Life at High Salt and Low Oxygen: How Do the Halobacteriaceae Cope with Low Oxygen Concentrations in Their Environment?
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.
KeywordsAnaerobic Growth Terminal Electron Acceptor Hypersaline Environment Hypersaline Lake Autotrophic Nitrification
- 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
- 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
- Klebahn H (1919) Die Schädlinge des Klippfisches. Mitt Inst Allg Bot Hamburg 4:11–69Google Scholar
- 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
- Oesterhelt D, Krippahl G (1983) Phototrophic growth of halobacteria and its use for isolation of photosynthetically-deficient mutants. Ann Microbiol 134B:137–150Google Scholar
- 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
- Parkes K, Walsby AE (1981) Ultrastructure of a gas-vacuolate square bacterium. J Gen Microbiol 126:503–506Google Scholar
- Petter HFM (1932) Over Roode en Andere Bacteriën van Gezouten Visch. PhD thesis, University of UtrechtGoogle Scholar
- Romanenko VI (1981) Square microcolonies in the surface water film of the Saxkoye lake. Mikrobiologiya (USSR) 50:571–574 (in Russian)Google Scholar
- 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