sp. nov., an acidophilic bacterium inhabiting mine tailings from a polymetallic mine Open Access

Abstract

A mixotrophic and acidophilic bacterial strain BGR 140 was isolated from mine tailings in the Harz Mountains near Goslar, Germany. Cells of BGR 140 were Gram-stain-positive, endospore-forming, motile and rod-shaped. BGR 140 grew aerobically at 25–55 °C (optimum 45 °C) and at pH 1.5–5.0 (optimum pH 3.0). The results of analysis of the 16S rRNA gene sequences indicated that BGR 140 was phylogenetically related to different members of the genus , and the sequence identities to DSM 10332, DSM 17362, and DSM 19468 were 94.8, 91.8 and 91.6 %, respectively. Its cell wall peptidoglycan is A1, composed of -diaminopimelic acid. The respiratory quinone is DMK-6. The major polar lipids were determined to be glycolipid, phospholipid and phosphatidylglycerol. The predominant fatty acid is 11-cycloheptanoyl-undecanoate. The genomic DNA G+C content is 58.2 mol%. On the basis of the results of phenotypic and genomic analyses, it is concluded that strain BGR 140 represents a novel species of the genus , for which the name sp. nov. is proposed because of its origin. Its type strain is BGR 140 (=DSM 109850=JCM 39070).

Funding
This study was supported by the:
  • National Natural Science Foundation of China (Award 42076044)
    • Principle Award Recipient: NotApplicable
  • Deutsche Forschungsgemeinschaft (Award SCHI 535/15-1)
    • Principle Award Recipient: NotApplicable
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2021-07-08
2024-03-28
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References

  1. Golovacheva RS, Karavaiko G. Sulfobacillus, a new genus of thermophilic sporulating bacteria. Mikrobiologiia 1978; 47:815–822 [PubMed]
    [Google Scholar]
  2. Johnson DB, Joulian C, d’Hugues P, Hallberg KB. Sulfobacillus benefaciens sp. nov., an acidophilic facultative anaerobic Firmicute isolated from mineral bioleaching operations. Extremophiles 2008; 12:789–798 [View Article] [PubMed]
    [Google Scholar]
  3. Norris PR, Clark DA, Owen JP, Waterhouse S. Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulphide-oxidizing bacteria. Microbiology 1996; 142:775–783 [View Article]
    [Google Scholar]
  4. Bogdanova TI, Tsaplina IA, Kondrat’eva TF, Duda VI, Suzina NE et al. Sulfobacillus thermotolerans sp. Nov., a thermotolerant, chemolithotrophic bacterium. Int J Syst Evol Microbiol 2006; 56:1039–1042 [View Article]
    [Google Scholar]
  5. Melamud VS, Pivovarova TA, Turova TP, Kolganova TV, Osipov GA et al. [Sulfobacillus sibiricus sp. nov., a new moderately thermophilic bacterium]. Mikrobiologiia 2003; 72:681–688 [PubMed]
    [Google Scholar]
  6. Dufresne S, Bousquet J, Boissinot M, Guay R. Sulfobacillus disulfidooxidans sp. nov., a new acidophilic, disulfide-oxidizing, Gram-positive, spore-forming bacterium. Int J Syst Evol Microbiol 1996; 46:1056–1064
    [Google Scholar]
  7. Karavaiko GI, Bogdanova TI, Tourova TP, Kondrat’eva TF, Tsaplina IA et al. Reclassification of “Sulfobacillus thermosulfidooxidans subsp. thermotolerans” strain K1 as Alicyclobacillus tolerans sp. nov. and Sulfobacillus disulfidooxidans Dufresne et al. 1996 as Alicyclobacillus disulfidooxidans comb. nov., and emended description of the genus Alicyclobacillus. Int J Syst Evol Microbiol 2005; 55:941–947 [View Article]
    [Google Scholar]
  8. Vos P, Garrity G, Jones D, Krieg NR, Ludwig W et al. Bergey's Manual of Systematic Bacteriology: Volume 3: The Firmicutes Springer Science & Business Media; 2011
    [Google Scholar]
  9. Watling HR, Perrot FA, Shiers DW. Comparison of selected characteristics of Sulfobacillus species and review of their occurrence in acidic and bioleaching environments. Hydrometallurgy 2008; 93:57–65 [View Article]
    [Google Scholar]
  10. Baker BJ, Banfield JF. Microbial communities in acid mine drainage. FEMS Microbiol Ecol 2003; 44:139–152 [View Article] [PubMed]
    [Google Scholar]
  11. Schippers A. Microorganisms involved in bioleaching and nucleic acid-based molecular methods for their identification and quantification. Donati E, Sand W. eds In Microbial Processing of Metal Sulfides Dordrecht: Springer; 2007 pp 3–33
    [Google Scholar]
  12. Johnson DB. Biomining-biotechnologies for extracting and recovering metals from ores and waste materials. Curr Opin Biotechnol 2014; 30:24–31 [View Article] [PubMed]
    [Google Scholar]
  13. Schippers A, Hedrich S, Vasters J, Drobe M, Sand W et al. Biomining: metal recovery from ores with microorganisms. Schippers A, Glombitza F, Sand W. eds In Geobiotechnology I - Metal Related Issues, Advances in Biochemical Engineering & Biotechnology Berlin: Heidelberg Springer; 2014 pp 1–47
    [Google Scholar]
  14. Liu H-C, Nie Z-Y, Xia J-L, Zhu H-R, Yang Y et al. Investigation of copper, iron and sulfur speciation during bioleaching of chalcopyrite by moderate thermophile Sulfobacillus thermosulfidooxidans. Int J Miner Process 2015; 137:1–8
    [Google Scholar]
  15. Li Q, Zhu J, Li S, Zhang R, Xiao T et al. Interactions between cells of Sulfobacillus thermosulfidooxidans and Leptospirillum ferriphilum during pyrite bioleaching. Front Microbiol 202011
    [Google Scholar]
  16. Christel S, Herold M, Bellenberg S, Buetti-Dinh A, El Hajjami M et al. Weak iron oxidation by Sulfobacillus thermosulfidooxidans maintains a favorable redox potential for chalcopyrite bioleaching. Front Microbiol 2018; 9:3059 [View Article] [PubMed]
    [Google Scholar]
  17. Huynh D, Giebner F, Kaschabek SR, Rivera-Araya J, Levican G et al. Effect of sodium chloride on leptospirillum ferriphilum DSM 14647T and sulfobacillus thermosulfidooxidans DSM 9293T: Growth, iron oxidation activity and bioleaching of sulfidic metal ores. Miner Eng 2019; 138:52–59 [View Article]
    [Google Scholar]
  18. Zhang R, Hedrich S, Römer F, Goldmann D, Schippers A. Bioleaching of cobalt from cu/co-rich sulfidic mine tailings from the polymetallic Rammelsberg mine, Germany. Hydrometallurgy 2020; 197:105443 [View Article]
    [Google Scholar]
  19. Ňancucheo I, Rowe OF, Hedrich S, Johnson DB. Solid and liquid media for isolating and cultivating acidophilic and acid-tolerant sulfate-reducing bacteria. FEMS Microbiol Lett 2016363
    [Google Scholar]
  20. Johnson DB, Hallberg KB. Techniques for detecting and identifying acidophilic mineral-oxidizing microorganisms. Rawlings D, Johnson D. eds In Biomining Berlin, Heidelberg: Springer Berlin Heidelberg; 2007 pp 237–261
    [Google Scholar]
  21. Johnson DB, McGinness S. A highly effecient and universal solid medium for growing mesophilic and moderately thermophilic, iron-oxidizing, acidophilic bacteria. J Microbiol Methods 1991; 13:113–122
    [Google Scholar]
  22. Johnson D. Selective solid media for isolating and enumerating acidophilic bacteria. J Microbiol Methods 1995; 23:205–218 [View Article]
    [Google Scholar]
  23. Webster G, Newberry CJ, Fry JC, Weightman AJ. Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J Microbiol Methods 2003; 55:155–164 [View Article] [PubMed]
    [Google Scholar]
  24. Hall TA. Bioedit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symposium Series London: Information Retrieval Ltd., c1979-c2000; 1999 pp 95–98
    [Google Scholar]
  25. Lagesen K, Hallin P, Rødland EA, Stærfeldt H-H, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article]
    [Google Scholar]
  26. 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]
  27. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  28. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
    [Google Scholar]
  29. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  30. Nguyen L-T, Schmidt HA, Von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
    [Google Scholar]
  31. Felsenstein J. Statistical inference of phylogenies. J R Stat Soc A Stat 1983; 146:246–262
    [Google Scholar]
  32. Meier-Kolthoff JP, Goker 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]
  33. Meier-Kolthoff JP, Auch AF, Klenk H-P, 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. Lefort V, Desper R, Gascuel O. FastME 2.0: A comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article] [PubMed]
    [Google Scholar]
  35. Farris JS. Estimating phylogenetic trees from distance matrices. The American Naturalist 1972; 106:645–668 [View Article]
    [Google Scholar]
  36. Wayne L, Brenner D, Colwell R, Grimont P, Kandler O et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 1987; 37:463–464 [View Article]
    [Google Scholar]
  37. Yoon SH, Ha S, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Anton Leeuw Int J G 2017; 110:1281–1286
    [Google Scholar]
  38. 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]
  39. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article] [PubMed]
    [Google Scholar]
  40. Palmer M, Steenkamp ET, Blom J, Hedlund BP, Venter SN. All ANIs are not created equal: implications for prokaryotic species boundaries and integration of ANIs into polyphasic taxonomy. Int J Syst Evol Microbiol 2020; 70:2937–2948 [View Article] [PubMed]
    [Google Scholar]
  41. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100–3108 [View Article]
    [Google Scholar]
  42. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9:1–15
    [Google Scholar]
  43. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S et al. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5:8365 [View Article] [PubMed]
    [Google Scholar]
  44. Huerta-Cepas J, Szklarczyk D, Heller D. Eggnog 5.0: A hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2018; 47:D309–D314
    [Google Scholar]
  45. Zhang X, Liu X, Liang Y, Guo X, Xiao Y et al. Adaptive evolution of extreme acidophile Sulfobacillus thermosulfidooxidans potentially driven by horizontal gene transfer and gene loss. Appl Environ Microbiol 2017; 83:e03098 [View Article]
    [Google Scholar]
  46. Justice NB, Norman A, Brown CT, Singh A, Thomas BC et al. Comparison of environmental and isolate Sulfobacillus genomes reveals diverse carbon, sulfur, nitrogen, and hydrogen metabolisms. BMC Genomics 2014; 15:1107 [View Article] [PubMed]
    [Google Scholar]
  47. Schumann P. Peptidoglycan structure. Method Microbiol 2011; 38:101–129
    [Google Scholar]
  48. Kuykendall L, Roy M, O’neill J, Devine T. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Evol Microbiol 1988; 38:358–361
    [Google Scholar]
  49. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16:584–586 [View Article] [PubMed]
    [Google Scholar]
  50. Moss CW, Lambert-Fair MA. Location of double bonds in monounsaturated fatty acids of Campylobacter cryaerophila with dimethyl disulfide derivatives and combined gas chromatography-mass spectrometry. J Clin Microbiol 1989; 27:1467–1470 [View Article] [PubMed]
    [Google Scholar]
  51. Harvey DJ. Picolinyl esters as derivatives for the structural determination of long chain branched and unsaturated fatty acids. In Biological Mass Spectrometry Vol 9January 1982 1982 pp 33–38 [View Article]
    [Google Scholar]
  52. Spitzer V. Structure analysis of fatty acids by gas chromatography—low resolution electron impact mass spectrometry of their 4, 4-dimethyloxazoline derivatives—a review. Prog Lipid Res 1996; 35:387–408 [View Article] [PubMed]
    [Google Scholar]
  53. Yu Q, Liu B, Zhang J, Huang Z. Location of methyl branchings in fatty acids: fatty acids in uropygial secretion of Shanghai duck by GC-MS of 4, 4-dimethyloxazoline derivatives. Lipids 1988; 23:804–810 [View Article] [PubMed]
    [Google Scholar]
  54. Tindall B. A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 1990; 13:128–130 [View Article]
    [Google Scholar]
  55. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem 1959; 37:911–917 [View Article] [PubMed]
    [Google Scholar]
  56. Mesbah M, Premachandran U, Whitman WB. Precise measurement of the G+ C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Evol Microbiol 1989; 39:159–167
    [Google Scholar]
  57. Zhang R, Neu TR, Blanchard V, Vera M, Sand W. Biofilm dynamics and EPS production of a thermoacidophilic bioleaching archaeon. New Biotechnol 2019; 51:21–30 [View Article]
    [Google Scholar]
  58. Yang Y, Tan S, Glenn A, Harmer S, Bhargava S et al. A direct observation of bacterial coverage and biofilm formation by Acidithiobacillus ferrooxidans on chalcopyrite and pyrite surfaces. Biofouling 2015; 31:575–586 [View Article] [PubMed]
    [Google Scholar]
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