Life at High Salt and Low Oxygen: How Do the Halobacteriaceae Cope with Low Oxygen Concentrations in Their Environment?

  • Aharon OrenEmail author
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 27)


Halophilic Archaea of the family Halobacteriaceae generally lead an aerobic chemoheterotrophic life. As the solubility of oxygen in concentrated brines is very small, it can be expected that these organisms will often experience a limited availability of molecular oxygen. To cope with the potential lack of oxygen, many members of the Halobacteriaceae have developed strategies enabling them to grow and survive in the absence of oxygen and/or ways to move toward more oxygen-rich niches. Some species can grow by denitrification, reducing nitrate to N2 and N2O. Some can couple growth with the reduction of other alternative electron acceptors such as dimethyl sulfoxide (DMSO), trimethylamine N-oxide (TMAO), and/or fumarate. Fermentative growth is rarely found among the halophilic Archaea, but growth of Halobacterium spp. by fermentation of arginine is well documented. Halobacterium salinarum and probably a few other species as well can use light energy absorbed by bacteriorhodopsin for photoheterotrophic growth. Another strategy used by some members of the group is to move toward more oxygen-rich areas, either by active motility (aerotaxis) or by passive flotation by means of gas vesicles. It is tempting to speculate that these strategies may help halophilic Archaea to grow and survive in situations where oxygen is limiting. However, nitrate is seldom abundant in hypersaline lakes (also due to the absence of autotrophic nitrification at high salt concentrations), and there is no reason to assume that DMSO, fumarate, or arginine may accumulate in any hypersaline environment to concentrations high enough to support anaerobic growth. TMAO may become available during the decay of salted fish but hardly elsewhere. Only a few species of Halobacteriaceae produce gas vesicles, and there is little evidence that those that do can exploit them to efficiently buoy up to the brine surface in natural salt lakes and saltern ponds to reach the oxygen. It is not yet clear to what extent their communities are truly oxygen limited in their natural environments. The fact that the halophilic Archaea also possess genes, encoding enzymes important in protection against peroxides, and superoxide radicals suggests that at least from time to time they may become exposed not only to low oxygen stress but to high oxygen stress as well.


Anaerobic Growth Terminal Electron Acceptor Hypersaline Environment Hypersaline Lake Autotrophic Nitrification 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Antunes A, Tiborda M, Huber R, Moissl C, Nobre MF, da Costa MS (2008) Halorhabdus tiamatea sp. nov., a non-pigmented, extremely halophilic archaeon from a deep-sea, hypersaline anoxic basin of the Red Sea, and emended description of the genus Halorhabdus. Int J Syst Evol Microbiol 58:215–220PubMedCrossRefGoogle Scholar
  2. Antunes A, Alam I, Bajic VB, Stingl U (2011a) Genome sequence of Halorhabdus tiamatea, the first archaeon isolated from a deep-sea anoxic brine lake. J Bacteriol 193:4553–4554PubMedCrossRefGoogle Scholar
  3. Antunes A, Kamanda Ngugi D, Stingl U (2011b) Microbiology of the Red Sea (and other) deep-sea anoxic brine lakes. Environ Microbiol Rep 3:416–433PubMedCrossRefGoogle Scholar
  4. Beard SJ, Hayes PK, Walsby AE (1997) Growth competition between Halobacterium salinarum strain PHH1 and mutants affected in gas vesicle synthesis. Microbiology 143:467–473CrossRefGoogle Scholar
  5. Bibikov SI, Skulachev VP (1989) Mechanisms of phototaxis and aerotaxis in Halobacterium halobium. FEBS Lett 243:303–306CrossRefGoogle Scholar
  6. Bickel-Sandkötter S, Gärtner W, Dane M (1996) Conversion of energy in halobacteria: ATP synthesis and phototaxis. Arch Microbiol 166:1–11PubMedCrossRefGoogle Scholar
  7. Bolhuis H, Palm P, Wende A, Falb M, Rampp M, Rodriguez-Valera F, Pfeiffer F, Oesterhelt D (2006) The genome of the square archaeon Haloquadratum walsbyi: life at the limits of water activity. BMC Genomics 7:169PubMedCrossRefGoogle Scholar
  8. Brown-Peterson NJ, Salin ML (1994) Salt stress in a halophilic bacterium: alterations in oxidative metabolism and oxy-intermediate scavenging systems. Can J Microbiol 40:1057–1063CrossRefGoogle Scholar
  9. Brown-Peterson NJ, Chen H, Salin ML (1994) Enhanced superoxide production by membrane vesicles from Halobacterium halobium in a hyposaline environment. Biochem Biophys Res Commun 205:1736–1740PubMedCrossRefGoogle Scholar
  10. Brown-Peterson NJ, Begonia GB, Salin ML (1995) Alterations in oxidative activity and superoxide dismutase in Halobacterium halobium in response to aerobic respiratory inhibitors. Free Radic Biol Med 18:249–256PubMedCrossRefGoogle Scholar
  11. Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML (2004) Cultivation of Walsby’s square haloarchaeon. FEMS Microbiol Lett 238:469–473PubMedGoogle Scholar
  12. Burns DG, Janssen PH, Itoh T, Kamekura M, Li Z, Jensen G, Rodríguez-Valera F, Bolhuis H, Dyall-Smith ML (2007) Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. Int J Syst Evol Microbiol 57:387–392PubMedCrossRefGoogle Scholar
  13. Cui H-L, Gao X, Li X-Y, Xu X-W, Zhou Y-G, Liu H-C, Zhou P-J (2010) Haloplanus vescus sp. nov., an extremely halophilic archaeon from a marine solar saltern, and emended description of the genus Haloplanus. Int J Syst Evol Microbiol 60:1824–1827PubMedCrossRefGoogle Scholar
  14. DasSarma P, Klebahn G, Klebahn H (2010) Translation of Henrich Klebahn’s ‘Damaging agents of the klippfish – a contribution to the knowledge of the salt-loving organisms’. Saline Syst 6:7PubMedCrossRefGoogle Scholar
  15. Ducharme L, Matheson AT, Yaguchi M, Visentin LP (1972) Utilization of amino acids by Halobacterium cutirubrum in chemically defined medium. Can J Microbiol 18:1349–1351PubMedCrossRefGoogle Scholar
  16. Dundas ID, Halvorson HO (1966) Arginine metabolism in Halobacterium salinarium, an obligately halophilic bacterium. J Bacteriol 91:113–119PubMedGoogle Scholar
  17. Elevi Bardavid R, Mana L, Oren A (2007) Haloplanus natans gen. nov., sp. nov., an extremely halophilic gas-vacuolate archaeon from Dead Sea – Red Sea water mixtures in experimental mesocosms. Int J Syst Evol Microbiol 57:780–783CrossRefGoogle Scholar
  18. Englert C, Horne M, Pfeifer F (1990) Expression of the major gas vesicle protein in the halophilic archaebacterium Haloferax mediterranei is modulated by salt. Mol Gen Genet 222:225–232PubMedCrossRefGoogle Scholar
  19. Englert C, Wanner G, Pfeifer F (1992) Functional analysis of the gas vesicle gene cluster of the halophilic archaeon Haloferax mediterranei defines the vac-region boundary and suggests a regulatory role for the gvpD gene or its product. Mol Microbiol 6:3543–3550PubMedCrossRefGoogle Scholar
  20. Fukumori Y, Fujiwara T, Okada-Takahashi Y, Mukohata Y, Yamanaka T (1985) Purification and properties of a peroxidase from Halobacterium halobium L-33. J Biochem 98:1055–1061PubMedGoogle Scholar
  21. Gonzalez C, Gutierrez C, Ramirez C (1978) Halobacterium vallismortis sp. nov. An amylolytic and carbohydrate-metabolizing extremely halophilic bacterium. Can J Microbiol 24:710–715PubMedCrossRefGoogle Scholar
  22. Hartmann R, Sickinger H-D, Oesterhelt D (1980) Anaerobic growth of halobacteria. Proc Natl Acad Sci U S A 77:3821–3825PubMedCrossRefGoogle Scholar
  23. Hochstein LI (1991) Nitrate reduction in the extremely halophilic bacteria. In: Rodriguez-Valera F (ed) General and applied aspects of halophilic microorganisms. Plenum Press, New York, pp 129–137CrossRefGoogle Scholar
  24. Hochstein LI, Tomlinson GA (1985) Denitrification by extremely halophilic bacteria. FEMS Microbiol Lett 27:329–331PubMedCrossRefGoogle Scholar
  25. Houwink AL (1956) Flagella, gas vacuoles and cell-wall structure in Halobacterium halobium: an electron microscope study. J Gen Microbiol 15:146–150PubMedCrossRefGoogle Scholar
  26. Javor BJ (1984) Growth potential of halophilic bacteria isolated from solar salt environments: carbon sources and salt requirements. Appl Environ Microbiol 48:352–360PubMedGoogle Scholar
  27. Klebahn H (1919) Die Schädlinge des Klippfisches. Mitt Inst Allg Bot Hamburg 4:11–69Google Scholar
  28. Larsen H, Omang S, Steensland H (1967) On the gas vacuoles of the halobacteria. Arch Mikrobiol 59:197–203PubMedCrossRefGoogle Scholar
  29. Levy Y (1980) Seasonal and long range changes in oxygen and hydrogen sulfide concentration in the Dead Sea. Report MG/9/80, Ministry of Energy and Infrastructure, Geological Survey of Israel, JerusalemGoogle Scholar
  30. Lindbeck JC, Goulbourne EA Jr, Johnson MS, Taylor BL (1995) Aerotaxis in Halobacterium salinarium is methylation-dependent. Microbiology 141:2945–2953PubMedCrossRefGoogle Scholar
  31. Long SN, Salin ML (2000) Archaeal promoter-directed expression of the Halobacterium salinarum catalase-peroxidase gene. Extremophiles 4:351–356PubMedCrossRefGoogle Scholar
  32. Mancinelli RL, Hochstein LI (1986) The occurrence of denitrification in extremely halophilic bacteria. FEMS Microbiol Lett 35:55–58PubMedCrossRefGoogle Scholar
  33. May BP, Dennis PP (1987) Superoxide dismutase from the extremely halophilic archaebacterium Halobacterium cutirubrum. J Bacteriol 169:1417–1422PubMedGoogle Scholar
  34. May BP, Tam P, Dennis PP (1989) The expression of the superoxide dismutase gene in Halobacterium halobium and Halobacterium volcanii. Can J Microbiol 35:171–175PubMedCrossRefGoogle Scholar
  35. Monstadt GM, Holldorf AM (1991) Arginine deiminase from Halobacterium salinarium: purification and properties. Biochem J 273:739–746PubMedGoogle Scholar
  36. Montalvo-Rodríguez R, Vreeland RH, Oren A, Kessel M, Betancourt C, López-Garriga J (1998) Halogeometricum borinquense gen. nov., sp. nov., a novel halophilic Archaeon from Puerto Rico. Int J Syst Bacteriol 48:1305–1312PubMedCrossRefGoogle Scholar
  37. Müller JA, DasSarma S (2005) Genomic analysis of anaerobic respiration in the archaeon Halobacterium sp. strain NRC-1: dimethyl sulfoxide and trimethylamine N-oxide as terminal electron acceptors. J Bacteriol 187:1659–1667PubMedCrossRefGoogle Scholar
  38. Mwatha WE, Grant WD (1993) Natronobacterium vacuolata, a haloalkaliphilic archaeon isolated from Lake Magadi, Kenya. Int J Syst Bacteriol 43:401–404CrossRefGoogle Scholar
  39. Oesterhelt D (1982) Anaerobic growth of halobacteria. Methods Enzymol 88:417–420CrossRefGoogle Scholar
  40. Oesterhelt D, Krippahl G (1983) Phototrophic growth of halobacteria and its use for isolation of photosynthetically-deficient mutants. Ann Microbiol 134B:137–150Google Scholar
  41. Offner S, Ziese U, Wanner G, Typke D, Pfeifer F (1998) Structural characteristics of halobacterial gas vesicles. Microbiology 144:1331–1342PubMedCrossRefGoogle Scholar
  42. Oren A (1991) Anaerobic growth of halophilic archaeobacteria by reduction of fumarate. J Gen Microbiol 137:1387–1390CrossRefGoogle Scholar
  43. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348PubMedGoogle Scholar
  44. Oren A (2001) The bioenergetic basis for the decrease in metabolic diversity at increasing salt concentrations: implications for the functioning of salt lake ecosystems. Hydrobiologia 466:61–72CrossRefGoogle Scholar
  45. Oren A (2002) Halophilic microorganisms and their environments. Kluwer Scientific, DordrechtCrossRefGoogle Scholar
  46. Oren A (2006) The order Halobacteriales. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. A handbook on the biology of bacteria: ecophysiology and biochemistry, vol 3. Springer, New York, pp 113–164Google Scholar
  47. Oren A (2011) Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 13:1908–1923PubMedCrossRefGoogle Scholar
  48. Oren A (2012) Taxonomy of Halobacteriaceae: a paradigm for changing concepts in prokaryote systematics. Int J Syst Evol Microbiol 62:263–271PubMedCrossRefGoogle Scholar
  49. Oren A, Litchfield CD (1999) A procedure for the enrichment and isolation of Halobacterium. FEMS Microbiol Lett 173:353–358CrossRefGoogle Scholar
  50. Oren A, Trüper HG (1990) Anaerobic growth of halophilic archaeobacteria by reduction of dimethylsulfoxide and trimethylamine N-oxide. FEMS Microbiol Lett 70:33–36CrossRefGoogle Scholar
  51. Oren A, Ginzburg M, Ginzburg BZ, Hochstein LI, Volcani BE (1990) Haloarcula marismortui (Volcani) sp. nov., nom. rev., an extremely halophilic bacterium from the Dead Sea. Int J Syst Bacteriol 40:209–210PubMedCrossRefGoogle Scholar
  52. Oren A, Priel N, Shapiro O, Siboni N (2006) Buoyancy studies in natural communities of square gas-vacuolate archaea in saltern crystallizer ponds. Saline Syst 2:4PubMedCrossRefGoogle Scholar
  53. Oren A, Ventosa A, Ma Y (2011) Helge Larsen (1922–2005) and his contributions to the study of halophilic microorganisms. In: Ventosa A, Oren A, Ma Y (eds) Halophiles and hypersaline environments: current research and future trends. Springer, Berlin, pp 1–7CrossRefGoogle Scholar
  54. Parkes K, Walsby AE (1981) Ultrastructure of a gas-vacuolate square bacterium. J Gen Microbiol 126:503–506Google Scholar
  55. Petter HFM (1932) Over Roode en Andere Bacteriën van Gezouten Visch. PhD thesis, University of UtrechtGoogle Scholar
  56. Pfeifer F, Krüger K, Röder R, Mayr A, Ziesche S, Offner S (1997) Gas vesicle formation in halophilic Archaea. Arch Microbiol 167:259–268PubMedCrossRefGoogle Scholar
  57. Pfeifer F, Gregor D, Hofacker A, Ploßer P, Zimmermann P (2002) Regulation of gas vesicle formation in halophilic archaea. J Mol Microbiol Biotechnol 4:175–181PubMedGoogle Scholar
  58. Röder R, Pfeifer F (1996) Influence of salt on the transcription of the gas-vesicle gene of Haloferax mediterranei and identification of the endogenous transcriptional activator. Microbiology 142:1715–1723PubMedCrossRefGoogle Scholar
  59. Rodriguez-Valera F, Juez G, Kushner DJ (1983) Halobacterium mediterranei spec. nov., a new carbohydrate-utilizing extreme halophile. Syst Appl Microbiol 4:369–381PubMedCrossRefGoogle Scholar
  60. Rodriguez-Valera F, Ventosa A, Juez G, Imhoff JF (1985) Variation of environmental features and microbial populations with salt concentration in a multi-pond saltern. Microb Ecol 11:107–115PubMedCrossRefGoogle Scholar
  61. Romanenko VI (1981) Square microcolonies in the surface water film of the Saxkoye lake. Mikrobiologiya (USSR) 50:571–574 (in Russian)Google Scholar
  62. Ruepp A, Soppa J (1996) Fermentative arginine degradation in Halobacterium salinarium (formerly Halobacterium halobium): genes, gene products, and transcripts of the arcRACB gene cluster. J Bacteriol 178:4942–4947PubMedGoogle Scholar
  63. Ruepp A, Müller HN, Lottspeich F, Soppa J (1995) Catabolic ornithine transcarbamylase of Halobacterium halobium (salinarium): purification, characterization, sequence determination, and evolution. J Bacteriol 177:1129–1136PubMedGoogle Scholar
  64. Salin ML, Brown-Peterson NJ (1993) Dealing with active oxygen intermediates: a halophilic perspective. Experientia 49:523–529CrossRefGoogle Scholar
  65. Salin ML, Oesterhelt D (1988) Purification of a manganese-containing superoxide dismutase from Halobacterium halobium. Arch Biochem Biophys 260:806–810PubMedCrossRefGoogle Scholar
  66. Shand RF, Betlach MC (1991) Expression of the bop gene cluster of Halobacterium halobium is induced by low oxygen tension and by light. J Bacteriol 173:4692–4699PubMedGoogle Scholar
  67. Shatkay M (1991) Dissolved oxygen in highly saline sodium chloride solutions and in the Dead Sea – measurements of its concentration and isotopic composition. Mar Chem 32:89–99CrossRefGoogle Scholar
  68. Shatkay M, Anati DA, Gat JR (1993) Dissolved oxygen in the Dead Sea – seasonal changes during the holomictic stage. Int J Salt Lake Res 2:93–110CrossRefGoogle Scholar
  69. Sherwood JE, Stagnitti F, Kokkinn MJ, Williams WD (1991) Dissolved oxygen concentrations in hypersaline waters. Limnol Oceanogr 36:235–250CrossRefGoogle Scholar
  70. Sherwood JE, Stagnitti F, Kokkinn MJ, Williams WD (1992) A standard table for predicting equilibrium dissolved oxygen concentrations in salt lakes dominated by sodium chloride. Int J Salt Lake Res 1:1–6CrossRefGoogle Scholar
  71. Stoeckenius W, Wolff EK, Hess B (1988) A rapid population method for action spectra applied to Halobacterium halobium. J Bacteriol 170:2790–2795PubMedGoogle Scholar
  72. Strøm AR, Larsen H (1979) Anaerobic fish spoilage by bacteria. Biochemical changes in herring extracts. J Appl Bacteriol 46:269–277CrossRefGoogle Scholar
  73. Strøm AR, Olafsen JA, Larsen H (1979) Trimethylamine oxide: a terminal electron acceptor in anaerobic respiration of bacteria. J Gen Microbiol 112:315–320PubMedCrossRefGoogle Scholar
  74. Takao M, Kobayashi T, Oikawa A, Yasui A (1989) Tandem arrangement of photolyase and superoxide dismutase genes in Halobacterium halobium. J Bacteriol 171:6323–6329PubMedGoogle Scholar
  75. Tindall BJ, Trüper HG (1986) Ecophysiology of the aerobic halophilic archaebacteria. Syst Appl Microbiol 7:202–212CrossRefGoogle Scholar
  76. Tomlinson GA, Jahnke LL, Hochstein LI (1986) Halobacterium denitrificans sp. nov., an extremely halophilic denitrifying bacterium. Int J Syst Bacteriol 36:66–70PubMedCrossRefGoogle Scholar
  77. van der Wielen PWJJ, Bolhuis H, Borin S, Daffonchio D, Corselli C, Giuliano L, D’Auria G, de Lange GJ, Huebner A, Varnavas SP, Thomson J, Tamburini C, Marty D, McGenity TJ, Timmis KN, BioDeep Scientific Party (2005) The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307:121–123PubMedCrossRefGoogle Scholar
  78. Walsby AE (1980) A square bacterium. Nature 283:69–71CrossRefGoogle Scholar
  79. Warkentin M, Schumann R, Oren A (2009) Community respiration studies in saltern crystallizer ponds. Aquat Microb Ecol 56:255–261CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Plant and Environmental Sciences, The Institute of Life SciencesThe Hebrew University of JerusalemJerusalemIsrael

Personalised recommendations