1887

Abstract

Eight pure cultures of alkaliphilic haloaloarchaea capable of growth by dissimilatory sulfur reduction (previously only shown for neutrophilic haloarchaea) were isolated from hypersaline alkaline lakes in different geographic locations. These anaerobic enrichments, inoculated with sediments and brines, used formate, butyrate and peptone as electron donors and elemental sulfur as an electron acceptor 4 M total Na and at pH 9–10. According to 16S rRNA gene sequencing, the isolates fell into two distinct groups. A major group, comprising seven obligate alkaliphilic isolates from highly alkaline soda lakes, represents a new species-level branch within the genus (order ), while a single moderately alkaliphilic isolate from the less alkaline Searles Lake forms a novel genus-level lineage within the order . The cells of the isolates are either flat rods or coccoid. They are facultative anaerobes using formate or H (in the presence of acetate or yeast extract as carbon source), C–C fatty acids or peptone (the major group) as electron donors and either sulfur or DMSO (the major group) as electron acceptors. Aerobic growth is only possible with organic acids and peptone–yeast extract. All isolates are extreme halophiles, growing optimally at 4 M total Na. On the basis of their unique physiological properties and distinct phylogeny, we propose that the seven isolates from the soda lakes are placed into a novel species, sp. nov. (type strain AArc1=JCM 30663=UNIQEM U932), and the Searles Lake isolate, AArc-Sl, into a new genus and species (=JCM 30664=UNIQEM U999).

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.003506
2019-09-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/69/9/2662.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.003506&mimeType=html&fmt=ahah

References

  1. Sorokin DY, Kublanov IV, Gavrilov SN, Rojo D, Roman P et al. Elemental sulfur and acetate can support life of a novel strictly anaerobic haloarchaeon. Isme J 2016; 10:240–252 [View Article][PubMed]
    [Google Scholar]
  2. 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; 66:2377–2381 [View Article][PubMed]
    [Google Scholar]
  3. Sorokin DY, Yakimov MM, Kublanov Iv OA. Halanaeroarchaeum. In Whitman WB. (editor) Bergey's Manual of Systematic of Bacteria and Archaea Chichester: John Wiley & Sons, Ltd; 2017
    [Google Scholar]
  4. Sorokin DY, Messina E, Smedile F, Roman P, Damsté JSS et al. Discovery of anaerobic lithoheterotrophic haloarchaea, ubiquitous in hypersaline habitats. Isme J 2017; 11:1245–1260 [View Article][PubMed]
    [Google Scholar]
  5. Sorokin DY, Messina E. Halodesulfurarchaeum. In Whitman WB. (editor) Bergey's Manual of Systematic of Bacteria and Archaea Chichester: John Wiley & Sons, Ltd; 2018
    [Google Scholar]
  6. Sorokin DY, Rusanov II, Pimenov NV, Tourova TP, Abbas B et al. Sulfidogenesis under extremely haloalkaline conditions in soda lakes of Kulunda Steppe (Altai, Russia). FEMS Microbiol Ecol 2010; 73:278–290 [View Article][PubMed]
    [Google Scholar]
  7. Sorokin DY, Kuenen JG, Muyzer G. The microbial sulfur cycle in soda lakes. Front Microb Physiol 2011; 2:
    [Google Scholar]
  8. Sorokin DY, Messina E, La Cono V, Ferrer M, Ciordia S et al. Sulfur respiration in a group of facultatively anaerobic natronoarchaea ubiquitous in hypersaline soda lakes. Front Microbiol 2018; 9: [View Article][PubMed]
    [Google Scholar]
  9. Sorokin DY, Detkova EN, Muyzer G. Sulfur-dependent respiration under extremely haloalkaline conditions in soda lake 'acetogens' and the description of Natroniella sulfidigena sp. nov. FEMS Microbiol Lett 2011; 319:88–95 [View Article][PubMed]
    [Google Scholar]
  10. Sorokin DY, Foti M, Tindall BJ, Muyzer G. Desulfurispirillum alkaliphilum gen. nov. sp. nov., a novel obligately anaerobic sulfur- and dissimilatory nitrate-reducing bacterium from a full-scale sulfide-removing bioreactor. Extremophiles 2007; 11:363–370 [View Article][PubMed]
    [Google Scholar]
  11. Weijers JWH, Panoto E, van Bleijswijk J, Schouten S, Rijpstra WIC et al. Constraints on the biological source(s) of the orphan branched tetraether membrane lipids. Geomicrobiol J 2009; 26:402–414 [View Article]
    [Google Scholar]
  12. Itoh T, Yamaguchi T, Zhou P, Takashina T. Natronolimnobius baerhuensis gen. nov., sp. nov. and Natronolimnobius innermongolicus sp. nov., novel haloalkaliphilic archaea isolated from soda lakes in inner mongolia, China. Extremophiles 2005; 9:111–116 [View Article][PubMed]
    [Google Scholar]
  13. Validation list no. 105. Int J Syst Evol Microbiol 2005; 55:1743–1745
    [Google Scholar]
  14. Damsté JS, Rijpstra WI, Hopmans EC, Weijers JW, Foesel BU et al. 13,16-Dimethyl octacosanedioic acid (iso-diabolic acid), a common membrane-spanning lipid of Acidobacteria subdivisions 1 and 3. Appl Environ Microbiol 2011; 77:4147–4154 [View Article][PubMed]
    [Google Scholar]
  15. 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]
  16. Sorokin DY, Elcheninov AG, Toshchakov SV, Bale NJ, Sinninghe Damsté JS et al. Natrarchaeobius chitinivorans gen. nov., sp. nov., and Natrarchaeobius halalkaliphilus sp. nov., alkaliphilic, chitin-utilizing haloarchaea from hypersaline alkaline lakes. Syst Appl Microbiol 2019; 42:309–318 [View Article][PubMed]
    [Google Scholar]
  17. Sorokin DY, Khijniak TV, Kostrikina NA, Elcheninov AG, Toshchakov SV et al. Natronobiforma cellulositropha gen. nov., sp. nov., a novel haloalkaliphilic member of the family Natrialbaceae (class Halobacteria) from hypersaline alkaline lakes. Syst Appl Microbiol 2018; 41:355–362 [View Article][PubMed]
    [Google Scholar]
  18. Angelini R, Corral P, Lopalco P, Ventosa A, Corcelli A. Novel ether lipid cardiolipins in archaeal membranes of extreme haloalkaliphiles. Biochim Biophys Acta 2012; 1818:1365–1373 [View Article][PubMed]
    [Google Scholar]
  19. Collins MD. Analysis of isoprenoid quinones. Meth Microbiol 1985; 18:329–363
    [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. Gupta RS, Naushad S, Baker S. Phylogenomic analyses and molecular signatures for the class Halobacteria and its two major clades: a proposal for division of the class Halobacteria into an emended order Halobacteriales and two new orders, Haloferacales ord. nov. and Natrialbales ord. nov., containing the novel families Haloferacaceae fam. nov. and Natrialbaceae fam. nov. Int J Syst Evol Microbiol 2015; 65:1050–1069 [View Article][PubMed]
    [Google Scholar]
  22. Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012; 28:1823–1829 [View Article][PubMed]
    [Google Scholar]
  23. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article][PubMed]
    [Google Scholar]
  24. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article][PubMed]
    [Google Scholar]
  25. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  26. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article][PubMed]
    [Google Scholar]
  27. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119 [View Article][PubMed]
    [Google Scholar]
  28. Nakamura T, Yamada KD, Tomii K, Katoh K. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 2018; 34:2490–2492 [View Article][PubMed]
    [Google Scholar]
  29. 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 [View Article][PubMed]
    [Google Scholar]
  30. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 2006; 55:539–552 [View Article][PubMed]
    [Google Scholar]
  31. Lefort V, Longueville JE, Gascuel O. SMS: smart model selection in PhyML. Mol Biol Evol 2017; 34:2422–2424 [View Article][PubMed]
    [Google Scholar]
  32. 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]
  33. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  34. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Magazine 2014; 9:111–118 [View Article]
    [Google Scholar]
  35. Zhao B, Hu Q, Guo X, Liao Z, Bowers KJ et al. Natronolimnobius aegyptiacus sp. nov., an extremely halophilic alkalithermophilic archaeon isolated from the athalassohaline Wadi An Natrun, Egypt. Int J Syst Evol Microbiol 2018; 68:498–506 [View Article][PubMed]
    [Google Scholar]
  36. Itoh T. Natronolimnobius. In Whitman WB. (editor) Bergey's Manual of Systematic of Bacteria and Archaea Chichester: John Wiley & Sons, Ltd; 2016
    [Google Scholar]
  37. Oren A, Ventosa A, Grant WD. Proposed minimal standards for description of new taxa in the order Halobacteriales . Int J Syst Bacteriol 1997; 47:233–238 [View Article]
    [Google Scholar]
  38. Holding AJ, Collee JG. Routine biochemical tests. Meth Microbiol 1971; 6A:1–32
    [Google Scholar]
  39. Oren A. Halorubraceae. In Whitman WB. (editor) Bergey's Manual of Systematic of Bacteria and Archaea Chichester: John Wiley & Sons, Ltd; 2017
    [Google Scholar]
  40. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.003506
Loading
/content/journal/ijsem/10.1099/ijsem.0.003506
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error