The Order Haloanaerobiales

  • Aharon Oren


Bottom sediments of hypersaline lakes and lagoons may be expected to support a rich community of anaerobic halophilic bacteria, as the solubility of oxygen in hypersaline brines is low and the amounts of organic matter available are often high (Oren, 1988). Therefore, it is surprising that the first records of obligatory anaerobic fermentative bacteria growing at salt concentrations of 10–20% and higher appeared only in the early 1980s, when Haloanaerobium praevalens was isolated from the bottom sediments of the Great Salt Lake in Utah (Zeikus, 1983; Zeikus et al., 1983) and Sporohalobacter lortetii and Halobacteroides halobius were discovered in Dead Sea sediments (Oren, 1983; Oren et al., 1984b). Haloanaerobium praevalens may be similar to “Bacteroides halosmophilus,” isolated by Baumgartner, 1937 from solar salt and from salted anchovies, but unfortunately no cultures of that isolate have been preserved.

The fermentative obligatory anaerobic halophilic Bacteria appear...


Glycine Betaine Great Salt Lake Hypersaline Lake Signature Nucleotide Hypersaline Lagoon 
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Literature Cited

  1. Baumgartner, J. G. 1937 The salt limits and thermal stability of a new species of anaerobic halophile Food Res. 2 321–329CrossRefGoogle Scholar
  2. Bhupathiraju, V. K., P. K. Sharma, M. J. McInerney, R. M. Knapp, K. Fowler, W. Jenkins. 1991 Isolation and characterization of novel halophilic anaerobic bacteria from oil field brines Dev. Petrol. Sci. 31 132–143Google Scholar
  3. Bhupathiraju, V. K., M. J. McInerney, R. M. Knapp. 1993 Pretest studies for a microbially enhanced oil recovery field pilot in a hypersaline oil reservoir Geomicrobiol. J. 11 19–34CrossRefGoogle Scholar
  4. Bhupathiraju, V. K., A. Oren, P. K. Sharma, R. S. Tanner, C. R. Woese, M. J. McInerney. 1994 Haloanaerobium salsugo sp. nov., a moderately halophilic, anaerobic bacterium from a subterranean brine Int. J. Syst. Bacteriol. 44 565–572PubMedCrossRefGoogle Scholar
  5. Bhupathiraju, V. K., M. J. McInerney, C. R. Woese, R. S. Tanner. 1999 Haloanaerobium kushneri sp. nov., an obligately halophilic, anaerobic bacterium from an oil brine Int. J. Syst. Bacteriol. 49 953–960PubMedCrossRefGoogle Scholar
  6. Bolobova, A. V., M. C. Simankova, N. A. Markovich. 1992 Cellulase complex of a new halophilic bacterium Halocella cellulolytica. Mikrobiologiya 61:804–811 (in Russian) (English translation: Cellulase complex of a new halophilic bacterium Halocella cellulolytica Microbiology 61 557–562Google Scholar
  7. Bykhovsky, V. Y. A., M. A. Pusheva, N. I. Zaitseva, T. N. Zhilina, D. B. Pankovskii, and E. N. Detkova. 1994 Biosynthesis of corrinoids and its possible precursers in extremely halophilic homoacetogenic bacterium Acetohalobium arabaticum gen. nov., sp. nov Pritladnaya Mikrobiologiya Biochimiya (in Russian) 30 93–103Google Scholar
  8. Cayol, J.-L., B. Ollivier, A. Lawson Anani Soh, M.-L. Fardeau, E. Ageron, P. A. D. Grimont, G. Prensier, J. Guezennec, M. Magot, J.-L. Garcia. 1994a Haloincola saccharolytica subsp. senegalensis subsp. nov., isolated from the sediments of a hypersaline lake, and emended description of Haloincola saccharolytica Int. J. Syst. Bacteriol. 44 805–811CrossRefGoogle Scholar
  9. Cayol, J.-L., B. Ollivier, B. K. C. Patel, G. Prensier, J. Guezennec, J.-L. Garcia. 1994b Isolation and characterization of Halothermothrix orenii gen. nov., sp. nov., a halophilic, thermophilic, fermentative, strictly anaerobic bacterium Int. J. Syst. Bacteriol. 44 534–540PubMedCrossRefGoogle Scholar
  10. Cayol, J.-L., B. Ollivier, B. K. C. Patel, E. Ageron, P. A. D. Grimont, G. Prensier, J.-L. Garcia. 1995 Haloanaerobium lacusroseus sp. nov., an extremely halophilic fermentative bacterium from the sediments of a hypersaline lake Int. J. Syst. Bacteriol. 45 790–797PubMedCrossRefGoogle Scholar
  11. Euzéby, J. P. 1998 Taxonomic note: necessary correction of specific and subspecific epithets according to Rules 12c and 13b of the International Code of Nomenclature of Bacteria (1990 Revision) Int. J. Syst. Bacteriol. 48 1073–1075CrossRefGoogle Scholar
  12. Kevbrin, V. V., G. A. Zavarzin. 1992a Methanethiol utilization and sulfur reduction by anaerobic halophilic saccharolytic bacteria Curr. Microbiol. 24 247–250CrossRefGoogle Scholar
  13. Kevbrin, V. V., G. A. Zavarzin. 1992b The effect of sulfur compounds on growth of halophilic homoacetic bacterium Acetohalobium arabaticum. Mikrobiologiya 61:812–817 (in Russian). English translation: Effect of sulfur compounds on the growth of the halophilic homoacetogenic bacterium Acetohalobium arabaticum.) Microbiology 61 563–567Google Scholar
  14. Kevbrin, V. V., T. N. Zhilina, G. A. Zavarzin. 1995 Physiology of homoacetogenic bacteria Acetohalobium arabaticum. Mikrobiologiya 64:165–170 (in Russian). English translation: Physiology of the halophilic homoacetic bacterium Acetohalobium arabaticum.) Microbiology 64 134–138Google Scholar
  15. Liaw, H. J., R. A. Mah. 1992 Isolation and characterization of Haloanaerobacter chitinovorans gen. nov., sp. nov., a halophilic, anaerobic, chitinolytic bacterium from a solar saltern Appl. Environ. Microbiol. 58 260–266PubMedGoogle Scholar
  16. Lowe, S. E., M. K. Jain, J. G. Zeikus. 1993 Biology, ecology, and biotechnological applications of anaerobic bacteria adapted to environmental stresses in temperature, pH, salinity, or substrates Microbiol. Rev. 57 451–509PubMedGoogle Scholar
  17. Matheson, A. T., K. A. Louie, B. D. Tak, M. Zuker. 1987 The primary structure of the ribosomal A-protein (L12) from the halophilic eubacterium Haloanaerobium praevalens Biochimie 69 1013–1020PubMedCrossRefGoogle Scholar
  18. Mouné, S., M. Manac’h, A. Hirshler, P. Caumette, J. C. Willison, R. Matheron. 1999 Haloanaerobacter salinarius sp. nov., a novel halophilic fermentative bacterium that reduces glycine-betaine to trimethylamine with hydrogen or serine as electron donors; emendation of the genus Haloanaerobacter Int. J. Syst. Bacteriol. 49 103–112PubMedCrossRefGoogle Scholar
  19. Ollivier, B., P. Caumette, J.-L. Garcia, R. A. Mah. 1994 Anaerobic bacteria from hypersaline environments Microbiol. Rev. 58 27–38PubMedGoogle Scholar
  20. Oren, A. 1983 Clostridium lortetii sp. nov., a halophilic obligatory anaerobic bacterium producing endospores with attached gas vacuoles Arch. Microbiol. 136 42–48CrossRefGoogle Scholar
  21. Oren, A. 1986a The ecology and taxonomy of anaerobic halophilic eubacteria FEMS Microbiol. Rev. 39 23–29CrossRefGoogle Scholar
  22. Oren, A. 1986b Intracellular salt concentrations of the anaerobic halophilic eubacteria Haloanaerobium praevalens and Halobacteroides halobius Can. J. Microbiol. 32 4–9CrossRefGoogle Scholar
  23. Oren, A. 1987 A procedure for the selective enrichment of Halobacteroides halobius and related bacteria from anaerobic hypersaline sediments FEMS Microbiol. Lett. 42 201–204CrossRefGoogle Scholar
  24. Oren, A. 1988 Anaerobic degradation of organic compounds at high salt concentrations Ant. v. Leeuwenhoek 54 267–277CrossRefGoogle Scholar
  25. Oren, A. 1989 Photosynthetic and heterotrophic benthic bacterial communities of a hypersaline sulfur spring on the shore of the Dead Sea. In: Y. Cohen and E. Rosenberg (eds.), Microbial mats. Physiological ecology of benthic microbial communities American Society for Microbiology Washington, DC 64–76Google Scholar
  26. Oren, A. 1990 Anaerobic degradation of organic compounds in hypersaline environments: possibilities and limitations. In: D. L. Wise (ed.), Bioprocessing and biotreatment of coal Marcel Dekker New York NY 155–175Google Scholar
  27. Oren, A. 1993a The genera Haloanaerobium, Halobacteroides, and Sporohalobacter. In: A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer (eds.), The prokaryotes. A handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, 2nd ed Springer-Verlag New York NY II 1893–1900Google Scholar
  28. Oren, A. 1993b Anaerobic heterotrophic bacteria growing at extremely high salt concentrations. In: R. Guerrero and C. Pedrós-Alió (eds.), Trends in microbial ecology Spanish Society for Microbiology Madrid Spain 539–542Google Scholar
  29. Oren, A., P. Gurevich. 1993 The fatty acid synthetase complex of Haloanaerobium praevalens is not inhibited by salt FEMS Microbiol. Lett. 108 287–290CrossRefGoogle Scholar
  30. Oren, A., B. J. Paster, C. R. Woese. 1984a Haloanaerobiaceae: a new family of moderately halophilic, obligatory anaerobic bacteria Syst. Appl. Microbiol. 5 71–80CrossRefGoogle Scholar
  31. Oren, A., W. G. Weisburg, M. Kessel, C. R. Woese. 1984b Halobacteroides halobius gen. nov., sp. nov., a moderately halophilic anaerobic bacterium from the bottom sediments of the Dead Sea Syst. Appl. Microbiol. 5 58–70CrossRefGoogle Scholar
  32. Oren, A., H. Pohla, E. Stackebrandt. 1987 Transfer of Clostridium lortetii to a new genus Sporohalobacter gen. nov. as Sporohalobacter lortetii comb. nov., and description of Sporohalobacter marismortui sp. nov Syst. Appl. Microbiol. 9 239–246CrossRefGoogle Scholar
  33. Oren, A., L. V. Gofshtein-Gandman, A. Keynan. 1989 Hydrolysis of N′-benzoyl-D-arginine-p-nitroanilide by members of the Haloanaerobiaceae: additional evidence that Haloanaerobium praevalens is related to endospore-forming bacteria FEMS Microbiol. Lett. 58 5–10Google Scholar
  34. Oren, A., P. Gurevich, Y. Henis. 1991 Reduction of nitrosubstituted aromatic compounds by the halophilic eubacteria Haloanaerobium praevalens and Sporohalobacter marismortui Appl. Environ. Microbiol. 57 3367–3370PubMedGoogle Scholar
  35. Oren, A., P. Gurevich, M. Azachi. 1992 Microbial degradation of pollutants at high salt concentrations Biodegradation 3 387–398CrossRefGoogle Scholar
  36. Oren, A., M. Heldal, S. Norland. 1997 X-ray microanalysis of intracellular ions in the anaerobic halophilic eubacterium Haloanaerobium praevalens Can. J. Microbiol. 43 588–592CrossRefGoogle Scholar
  37. Patel, B. K. C., K. T. Andrews, B. Ollivier, R. A. Mah, J.-L. Garcia. 1995 Reevaluating the classification of Halobacteroides and Haloanaerobacter species based on sequence comparisons of the 16S ribosomal RNA gene FEMS Microbiol. Lett. 134 115–119PubMedCrossRefGoogle Scholar
  38. Pusheva, M. A., E. N. Detkova. 1996 Bioenergetic aspects of acetogenesis on various substrates by the extremely halophilic acetogenic bacterium Acetohalobium arabaticum. Mikrobiologiya (in Russian). (English translation: Bioenergetic aspects of acetogenesis on various substrates by the extremely halophilic acetogenic bacterium Acetohalobium arabaticum.) Mikrobiologiya 65 589–593Google Scholar
  39. Pusheva, M. A., E. N. Detkova, N. P. Bolotina, T. N. Zhilina. 1992 The properties of periplasmic hydrogenase from extremely halophilic homoacetogenic bacterium Acetohalobium arabaticum. Mikrobiologiya (in Russian). (English translation: Properties of periplasmatic hydrogenase of Acetohalobium arabaticum, an extremely halophilic homoacetogenic bacterium.) Microbiology 61 653–657Google Scholar
  40. Rainey, F. A., T. N. Zhilina, E. S. Boulygina, E. Stackebrandt, T. P. Tourova, G. A. Zavarzin. 1995 The taxonomic status of the fermentative halophilic anaerobic bacteria: description of Halobacteriales ord. nov., Halobacteroidaceae fam. nov., Orenia gen. nov. and further taxonomic rearrangements at the genus and species level Anaerobe 1 185–199PubMedCrossRefGoogle Scholar
  41. Ravot, G., M. Magot, B. Ollivier, B. K. C. Patel, E. Ageron, P. A. D. Grimont, P. Thomas, J.-L. Garcia. 1997 Haloanaerobium congolense sp. nov., an anaerobic, moderately halophilic, thiosulfate-and sulfur-reducing bacterium from an African oil field FEMS Microbiol. Lett. 147 81–88PubMedCrossRefGoogle Scholar
  42. Rengpipat, S., T. A. Langworthy, J. G. Zeikus. 1988a Halobacteroides acetoethylicus sp. nov., a new obligately anaerobic halophile isolated from deep subsurface hypersaline environments Syst. Appl. Microbiol. 11 28–35CrossRefGoogle Scholar
  43. Rengpipat, S., S. E. Lowe, J. G. Zeikus. 1988b Effect of extreme salt concentrations on the physiology and biochemistry of Halobacteroides acetoethylicus J. Bacteriol. 170 3065–3071PubMedGoogle Scholar
  44. Senyushkin, A. A., L. O. Severina, T. N. Zhilina. 1992 Influence of the environmental conditions on glucose transport in cells of halophilic anaerobic eubacteria of the genus Halobacteroides. Mikrobiologiya (in Russian). (English translation: Influence of the environmental conditions on glucose transport in cells of halophilic anaerobic eubacteria of the genus Halobacteroides.) Microbiology 60 545–549Google Scholar
  45. Severina, L. O., A. A. Senyushkin, T. N. Zhilina. 1992 Glucose uptake systems in halophilic anaerobic eubacteria of the genus Halobacteroides (in Russian) Mikrobiologiya 61 353–358Google Scholar
  46. Shiba, H. 1991 Anaerobic halophiles. In: K. Horikoshi and W. D. Grant (eds.),Superbugs. Microorganisms in extreme environments Japan Scientific Societies Press Springer-Verlag Tokyo Japan 191–211Google Scholar
  47. Shiba, H., K. Horikoshi. 1988 Isolation and characterization of novel anaerobic, halophilic eubacteria from hypersaline environments of western America and Kenya In: Proceedings of the FEMS Symposium on the microbiology of extreme environments and its biotechnological potential Portugal Spain 371–374Google Scholar
  48. Shiba, H., H. Yamamoto, K. Horikoshi. 1989 Isolation of strictly anaerobic halophiles from the aerobic surface sediments of hypersaline environments in California and Nevada FEMS Microbiol. Lett. 57 191–196CrossRefGoogle Scholar
  49. Simankova, M. V., G. A. Zavarzin. 1992 The anaerobic cellulose degradation in the Sivash lake and hypersaline lagoons of the Arabatskaya spit (in Russian) Mikrobiologiya 61 288–293Google Scholar
  50. Simankova, M. V., N. A. Chernych, G. A. Zavarzin. 1993 Halocella cellulolytica gen. nov., sp. nov., a new obligately anaerobic, halophilic, cellulolytic bacterium Syst. Appl. Microbiol. 16 385–389CrossRefGoogle Scholar
  51. Tourova, T. P., E. S. Boulygina, T. N. Zhilina, R. S. Hanson, G. A. Zavarzin. 1995 Phylogenetic study of haloanaerobic bacteria by 16S ribosomal RNA sequence analysis Syst. Appl. Microbiol. 18 189–195CrossRefGoogle Scholar
  52. Trüper, H. G., L. de’Clari. 1997 Taxonomic note: necessary corrections of specific epithets formed as substantives (nouns) “in apposition.” Int. J. Syst. Bacteriol. 47 908–909CrossRefGoogle Scholar
  53. Trüper, H. G., L. de’ Clari. 1998 Taxonomic note: erratum and correction of further specific epithets formed as substantives (nouns) “in apposition” Int. J. Syst. Bacteriol. 48 615Google Scholar
  54. Tsai, C.-R., J.-L. Garcia, B. K. C. Patel, J.-L. Cayol, L. Baresi, R. A. Mah. 1995 Haloanaerobium alcaliphilum sp. nov., an anaerobic moderate halophile from the sediments of Great Salt Lake, Utah Int. J. Syst. Bacteriol. 45 301–307PubMedCrossRefGoogle Scholar
  55. Wise, D. L. 1984 Meeting report—First international workshop on biogasification and biorefining of Texas lignite Resources and Conservation 15 229–247CrossRefGoogle Scholar
  56. Zavarzin, G. A., T. N. Zhilina, M. A. Pusheva. 1994 Halophilic acetogenic bacteria In: H. L. Drake (ed.) Acetogenesis Chapman and Hall New York NY 432–444Google Scholar
  57. Zeikus, J. G. 1983 Metabolic communication between biodegradative populations in nature. In: J. H. Slater, R. Whittenbury, and J. W. T. Wimpenny (eds.), Microbes in their natural environments 34th Symp., Soc. Gen. Microbiol. Cambridge University Press Cambridge England 423–462Google Scholar
  58. Zeikus, J. G., P. W. Hegge, T. E. Thompson, T. J. Phelps, T. A. Langworthy. 1983 Isolation and description of Haloanaerobium praevalens gen. nov. and sp. nov., an obligately anaerobic halophile common to Great Salt Lake sediments Curr. Microbiol. 9 225–234CrossRefGoogle Scholar
  59. Zhilina, T. N., G. A. Zavarzin. 1990a Extremely halophilic, methylotrophic, anaerobic bacteria FEMS Microbiol. Rev. 87 315–322CrossRefGoogle Scholar
  60. Zhilina, T. N., G. A. Zavarzin. 1990b A new extremely halophilic homoacetogenic bacterium Acetohalobium arabaticum gen. nov., sp. nov. (in Russian) Dokl. Akad. Nauk. SSSR 311 745–747Google Scholar
  61. Zhilina, T. N., G. A. Zavarzin. 1991 Anaerobic bacteria participating in organic matter destruction in halophilic cyanobacterial community J. Obshey. Biol. 52 302–318Google Scholar
  62. Zhilina, T. A., G. A. Zavarzin. 1994 Alkaliphilic anaerobic community at pH 10 Curr. Microbiol. 29 109–112CrossRefGoogle Scholar
  63. Zhilina, T. N., V. V. Kevbrin, A. M. Lysenko, G. A. Zavarzin. 1991 Saccharolytic anaerobic bacteria in a halophilic cyanobacterial mat (in Russian) Mikrobiologiya 60 139–147Google Scholar
  64. Zhilina, T. N., L. V. Miroshnikova, G. A. Osipov, G. A. Zavarzin. 1992a Halobacteroides lacunaris sp. nov., new saccharolytic, anaerobic, extremely halophilic organism from the lagoon-like hypersaline lake Chokrak (in Russian) Mikrobiologiya 60 714–724Google Scholar
  65. Zhilina, T. N., G. A. Zavarzin, E. S. Bulygina, V. V. Kevbrin, G. A. Osipov, K. M. Chumakov. 1992b Ecology, physiology and taxonomy studies on a new taxon of Haloanaerobiaceae, Haloincola saccharolytica gen. nov., sp. nov Syst. Appl. Microbiol. 15 275–284CrossRefGoogle Scholar
  66. Zhilina, T. N., G. A. Zavarzin, E. N. Detkova, F. A. Rainey. 1996 Natroniella acetigena gen. nov. sp. nov., an extremely haloalkaliphilic, homoacetogenic bacterium: a new member of Haloanaerobiales Curr. Microbiol. 32 320–326PubMedCrossRefGoogle Scholar
  67. Zhilina, T. N., T. P. Turova, A. M. Lysenko, V. V. Kevbrin. 1997 Reclassification of Halobacteroides halobius Z-7287 on the basis of phylogenetic analysis as a new species Halobacteroides elegans sp. nov. (in Russian) Mikrobiologiya 66 114–121Google Scholar

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  • Aharon Oren

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