Extremophiles

, Volume 21, Issue 3, pp 459–469 | Cite as

Acidicapsa ferrireducens sp. nov., Acidicapsa acidiphila sp. nov., and Granulicella acidiphila sp. nov.: novel acidobacteria isolated from metal-rich acidic waters

Original Paper

Abstract

Four novel strains of Acidobacteria were isolated from water samples taken from pit lakes at two abandoned metal mines in the Iberian Pyrite Belt mining district, south–west Spain. Three of the isolates belong to the genus Acidicapsa (MCF9T, MCF10T, and MCF14) and one of them to the genus Granulicella (MCF40T). All isolates are moderately acidophilic (pH growth optimum 3.8–4.1) and mesophilic (temperature growth optima 30–32 °C). Isolates MCF10T and MCF40T grew at pH lower (<3.0) than previously reported for all other acidobacteria. All four strains are obligate heterotrophs and metabolised a wide range of sugars. While all four isolates are obligate aerobes, MCF9T, MCF10T, and MCF14 catalysed the reductive dissolution of the ferric iron mineral schwertmannite when incubated under micro-aerobic conditions. Isolates MCF9T and MCF14 shared 99.5% similarity of their 16 S rRNA genes, and were considered to be strains of the same species. The major quinone of strains MCF10T, MCF9T, and MCF40T is MK-8, and their DNA G + C contents are 60.0, 59.7, and 62.1 mol%, respectively. Based on phylogenetic and phenotypic data, three novel species, Acidicapsa ferrireducens strain MCF9T (=DSM 28997T = NCCB 100575T), Acidicapsa acidiphila strain MCF10T (=DSM 29819T = NCCB 100576T), and Granulicella acidiphila strain MCF40T (DSM 28996T = NCCB 100577T), are proposed.

Keywords

Acidobacteria Acidophile Metal-tolerance Pit lakes Iron reduction 

Notes

Acknowledgements

The authors would like to acknowledge Anja Frühling, Dr. Susanne Verbarg, and Dr. Brian Tindall (DSMZ-German Collection of Microorganisms and Cell Cultures) for the analysis and identification of polar lipids. Birgit Grün, Brigitte Sträubler, Gabi Pötter, Dr. Peter Schumann, and Dr. Cathrin Spröer (all from DSMZ) for analysis of fatty acids, G + C-content determination and DDH analyses. Dr. Iñaki Yusta and Dr. Javier Sánchez-España for the help provided. The work presented in this paper was partially founded by the Spanish Ministry of Science and Innovation (Project Reference Number CGL2009-09070).

Supplementary material

792_2017_916_MOESM1_ESM.docx (5.7 mb)
Supplementary material 1 (DOCX 5844 KB)

References

  1. Auld RR, Myre M, Mykytczuk NC, Leduc LG, Merritt TJ (2013) Characterization of the microbial acid mine drainage microbial community using culturing and direct sequencing techniques. J Microbiol Methods 93:108–115CrossRefPubMedGoogle Scholar
  2. Baik KS, Choi JS, Kwon J, Park SC, Hwang YM, Kim MS, Kim EM, Seo DC, Cho JS, Seong CN (2013) Terriglobus aquaticus sp. nov., isolated from an artificial reservoir. Int J Syst Evol Microbiol 63:4744–4749CrossRefPubMedGoogle Scholar
  3. Barns SM, Cain EC, Sommerville L, Kuske CR (2007) Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73:3113–3116CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRefPubMedGoogle Scholar
  5. Brosius J, Palmer ML, Kennedy PJ, Noller HF (1978) Complete nucleotide sequence of a 16 S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 75:4801–4805CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cashion P, Hodler-Franklin MA, McCully J, Franklin M (1977) A rapid method for base ratio determination of bacterial DNA. Anal Biochem 81:461–466CrossRefPubMedGoogle Scholar
  7. Collins MD, Jones D (1981) Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implications. Microbiol Rev 45:316–354PubMedPubMedCentralGoogle Scholar
  8. Coupland K, Johnson DB (2008) Evidence that the potential for dissimilatory ferric iron reduction is widespread among acidophilic heterotrophic bacteria. FEMS Microbiol Lett 279:30–35CrossRefPubMedGoogle Scholar
  9. De Ley J, Cattoir H, Reynaerts A (1970) The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12:133–142CrossRefPubMedGoogle Scholar
  10. Falagán C, Johnson DB (2014) Acidibacter ferrireducens gen. nov., sp. nov.: an acidophilic ferric iron-reducing gammaproteobacterium. Extremophiles 18:1067–1073CrossRefPubMedGoogle Scholar
  11. Falagán C, Johnson DB (2016) Acidithiobacillus ferriphilus sp. nov., a facultatively anaerobic iron- and sulfur-metabolizing extreme acidophile. Int J Syst Evol Microbiol 66:206–211CrossRefPubMedPubMedCentralGoogle Scholar
  12. Falagán C, Sánchez-España J, Johnson DB (2014) New insights into the biogeochemistry of extremely acidic environments revealed by a combined cultivation-based and culture-independent study of two stratified pit lakes. FEMS Microbiol Ecol 87:231–243CrossRefPubMedGoogle Scholar
  13. Falagán C, Sánchez-España FJ, Yusta I, Johnson DB (2015) Microbial communities in sediments in acidic, metal-rich mine lakes: results from a study in south–west Spain. Adv Mat Res 1130:7–10.Google Scholar
  14. Falagán C, Sánchez-España J, Yusta I, Johnson DB (2016) New insight into the microbiology of meromictic acidic pit lakes in the Iberian Pyrite Belt (Spain). In Drebenstedt C, Paul M (eds) Proceeding International Mine Water Association 2016: Mining Meets Water – Conflicts and Solutions, pp. 192–198.Google Scholar
  15. Foesel BU, Mayer S, Luckner M, Wanner G, Rohde M, Overmann J (2016) Occallatibacter riparius gen. nov., sp. nov. and Occallatibacter savannae sp. nov., acidobacteria isolated from Namibian soils, and emended description of the family Acidobacteriaceae. Int J Syst Evol Microbiol 66:216–229Google Scholar
  16. García-Moyano A, González-Toril E, Aguilera A, Amils R (2012) Comparative microbial ecology study of the sediments and the water column of Río Tinto, an extreme acidic environment. FEMS Microbiol Ecol 81:303–314CrossRefPubMedGoogle Scholar
  17. González-Toril E, Santofimia E, López-Pamo E, García-Moyano A, Aguilera Á, Amils R (2014) Comparative microbial ecology of the water column of an extreme acidic pit lake, Nuestra Señora del Carmen, and the Río Tinto basin (Iberian Pyrite Belt). Int Microbiol 17:225–233PubMedGoogle Scholar
  18. Hallberg KB, Johnson DB (2003) Novel acidophiles isolated from moderately acidic mine drainage waters. Hydrometallurgy 71:139–148.CrossRefGoogle Scholar
  19. Hallberg KB, Coupland K, Kimura S, Johnson DB (2006) Macroscopic streamer growths in acidic, metal-rich mine waters in north Wales consist of novel and remarkably simple bacterial communities. Appl Environ Microbiol 72:2022–2030CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hallberg KB, González-Toril E, Johnson DB (2010) Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles 14:9–19CrossRefPubMedGoogle Scholar
  21. Hedrich S, Johnson DB (2013) Aerobic and anaerobic oxidation of hydrogen by acidophilic bacteria. FEMS Microbial Lett 349:40–45.Google Scholar
  22. Huang S, Vieira S, Bunk B, Riedel T, Spröer C, Overmann J (2016) First complete genome sequence of a subdivision 6 Acidobacterium strain. Genome Announc 4:e00469–16.PubMedPubMedCentralGoogle Scholar
  23. Huber KJ, Geppert AM, Wanner G, Foesel BU, Wüst PK, Overmann J (2016) Vicinamibacter silvestris—the first representative of the globally widespread subdivision 6 Acidobacteria isolated from subtropical savannah soil. Int J Syst Evol Microbiol. doi:10.1099/ijsem.0.001131 Google Scholar
  24. Huss VAR, Festl H, Schleifer KH (1983) Studies on the spectrophotometric determination of DNA hybridization from renaturation rates. Syst Appl Microbiol 4:184–192CrossRefPubMedGoogle Scholar
  25. Johnson DB, Hallberg KB (2007) Techniques for detecting and identifying acidophilic mineral-oxidising microorganisms. In Rawlings DE, Johnson DB (eds), Biomining Springer-Verlag, Heidelberg, pp 237–262Google Scholar
  26. Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE (2016) The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 7:744.PubMedPubMedCentralGoogle Scholar
  27. Kishimoto N, Kosako Y, Tano T (1991) Acidobacterium capsulatum gen. nov., sp. nov.: An acidophilic chemoorganotrophic bacterium containing menaquinone from acidic mineral environment. Curr Microbiol 22:1–7CrossRefGoogle Scholar
  28. Kishimoto N, Fukaya F, Inagaki K, Sugio T, Tanaka H, Tano T (1995) Distribution of bacteriochlorophyll-a among aerobic and acidophilic bacteria and light-enhanced CO2-incorporation in Acidiphilium rubrum. FEMS Microbiol Ecol 16:291–296CrossRefGoogle Scholar
  29. Kleinsteuber S, Müller FD, Chatzinotas A, Wendt-Potthoff K, Harms H (2008) Diversity and in situ quantification of Acidobacteria subdivision 1 in an acidic mining lake. FEMS Microbiol Ecol 63:107–117CrossRefPubMedGoogle Scholar
  30. Kulichevskaya IS, Kostina LA, Valášková V, Rijpstra WIC, Sinninghe Damsté JS, de Boer W, Dedysh SN (2012) Acidicapsa borealis gen. nov., sp. nov. and Acidicapsa ligni sp. nov., subdivision 1 Acidobacteria from Sphagnum peat and decaying wood. Int J Syst Evol Microbiol 62:1512–1520CrossRefPubMedGoogle Scholar
  31. Leistel JM, Marcoux E, Thiéblemont D, Quesada C, Sánchez A, Almodóvar GR, Pacual E, Sáez R (1998) The volcanic-hosted massive sulphide deposits of the Iberian Pyrite Belt. Miner Deposita 33:2–30CrossRefGoogle Scholar
  32. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar Buchner A, Lai T, Steppi S, other authors (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371CrossRefPubMedPubMedCentralGoogle Scholar
  33. Männistö MK, Rawat S, Starovoytov V, Häggblom MM (2012) Granulicella arctica sp. nov., Granulicella mallensis sp. nov., Granulicella tundricola sp. nov. and Granulicella sapmiensis sp. nov., novel acidobacteria from tundra soil. Int J Syst Evol Microbiol 62:2097–2106CrossRefPubMedGoogle Scholar
  34. Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G + C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39:159–167CrossRefGoogle Scholar
  35. Okamura K, Kawai A, Yamada T, Hiraishi A (2011) Acidipila rosea gen. nov., sp. nov., an acidophilic chemoorganotrophic bacterium belonging to the phylum Acidobacteria. FEMS Microb Lett 3:138–142.CrossRefGoogle Scholar
  36. Pankratov TA, Dedysh SN (2010) Granulicella paludicola gen. nov., sp. nov., Granulicella pectinivorans sp. nov., Granulicella aggregans sp. nov. and Granulicella rosea sp. nov., acidophilic, polymer-degrading acidobacteria from Sphagnum peat bogs. Int J Syst Evol Microbiol 60:2951–2959CrossRefPubMedGoogle Scholar
  37. Rowe OF, Sánchez-España J, Hallberg KB, Johnson DB (2007) Microbial communities and geochemical dynamics in an extremely acidic, metal-rich stream at an abandoned sulfide mine (Huelva, Spain) underpinned by two functional primary production systems. Environ Microbiol 9:1761–1771CrossRefPubMedGoogle Scholar
  38. Sánchez-España FJ, Santofimia E, González-Toril E, San Martín-Úriz P, López-Pamo E, Amils R (2007). Physicochemical and microbiological stratification of a meromictic, acidic mine pit lake (San Telmo, Iberian Pyrite Belt). In Cidu R, Frau F (eds) Proceeding of the International Mine Water Association 2007: Water in Mining Environments, pp. 447–451.Google Scholar
  39. Santofimia E, González-Toril E, López-Pamo E, Gomariz M, Amils R, Aguiler A (2013) Microbial diversity and its relationship to physicochemical characteristics of the water in two extreme acidic pit lakes from the Iberian Pyrite Belt (SW Spain). PLoS One 8:e66746CrossRefPubMedPubMedCentralGoogle Scholar
  40. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. Technical Note no 101. MIDI Inc, Newark, DEGoogle Scholar
  41. Schwertmann U, Cornell RM (2000) Iron oxides in the laboratory: preparation and characterization, 2nd edn. Wiley, Weinheim.CrossRefGoogle Scholar
  42. Stookey L (1970) Ferrozine –a new spectrophotometric reagent for iron. Anal Chem 42:779–781CrossRefGoogle Scholar
  43. Tamaoka J, Komagata K (1984) Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128CrossRefGoogle Scholar
  44. Tindall BJ (1990) Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66:199–202CrossRefGoogle Scholar
  45. Tindall BJ, Sikorski J, Smibert RM, Kreig NR (2007) Phenotypic characterization and the principles of comparative systematics. In Reddy CA, Beveridge TJ, Breznak JA, Marzluf G, Schmidt TM, Snyder LR (eds) Methods for General and Molecular Microbiology 3rd edn. ASM Press, Washington DC, pp 330–393.Google Scholar
  46. Tschech A, Pfennig N (1984) Growth yield increase linked to caffeate reduction in Acetobacterium woodii. Arch Microbiol 137:163–167CrossRefGoogle Scholar
  47. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464CrossRefGoogle Scholar
  48. Yang Y, Wan M-x, Shi W-y, Peng H, Qiu G-z, Zhou J-z, Liu X-d (2007) Bacterial diversity and community structure in acid mine drainage from Dabaoshan Mine, China. Aquat Microb Ecol 47:141–151CrossRefGoogle Scholar
  49. Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer KH, Ludwig W, Glöckner FO, Rosselló-Móra R (2008) The All-Species Living Tree project: a 16 S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31:241–250CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan 2017

Authors and Affiliations

  • Carmen Falagán
    • 1
  • Bärbel Foesel
    • 2
  • Barrie Johnson
    • 1
  1. 1.College of Natural SciencesBangor UniversityBangorUK
  2. 2.Leibniz Institute DSMZ-German Collection of Microorganisms and Cell CulturesBrunswickGermany

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