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INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo International Journal of Systematic and Evolutionary Microbiology

Volume 74, Issue 8

gen. nov., sp. nov., an extremely acidophilic organotrophic member of the order Open Access

Abstract

A mesophilic, hyperacidophilic archaeon, strain M1, was isolated from a rock sample from Vulcano Island, Italy. Cells of this organism were cocci with an average diameter of 1 µm. Some cells possessed filaments. The strain grew in the range of temperatures between 15 and 52 °C and pH 0.5–4.0 with growth optima at 40 °C and pH 1.0. Strain M1 was aerobic and chemoorganotrophic, growing on complex substrates, such as casamino acids, trypticase, tryptone, yeast and beef extracts. No growth at expenses of oxidation of elemental sulphur or reduced sulphur compounds, pyrite, or ferrous sulphate was observed. The core lipids were glycerol dibiphytanyl glycerol tetraether lipids (membrane spanning) with 0 to 4 cyclopentane moieties and archaeol, with trace amounts of hydroxy archaeol. The dominant quinone was MK-7 : 7. The genome size of M1 was 1.67 Mbp with a G+C content of 39.76 mol%, and both characteristics were well within the common range for . The phylogenetic analysis based on 16S rRNA gene sequence placed the strain M1 within the order with sequence identities of 90.9, 90.3 and 90.5% to the closest SSU rRNA gene sequences from organisms with validly published names, , and , respectively. Based on the results of our genomic, phylogenetic, physiological and chemotaxonomic studies, we propose that strain M1 (=DSM 116605=JCM 36570) represents a new genus and species, gen. nov., sp. nov., within the order .

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): acidic environments , acidophilic archaea , geothermal environments , Oxyplasma and Thermoplasmatales
Funding
This study was supported by the:
  • NextGenerationEU/PRTR (Award TED2021-130544B-I00)
    • Principle Award Recipient: ManuelFerrer
  • NextGenerationEU/PRTR (Award PDC2021-121534-I00)
    • Principle Award Recipient: ManuelFerrer
  • NextGenerationEU/PRTR (Award PID2020-112758RB-I00)
    • Principle Award Recipient: ManuelFerrer
  • Ministerio de Ciencia e Innovación (Award 10.13039/501100011033)
    • Principle Award Recipient: ManuelFerrer
  • European Regional Development Fund (Award 810280)
    • Principle Award Recipient: PeterN. Golyshin
  • BBSRC (Award BB/M029085/1)
    • Principle Award Recipient: PeterN. Golyshin
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-08-27
2025-07-10
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References

  1. Golyshina OV. Environmental, biogeographic, and biochemical patterns of archaea of the family Ferroplasmaceae. Appl Environ Microbiol 2011; 77:5071–5078 [View Article] [PubMed]
     [Google Scholar]
  2. Huber H, Stetter KO. Thermoplasmatales. In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. eds The Prokaryotes New York: Springer; 2006 [View Article]
     [Google Scholar]
  3. Méndez-García C, Peláez AI, Mesa V, Sánchez J, Golyshina OV et al. Microbial diversity and metabolic networks in acid mine drainage habitats. Front Microbiol 2015; 6:475 [View Article] [PubMed]
     [Google Scholar]
  4. Arce-Rodríguez A, Puente-Sánchez F, Avendaño R, Martínez-Cruz M, de Moor JM et al. Thermoplasmatales and sulfur-oxidizing bacteria dominate the microbial community at the surface water of a CO2-rich hydrothermal spring located in Tenorio Volcano National Park, Costa Rica. Extremophiles 2019; 23:177–187 [View Article] [PubMed]
     [Google Scholar]
  5. Korzhenkov AA, Toshchakov SV, Bargiela R, Gibbard H, Ferrer M et al. Archaea dominate the microbial community in an ecosystem with low-to-moderate temperature and extreme acidity. Microbiome 2019; 7:11 [View Article] [PubMed]
     [Google Scholar]
  6. Distaso MA, Bargiela R, Brailsford FL, Williams GB, Wright S et al. High representation of archaea across all depths in oxic and low-pH sediment layers underlying an acidic stream. Front Microbiol 2020; 11:576520 [View Article] [PubMed]
     [Google Scholar]
  7. Golyshina OV, Lünsdorf H, Kublanov IV, Goldenstein NI, Hinrichs K-U et al. The novel extremely acidophilic, cell-wall-deficient archaeon Cuniculiplasma divulgatum gen. nov., sp. nov. represents a new family, Cuniculiplasmataceae fam. nov., of the order Thermoplasmatales. Int J Syst Evol Microbiol 2016; 66:332–340 [View Article] [PubMed]
     [Google Scholar]
  8. Chuvochina M, Mussig AJ, Chaumeil P-A, Skarshewski A, Rinke C et al. Proposal of names for 329 higher rank taxa defined in the genome taxonomy database under two prokaryotic codes. FEMS Microbiol Lett 2023; 370:370 [View Article] [PubMed]
     [Google Scholar]
  9. Oren A, Göker M. Validation List no. 215. Valid publication of new names and new combinations effectively published outside the IJSEM. Int J Syst Evol Microbiol 2024; 74:doi [View Article] [PubMed]
     [Google Scholar]
  10. Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D et al. Picrophilus gen. nov., fam. nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J Bacteriol 1995; 177:7050–7059 [View Article] [PubMed]
     [Google Scholar]
  11. Rossoni L, Hall SJ, Eastham G, Licence P, Stephens G. The putative mevalonate diphosphate decarboxylase from Picrophilus torridus is in reality a mevalonate-3-kinase with high potential for bioproduction of isobutene. Appl Environ Microbiol 2015; 81:2625–2634 [View Article] [PubMed]
     [Google Scholar]
  12. Murphy J, Walsh G. Purification and characterization of a novel thermophilic β-galactosidase from Picrophilus torridus of potential industrial application. Extremophiles 2019; 23:783–792 [View Article] [PubMed]
     [Google Scholar]
  13. Nagy I, Knispel RW, Kofler C, Orsini M, Boicu M et al. Lipoprotein-like particles in a prokaryote: quinone droplets of Thermoplasma acidophilum. FEMS Microbiol Lett 2016; 363:fnw169 [View Article] [PubMed]
     [Google Scholar]
  14. Lund S, Courtney T, Williams GJ. Probing the substrate promiscuity of isopentenyl phosphate kinase as a platform for hemiterpene analogue production. Chembiochem 2019; 20:2217–2221 [View Article] [PubMed]
     [Google Scholar]
  15. Rennella E, Huang R, Yu Z, Kay LE. Exploring long-range cooperativity in the 20S proteasome core particle from Thermoplasma acidophilum using methyl-TROSY-based NMR. Proc Natl Acad Sci U S A 2020; 117:5298–5309 [View Article] [PubMed]
     [Google Scholar]
  16. Golyshina OV, Yakimov MM, Lünsdorf H, Ferrer M, Nimtz M et al. Acidiplasma aeolicum gen. nov., sp. nov., a euryarchaeon of the family Ferroplasmaceae isolated from a hydrothermal pool, and transfer of Ferroplasma cupricumulans to Acidiplasma cupricumulans comb. nov. Int J Syst Evol Microbiol 2009; 59:2815–2823 [View Article] [PubMed]
     [Google Scholar]
  17. Bale NJ, Ding S, Hopmans EC, Arts MGI, Villanueva L et al. Lipidomics of environmental microbial communities. I: visualization of component distributions using untargeted analysis of high-resolution mass spectrometry data. Front Microbiol 2021; 12:659302 [View Article] [PubMed]
     [Google Scholar]
  18. Yoshinaga MY, Kellermann MY, Rossel PE, Schubotz F, Lipp JS et al. Systematic fragmentation patterns of archaeal intact polar lipids by high-performance liquid chromatography/electrospray ionization ion-trap mass spectrometry. Rapid Commun Mass Spectrom 2011; 25:3563–3574 [View Article] [PubMed]
     [Google Scholar]
  19. Bale NJ, Sorokin DY, Hopmans EC, Koenen M, Rijpstra WIC et al. New insights into the polar lipid composition of extremely halo(alkali)philic Euryarchaea from hypersaline lakes. Front Microbiol 2019; 10:377 [View Article] [PubMed]
     [Google Scholar]
  20. Elling FJ, Becker KW, Könneke M, Schröder JM, Kellermann MY et al. Respiratory quinones in Archaea: phylogenetic distribution and application as biomarkers in the marine environment. Environ Microbiol 2016; 18:692–707 [View Article] [PubMed]
     [Google Scholar]
  21. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
     [Google Scholar]
  22. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
     [Google Scholar]
  23. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
     [Google Scholar]
  24. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
     [Google Scholar]
  25. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. TrimAl: a tool for automated alignment trimming. Bioinformatics 2009; 25:1972–1973 [View Article]
     [Google Scholar]
  26. Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics 2011; 27:592–593 [View Article] [PubMed]
     [Google Scholar]
  27. R Core Team R: a language and environment for statistical computing. R Foundation for Statistical Computing; 2022 https://www.R-project.org
  28. Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 2019; 35:526–528 [View Article] [PubMed]
     [Google Scholar]
  29. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk v2: memory friendly classification with the genome taxonomy database. Bioinformatics 2022; 38:5315–5316 [View Article] [PubMed]
     [Google Scholar]
  30. Macalady JL, Vestling MM, Baumler D, Boekelheide N, Kaspar CW et al. Tetraether-linked membrane monolayers in Ferroplasma spp: a key to survival in acid. Extremophiles 2004; 8:411–419 [View Article] [PubMed]
     [Google Scholar]
  31. Itoh T, Yoshikawa N, Takashina T. Thermogymnomonas acidicola gen. nov., sp. nov., a novel thermoacidophilic, cell wall-less archaeon in the order Thermoplasmatales, isolated from a solfataric soil in Hakone, Japan. Int J Syst Evol Microbiol 2007; 57:2557–2561 [View Article] [PubMed]
     [Google Scholar]
  32. Shimada H, Nemoto N, Shida Y, Oshima T, Yamagishi A. Effects of pH and temperature on the composition of polar lipids in Thermoplasma acidophilum HO-62. J Bacteriol 2008; 190:5404–5411 [View Article] [PubMed]
     [Google Scholar]
  33. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article] [PubMed]
     [Google Scholar]
  34. Fütterer O, Angelov A, Liesegang H, Gottschalk G, Schleper C et al. Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proc Natl Acad Sci U S A 2004; 101:9091–9096 [View Article] [PubMed]
     [Google Scholar]
  35. Azami Y, Hattori A, Nishimura H, Kawaide H, Yoshimura T et al. (R)-mevalonate 3-phosphate is an intermediate of the mevalonate pathway in Thermoplasma acidophilum. J Biol Chem 2014; 289:15957–15967 [View Article] [PubMed]
     [Google Scholar]
  36. Vinokur JM, Cummins MC, Korman TP, Bowie JU. An adaptation to life in acid through a novel mevalonate pathway. Sci Rep 2016; 6:39737 [View Article] [PubMed]
     [Google Scholar]
  37. Hoshino Y, Villanueva L. Four billion years of microbial terpenome evolution. FEMS Microbiol Rev 2023; 47:1–39 [View Article] [PubMed]
     [Google Scholar]
  38. Rawat M, Maupin-Furlow JA. Redox and thiols in archaea. Antioxidants 2020; 9:381 [View Article] [PubMed]
     [Google Scholar]
  39. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
     [Google Scholar]
  40. Darland G, Brock TD, Samsonoff W, Conti SF. A thermophilic, acidophilic mycoplasma isolated from A coal refuse pile. Science 1970; 170:1416–1418 [View Article] [PubMed]
     [Google Scholar]
  41. Segerer A, Langworthy TA, Stetter KO. Thermoplasma acidophilum and Thermoplasma volcanium sp. nov. from solfatara fields. Syst Appl Microbiol 1988; 10:161–171 [View Article]
     [Google Scholar]
  42. Golyshina OV, Pivovarova TA, Karavaiko GI, Kondratéva TF, Moore ER et al. Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. Int J Syst Evol Microbiol 2000; 50:997–1006 [View Article] [PubMed]
     [Google Scholar]
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Oxyplasma meridianum gen. nov., sp. nov., an extremely acidophilic organotrophic member of the order Thermoplasmatales
Int J Syst Evol Microbiol 74, 006499 (2024); https://doi.org/10.1099/ijsem.0.006499
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