1887

Abstract

A strain of filamentous sulfur bacteria was isolated from freshwater spring contaminated with residential and agricultural wastewater in Moscow region, Russia. According to the results of phylogenetic analysis, strain D-402 belonged to the genus Beggiatoa within the family Beggiatoaceae of the class Gammaproteobacteria . Within the genus Beggiatoa , strain D-402 was most closely related to Beggiatoa alba strains. Strain D-402 had a DNA G+C content 42.1 mol%. The DNA-DNA hybridization value between strain D-402 and Beggiatoa alba strain B15LD was 33 %. Predominant fatty acids were C18 : 1 (46.1 and 53.3 %), C16 : 0 (15.5 and 16.2 %) and C16 : 1 (32.9 and 25.4 %) for strains D-402 and B15LD, respectively. In contrast to known representatives of Beggiatoa , strain D-402 was capable of chemolithoautotrophic growth with sulfide and thiosulfate as electron donors. Oxidation of sulfide and thiosulfate was accompanied by deposition of sulfur globules within the cells. Strain D-402 was capable of heterotrophic growth. The strain was capable of using different organic compounds, sulfur compounds and hydrogen as electron donors. Based on these observations, strain D-402 is considered as a representative of a species Beggiatoa leptomitoformis sp. nov. of the genus Beggiatoa . The type strain is D-402 (=DSM 14946=UNIQEM U 779).

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.001584
2017-03-16
2019-12-09
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/67/2/197.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.001584&mimeType=html&fmt=ahah

References

  1. Teske A, Salman V. The Beggiatoaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. (editors) The Prokaryotes Berlin Heidelberg: Springer; 2014; pp.93–134
    [Google Scholar]
  2. Mezzino MJ, Strohl WR, Larkin JM. Characterization of Beggiatoa alba. Arch Microbiol 1984;137:139–144[CrossRef]
    [Google Scholar]
  3. Strohl WR, Larkin JM. Enumeration, isolation, and characterization of Beggiatoa from freshwater sediments. Appl Environ Microbiol 1978;36:755–770[PubMed]
    [Google Scholar]
  4. Nelson DC, Castenholz RW. Organic nutrition of Beggiatoa sp. J Bacteriol 1981;147:236–247[PubMed]
    [Google Scholar]
  5. Nelson DC, Castenholz RW. Use of reduced sulfur compounds by Beggiatoa sp. J Bacteriol 1981;147:140–154[PubMed]
    [Google Scholar]
  6. Ahmad A, Kalanetra KM, Nelson DC. Cultivated Beggiatoa spp. define the phylogenetic root of morphologically diverse, noncultured, vacuolate sulfur bacteria. Can J Microbiol 2006;52:591–598 [CrossRef][PubMed]
    [Google Scholar]
  7. Pringsheim EG. Heterotrophism and species concepts in Beggiatoa. Amer Jour Bot 1964;51:898–913[CrossRef]
    [Google Scholar]
  8. Grabovich MY, Dubinina GA, Lebedeva VY, Churikova VV. Mixotrophic and litoheterotrophic growth of the freshwater filamentous sulfur bacterium Beggiatoa leptomitiformis D-402. Microbiology 1998;67:383–388
    [Google Scholar]
  9. Grabovich MY, Patritskaya VY, Muntyan MS, Dubinina GA. Lithoautotrophic growth of the freshwater strain Beggiatoa D-402 and energy conservation in a homogeneous culture under microoxic conditions. FEMS Microbiol Lett 2001;204:341–345[PubMed][CrossRef]
    [Google Scholar]
  10. Dubinina GA. Mechanisms of adaptation of colorless sulfur bacteria to the environment. Proceedings of Winogradsky Institute of Microbiology XII 2004;126–148
    [Google Scholar]
  11. Nelson DC, Jannasch HW. Chemoautotrophic growth of a marine Beggiatoa in sulfide-gradient cultures. Arch Microbiol 1983;136:262–269[CrossRef]
    [Google Scholar]
  12. Hagen KD, Nelson DC. Use of reduced sulfur compounds by Beggiatoa spp.: enzymology and physiology of marine and freshwater strains in homogeneous and gradient cultures. Appl Environ Microbiol 1997;63:3957–3964[PubMed]
    [Google Scholar]
  13. Nelson DC, Waterbury JB, Jannasch HW. Nitrogen fixation and nitrate utilization by marine and freshwater Beggiatoa. Arch Microbiol 1982;133:172–177[CrossRef]
    [Google Scholar]
  14. Schwedt A, Kreutzmann AC, Polerecky L, Schulz-Vogt HN. Sulfur respiration in a marine chemolithoautotrophic Beggiatoa strain. Front Microbiol 2012;2:e276[CrossRef]
    [Google Scholar]
  15. Strohl WR. Family I. Beggiatoaceae. In: Staley JT, Bryant MP, Pfennig N, Holt JG. (editors) Bergey’s Manual of Systematic Bacteriology vol. 3, 1st ed Baltimore: Williams & Wilkins; 1989; pp.2089–2106
    [Google Scholar]
  16. Pfennig N, Lippert KD. Über das vitamin B12-Bedürfnis phototropher Schwefelbakterien. Arch Microbiol 1966;55:425–432
    [Google Scholar]
  17. Kuznetsov SI, Dubinina GA. Methods of Investigation of Aqueous Microorganisms In: Yu I, Sorokin M. (editors) Moscow: Nauka; 1989; p. 285
  18. Patritskaya VY, Grabovich MY, Muntyan MS, Dubinina GA. Lithoautotrophic growth of the freshwater colorless sulfur bacterium Beggiatoa ‘leptomitiformis’ D-402. Microbiology 2001;70:145–150[CrossRef]
    [Google Scholar]
  19. Fomenkov A, Vincze T, Grabovich MY, Dubinina G, Orlova M et al. Complete genome sequence of the freshwater colorless sulfur bacterium Beggiatoa leptomitiformis neotype strain D-402T. Genome Announc 2015;3:e01436-15 [CrossRef][PubMed]
    [Google Scholar]
  20. Aziz RK, Bartels D, Best AA, Dejongh M, Disz T et al. The RAST server: rapid annotations using subsystems technology. BMC Genomics 2008;9:75 [CrossRef][PubMed]
    [Google Scholar]
  21. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007;35:182–185[CrossRef]
    [Google Scholar]
  22. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990;215:403–410 [CrossRef][PubMed]
    [Google Scholar]
  23. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J. Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism?. Appl Environ Microbiol 2001;67:2873–2882 [CrossRef][PubMed]
    [Google Scholar]
  24. Kreutzmann AC. Electron donors and acceptors for members of the family Beggiatoaceae The University of Bremen; Dissertation 2013
    [Google Scholar]
  25. Kappler U, Maher MJ. The bacterial SoxAX cytochromes. Cell Mol Life Sci 2013;70:977–992 [CrossRef][PubMed]
    [Google Scholar]
  26. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011;7:539 [CrossRef][PubMed]
    [Google Scholar]
  27. Frolov EN, Belousova EV, Lavrinenko KS, Dubinina GA, Grabovich MY. Capacity of Azospirillum thiophilum for lithotrophic growth coupled to oxidation of reduced sulfur compounds. Microbiology 2013;82:271–279[CrossRef]
    [Google Scholar]
  28. Kelly DP, Wood AP, Jordan SL, Padden AN, Gorlenko VM et al. Biological production and consumption of gaseous organic sulphur compounds. Biochem Soc Trans 1994;22:1011–1015[PubMed][CrossRef]
    [Google Scholar]
  29. Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M et al. Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 1995;373:580–587 [CrossRef][PubMed]
    [Google Scholar]
  30. Vignais PM, Billoud B, Meyer J. Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 2001;25:455–501[PubMed][CrossRef]
    [Google Scholar]
  31. Fujita K, Ehira S, Tanaka K, Asai K, Ohta N. Molecular phylogeny and evolution of the plastid and nuclear encoded cbbX genes in the unicellular red alga Cyanidioschyzon merolae. Genes Genet Syst 2008;83:127–133 [CrossRef][PubMed]
    [Google Scholar]
  32. Spiridonova EM, Berg IA, Kolganova TV, Ivanovsky RN, Kuznetsov BB et al. A system of oligonucleotide primers for the amplification of the ribulose-1,5-bisphosphate carboxylase/oxygenase genes of different taxonomicgroups of bacteria. Mikrobiologiia 2004;73:316–325
    [Google Scholar]
  33. Badger MR, Bek EJ. Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot 2008;59:1525–1541 [CrossRef][PubMed]
    [Google Scholar]
  34. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
  35. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985;39:783–791[CrossRef]
    [Google Scholar]
  36. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4:406–425[PubMed]
    [Google Scholar]
  37. Orlova MV, Shatsky ND, Belousova EV, Grabovich MY. The ability of freshwater filamentous sulfur bacteria from the family Beggiatoaceae to assimilate molecular nitrogen: molecular detection and expression of nifH - the marker gene of nitrogen fixation. Sorption and chromatographic processes 2016;16:280–285
    [Google Scholar]
  38. Stewart WD, Fitzgerald GP, Burris RH. Acetylene reduction by nitrogen-fixing blue-green algae. Arch Mikrobiol 1968;62:336–348[PubMed][CrossRef]
    [Google Scholar]
  39. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 1990;20:16
    [Google Scholar]
  40. Marmur A. A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 1961;3:208–218[CrossRef]
    [Google Scholar]
  41. Owen RJ, Lapage SP. The thermal denaturation of partly purified bacterial deoxyribonucleic acid and its taxonomic applications. J Appl Bacteriol 1976;41:335–340[PubMed][CrossRef]
    [Google Scholar]
  42. de Ley J, Cattoir H, Reynaerts A. The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 1970;12:133–142[PubMed][CrossRef]
    [Google Scholar]
  43. Rainey FA, Ward-Rainey NL, Janssen PH, Hippe H, Stackebrandt E. Clostridium paradoxum DSM 7308T contains multiple 16S rRNA genes with heterogeneous intervening sequences. Microbiology 1996;142:2087–2095 [CrossRef][PubMed]
    [Google Scholar]
  44. Hill JE, Town JR, Hemmingsen SM. Improved template representation in cpn60 polymerase chain reaction (PCR) product libraries generated from complex templates by application of a specific mixture of PCR primers. Environ Microbiol 2006;8:741–746 [CrossRef]
    [Google Scholar]
  45. Trüper HG, Euzéby JP. International code of nomenclature of prokaryotes. Appendix 9: orthography. Int J Syst Evol Microbiol 2009;59:2107–2113 [CrossRef][PubMed]
    [Google Scholar]
  46. Kobayashi S, Shibata H. Metabolic characteristics of Beggiatoa alba in thiosulfate medium and porcine colon contents. Anim Sci J 1999;70:349–355
    [Google Scholar]
  47. Jewell T, Huston SL, Nelson DC. Methylotrophy in freshwater Beggiatoa alba strains. Appl Environ Microbiol 2008;74:5575–5578 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.001584
Loading
/content/journal/ijsem/10.1099/ijsem.0.001584
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most Cited This Month

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