Abstract
Archaeal microorganisms that grow optimally at Na+ concentrations of 1.7 M, or the equivalent of 10% (w/v) NaCl, and greater are considered to be extreme halophiles. This review encompasses extremely halophilic archaea and their growth characteristics with respect to the correlation between the extent of alkaline pH and elevated temperature optima and the extent of salt tolerance. The focus is on poly-extremophiles, i.e., taxa growing optimally at a Na+ concentration at or above 1.7 M (approximately 10% w/v NaCl); alkaline pH, at or above 8.5; and elevated temperature optima, at or above 50°C. So far, only a very few extreme halophiles that are able to grow optimally under alkaline conditions as well as at elevated temperatures have been isolated. The distribution of extremely halophilic archaea growing optimally at 3.4 M Na+ (approximately 20% w/v NaCl) is bifurcated with respect to pH optima, either they are neutrophilic, with a pHopt of approximately 7, or strongly alkaliphilic, with pHopt at or above 8.5. Amongst these extreme halophiles which have elevated pH optima, only four taxa have an optimum temperature above 50°C: Haloarcula quadrata (52°C), Haloferax elongans (53°C), Haloferax mediterranei (51°C) and Natronolimnobius ‘aegyptiacus’ (55°C).
Similar content being viewed by others
References
Allen MA, Goh F, Leuko S, Echigo A, Mizuki T, Usami R, Kamekura M, Neilan BA, Burns BP (2008) Haloferax elongans sp. nov. and Haloferax mucosum sp. nov., isolated from microbial mats from Hamelin Pool, Shark Bay, Australia. Int J Syst Evol Microbiol 58:798–802
Antunes A, Taborda 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 58:215–220
Bowers KJ, Mesbah NM, Wiegel J (2009a) Biodiversity of poly-extremophilic bacteria: does combining the extremes of high salt, alkaline pH and elevated temperature approach a physico-chemical boundary for life? Saline Syst 5:9 (23 November 2009)
Bowers KJ, Sarmiento BF, Mesbah NM, Wiegel J (2009b) Natronolimnobius ‘aegyptiacus’, a novel poly-extremophilic archaeon isolated from athalassohaline lakes in the Wadi An Natrun, Egypt. Abs SE Branch Annual Meeting Am Soc Microbiol. Savannah, GA
Cavicchioli R (2006) Cold-adapted archaea. Nature Rev Microbiol 4:331–343
da Costa MS, Santos H, Galinski EA (1998) An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Adv Biochem Eng Biotechnol 61:117–153
Duckworth AW, Grant WD, Jones BE, van Steenbergen R (2006) Phylogenetic diversity of soda lake alkaliphiles. FEMS Microbiol Ecol 19:181–191
Feng J, Zhou P, Zhou YG, Liu SJ, Warren-Rhodes K (2005) Halorubrum alkaliphilum sp. nov., a novel haloalkaliphile isolated from a soda lake in Xinjiang, China. Int J Syst Evol Microbiol 55:149–152
Foti MJ, Sorokin DY, Zacharova EE, Pimenov NV, Kuenen JG, Muyzer G (2008) Bacterial diversity and activity along a salinity gradient in soda lakes of the Kulunda Steppe (Altai, Russia). Extremophiles 12:133–145
Ghozlan H, Deif H, Kandil RA, Sabry S (2006) Biodiversity of moderately halophilic bacteria in hypersaline habitats. J Gen Appl Microbiol 52:63–72
Gutiérrez MC, Castillo AM, Kamekura M, Xue Y, Ma Y, Cowan DA, Jones BE, Grant WD, Ventosa A (2007) Halopiger xanaduensis gen. nov., sp. nov., an extremely halophilic archaeon isolated from saline Lake Shangmatala in Inner Mongolia, China. Int J Syst Evol Microbiol 57:1402–1407
Hezayen FF, Rehm BHA, Tindall BJ, Steinbuchel A (2001) Transfer of Natrialba asiatica B1T to Natrialba taiwanensis sp. nov. and description of Natrialba aegyptiaca sp. nov., a novel extremely halophilic, aerobic, non-pigmented member of the Archaea from Egypt that produces extracellular poly(glutamic acid). Int J Syst Evol Microbiol 51:1133–1142
Hezayen FF, Tindall BJ, Steinbuchel A, Rehm BHA (2002) Characterization of a novel halophilic archaeon, Halobiforma haloterrestris gen. nov., sp. nov., and transfer of Natronobacterium nitratireducens to Halobiforma nitratireducens comb. nov. Int J Syst Evol Microbiol 52:2271–2280
Hu L, Pan H, Xue Y, Ventosa A, Cowan DA, Jones BE, Grant WD, Ma Y (2008) Halorubrum luteum sp. nov., isolated from Lake Chagannor, Inner Mongolia, China. Int J Syst Evol Microbiol 58:1705–1708
Ihara K, Watanabe S, Tamura T (1997) Haloarcula argentinensis sp. nov. and Haloarcula mukohataei sp. nov., two new extremely halophilic archaea collected in Argentina. Int J Syst Bacteriol 47:73–77
Kevbrin VV, Romanek CS, Wiegel J (2004) Alkalithermophiles: a double challenge from extreme environments. In: Seckback J (ed) Cellular origins, life in extreme habitats and astrobiology. Kluwer, Dordrecht, The Netherlands, pp 395–412
Krulwich TA, Ito M, Gilmour R, Hicks DB, Guffanti AA (1998) Energetics of alkaliphilic Bacillus species: physiology and molecules. Adv Microb Physiol 40:401–438
Kurr M, Huber R, König H, Jannasch HW, Fricke H, Trincone A, Kristjansson JK, Stetter KO (1991) Methanopyrus kandleri, gen. and sp. nov. represents a novel group of hyperthermophilic methanogens, growing at 110°C. Arch Microbiol 156:239–247
Marteinsson VT, Birrien JL, Reysenbach AL, Vernet M, Marie D, Gambacorta A, Messner P, Sleytr UB, Prieur D (1999) Thermococcus barophilus sp. nov., a new barophilic and hyperthermophilic archaeon isolated under high hydrostatic pressure from a deep-sea hydrothermal vent. Int J Syst Bacteriol 49:351–359
Mesbah NM, Wiegel J (2008) Life at extreme limits: the anaerobic halophilic alkalithermophiles. In: Wiegel J, Maier RJ, Adams MWW (eds) Incredible anaerobes: from physiology to genomics to fuels. Blackwell Pub. on behalf of the New York Academy of Sciences, Boston, pp 44–57
Mesbah NM, Hedrick DB, Peacock AD, Rohde M, Wiegel J (2007a) Natranaerobius thermophilus gen nov., sp. nov., a halophilic, alkalithermophilic bacterium from soda lakes of the Wadi An Natrun, Egypt, and proposal of Natranaerobiaceae fam. nov. and Natranaerobiales ord. nov. Int J Syst Evol Microbiol 57:2507–2512
Mesbah NM, Abou-El-Ela Soad H, Wiegel J (2007b) Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microb Ecol 54:598–617
Mesbah NM, Cook GM, Wiegel J (2009) The halophilic alkalithermophile Natranaerobius thermophilus adapts to multiple environmental extremes using a large repertoire of Na+(K+)/H+ antiporters. Mol Microbiol 74:270–281
Oren A (2002) Halophilic microorganisms and their environments. Kluwer, Dordrecht, the Netherlands
Oren A (2006) Life at high salt conditions. 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 2. Springer, New York, pp 263–282
Oren A, Ventosa A, Gutiérrez MC, Kamekura M (1999) Haloarcula quadrata sp. nov., a square, motile archaeon isolated from a brine pool in Sinai (Egypt). Int J Syst Bacteriol 49:1149–1155
Padan E, Krulwich TA (2000) Sodium stress. In: Storz G, Hengge-Aronis R (eds) Bacterial stress response. ASM Press, Washington, DC, pp 117–130
Paterek JR, Smith PH (1988) Methanohalophilus mahii gen. nov., sp. nov., a methylotrophic halophilic methanogen. Int J Syst Bacteriol 38:122–123
Rees HC, Grant WD, Jones BE, Heaphy S (2004) Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods. Extremophiles 8:63–71
Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst 1:5 (4 Aug 2005)
Roh SW, Nam YD, Chang HW, Sung Y, Kim KH, Oh HM, Bae JW (2007) Halalkalicoccus jeotgali sp. nov., a halophilic archaeon from shrimp jeotgal, a traditional Korean fermented seafood. Int J Syst Evol Microbiol 57:2296–2298
Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D, Santarius U, Klenk HP, Zillig W (1995) Picrophilus gen. nov., fam. nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. Syst Evol Microbiol Int J 24:7050–7059
Slonczewski JL, Fujisawa M, Dopson M, Krulwich TA (2009) Cytoplasmic pH measurement and homeostasis in bacteria and archaea. Adv Micro Physiol 55:1–79
Takei K, Nakamura K, Toki T, Tsunogai U, Miyazaki M, Miyazaki J, Hirayama H, Nakagawa S, Nunoura T, Horikoshi K (2008) Cell proliferation at 122°C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc Nat Acad Sci 105:10949–10954
Tomlinson GA, Jahnke LL, Hochstein LI (1986) Halobacterium denitrificans sp nov., an extremely halophilic denitrifying bacterium. Int J Syst Bacteriol 36:66–70
Torreblanca M, Rodriguez-Valera F, Juez G, Ventosa A, Kamekura M, Kates M (1986) Classification of non-alkaliphilic halobacteria based on numerical taxonomy and polar lipid composition and description of Haloarcula gen nov. and Haloferax gen. nov. Syst Appl Microbiol 8:89–99
Vossenberg JLCM, Driessen AJM, Grant WD, Konnings WN (1999) Lipid membranes from halophilic and alkali-halophilic Archaea have a low H+ and Na+ permeability at high salt concentration. Extremophiles 3:253–257
Waino M, Tindall BJ, Ingvorsen K (2000) Halorhabdus utahensis gen. nov., sp. nov., an aerobic, extremely halophilic member of the Archaea from Great Salt Lake, Utah. Int J Syst Evol Microbiol 50:183–190
Wiegel J (1998) Anaerobic alkalithermophiles, a novel group of extremophiles. Extremophiles 2:257–267
Xu Y, Zhou P, Tian X (1999) Characterization of two novel haloalkaliphilic archaea, Natronorubrum bangense gen. nov., sp. nov. and Natronorubrum tibetense gen. nov., sp. nov. Int J Syst Bacteriol 49:261–266
Xu Y, Wang Z, Xue Y, Zhou P, Ma Y, Ventosa A, Grant WD (2001) Natrialba hulunbeirensis sp. nov. and Natrialba chahannaoensis sp. nov., novel haloalkaliphilic archaea from soda lakes in Inner Mongolia Autonomous Region, China. Int J Syst Evol Microbiol 51:1693–1698
Zhilina TN, Zavarzin GA (1987) Methanohalobium evestigatus, n. gen., n. sp. The extremely halophilic methanogenic Archaebacterium. Dokl Akad Nauk SSSR 293:464–468
Acknowledgments
This work was financially supported by grant MCB 060224 from the National Science Foundation and grant AFOSR 033835-01 from the Air Force Office of Scientific Research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by H. Santos.
Rights and permissions
About this article
Cite this article
Bowers, K.J., Wiegel, J. Temperature and pH optima of extremely halophilic archaea: a mini-review. Extremophiles 15, 119–128 (2011). https://doi.org/10.1007/s00792-010-0347-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-010-0347-y