Article  CAS  PubMed  Google Scholar 

  63. Torregrosa-Crespo J, Pire C, Richardson DJ, Martínez-Espinosa RM. Exploring the molecular machinery of denitrification in Haloferax mediterranei through proteomics. Front Microbiol. 2020;11:605859.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Simon J, Klotz MG. Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations. Biochim Biophys Acta. 2013;1827:114–35.

    Article  CAS  PubMed  Google Scholar 

  65. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Miralles-Robledillo JM, Bernabeu E, Giani M, Martínez-Serna E, Martínez-Espinosa RM, Pire C. Distribution of denitrification among haloarchaea: a comprehensive study. Microorganisms. 2021;9:1669.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Duval S, Ducluzeau A-L, Nitschke W, Schoepp-Cothenet B. Enzyme phylogenies as markers for the oxidation state of the environment: the case of respiratory arsenate reductase and related enzymes. BMC Evol Biol. 2008;8:206.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

DS and AM were supported by the Russian Foundation for Basic Research (RFBR grant 19-04-00401) for field work and isolation of pure cultures and by the Russian Ministry of Science and Higher Education (genomic and phylogenomic analyses). DS and MP were also supported by the Gravitation-SIAM Program of the Dutch Ministry of Education, Culture and Science (grant 24002002). EM, MY and PG were supported by the European Commission’s Horizon 2020 Program under FUTURENZYME Project (Contract 101000327). PG was supported by the Center for Environmental Biotechnology Project, partly funded by the European Regional Development Fund via the Welsh Assembly Government.

Author information

Authors and Affiliations

  1. Winogradsky Institute of Microbiology, Federal Research Centre of Biotechnology, Russian Academy of Sciences, Moscow, Russia

    Dimitry Y. Sorokin & Alexander Y. Merkel

  2. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands

    Dimitry Y. Sorokin, Claudia Tugui & Martin Pabst

  3. IRBIM-CNR, Spianata S.Raineri 86, 98122, Messina, Italy

    Enzo Messina

  4. School of Natural Sciences, Bangor University, Gwynedd, LL57 2UW, UK

    Peter N. Golyshin

  5. Institute of Polar Sciences, ISP-CNR, Messina, Italy

    Michail M. Yakimov

Authors
  1. Dimitry Y. Sorokin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander Y. Merkel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enzo Messina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claudia Tugui
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Martin Pabst
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Peter N. Golyshin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michail M. Yakimov
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DS performed sampling, isolation and physiological characterisation of pure cultures. Bioinformatics analyses was carried out by DS, AM, EM and MY. MP and CT performed proteomic analysis. PG was responsible for the genome sequencing. The data were interpreted and manuscript was written by DS, AM and MY.

Corresponding author

Correspondence to Dimitry Y. Sorokin.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sorokin, D.Y., Merkel, A.Y., Messina, E. et al. Anaerobic carboxydotrophy in sulfur-respiring haloarchaea from hypersaline lakes. ISME J 16, 1534–1546 (2022). https://doi.org/10.1038/s41396-022-01206-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41396-022-01206-x

Search

Advanced search

Quick links