Two Centuries of Microbiological Research in the Wadi Natrun, Egypt: A Model System for the Study of the Ecology, Physiology, and Taxonomy of Haloalkaliphilic Microorganisms

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


The alkaline hypersaline lakes of the Wadi Natrun (most sources use the name “Wadi Natrun”; others prefer “Wadi An Natrun.”), Egypt, recently became famous following the description of the haloalkalithermophiles (order Natranaerobiales) discovered by Juergen Wiegel and his colleagues. However, it is seldom realized how many important discoveries in the past were based on the study of the Wadi Natrun and its microorganisms. The red coloration of the brines by “a vegetal-animal substance” was mentioned in 1799 by General Antoine Andréossy of Napoleon Bonaparte’s army. Studies published by Sickenberger (Chemiker-Zeitung, 16:1645–1646 and 16:1691, 1892) and Schweinfurth and Lewin (1899) presented state-of-the-art information on biogeochemical processes in the lakes, including sulfate reduction, other anaerobic degradation processes (including the formation of trimethylamine, a process understood only much later), anoxygenic photosynthesis, and the nature of the pigments of the microbial communities. Studies in the 1950s on the nature of the red pigmentation of the lakes by Holger Jannasch and on the link between bacterial sulfate reduction and alkalinity by Yousef Abd-el-Malek in the 1960s remain relevant today. Halorhodospira abdelmalekii (basonym Ectothiorhodospira abdelmalekii) was named to honor Abd-el-Malek’s contributions. Microbiological exploration of the Wadi Natrun resumed in the mid-1970s by Hans Trüper, Johannes Imhoff, and others. Studies of two organisms isolated from the site led to some of the most exciting discoveries in microbiology in the past decades: Natronomonas pharaonis became the model for the study of haloalkaliphilic Archaea and for research on halorhodopsin and sensory rhodopsins; the compatible solutes glycine betaine and ectoine, the latter of which has found interesting biotechnological applications, were first detected in Halorhodospira halochloris.


Glycine Betaine Soda Lake Osmotic Solute Bacterial Sulfate Reduction Desulfovibrio Desulfuricans 
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.



I thank Michael W. Adams, Robert J. Maier, and William B. Whitman (University of Georgia, Athens) for inviting me to participate in the symposium on “Extremophiles: Key to Bioenergy,” September 19–20, 2011, organized in honor of Juergen Wiegel, and to Juergen Wiegel for contributing the photographs of Fig. 6 and for many valuable comments.


  1. Abd-el-Malek Y, Risk SG (1963) Bacterial sulphate reduction and the development of alkalinity. III. Experiments under natural conditions in the Wadi Natrun. J Appl Bacteriol 26:20–26CrossRefGoogle Scholar
  2. Andéossy A (1800) Mémoire sur le lac Menzaleh, d’après la reconnaissance faite en vendémiaire an VII [sept. et oct. 1799]; par le général Andréossy. Mémoire sur la vallée des lacs de Natroun et celle du fleuve sans eau, d’après la reconnaissance faite les 4, 5, 6, 7 et 8 pluviôse an VII [23, 24, 25, 26 et 27 janvier 1799]; par le général Andréossy. De l’imprimerie impériale, Paris, 1809 (German translation used in the preparation of this chapter: Des Divisionsgenerales Andreossy’s Untersuchungen über das Thal der Natronsseen, und über den See Möris. Leipzig und Gera, bei Wilhelm Heinsius, 1801)Google Scholar
  3. Baas Becking LGM (1934) Geobiologie of Inleiding tot de Milieukunde. W.P. van Stockum & Zoon, Den HaagGoogle Scholar
  4. Bowers KJ, Wiegel J (2011) Temperature and pH optima of extremely halophilic Archaea. A minireview. Extremophiles 15:119–128PubMedCrossRefGoogle Scholar
  5. Bowers KJ, Mesbah NM, Wiegel J (2009) 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 5:9PubMedCrossRefGoogle Scholar
  6. Falb F, Pfeiffer F, Palm P, Rodewald K, Hickmann V, Tittor J, Oesterhelt D (2005) Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res 15:1336–1343PubMedCrossRefGoogle Scholar
  7. Fritze D (1996) Bacillus haloalkaliphilus sp. nov. Int J Syst Bacteriol 46:98–101CrossRefGoogle Scholar
  8. Galinski EA, Trüper HG (1982) Betaine, a compatible solute in the extremely halophilic phototrophic bacterium Ectothiorhodospira halochloris. FEMS Microbiol Lett 13:357–360CrossRefGoogle Scholar
  9. Galinski EA, Pfeiffer H-P, Trüper HG (1985) 1,4,5,6-Tetrahydro-2-methyl-4-pyrimidinecarboxylic acid. A novel cyclic amino acid from halophilic phototrophic bacteria of the genus Ectothiorhodospira. Eur J Biochem 149:135–139PubMedCrossRefGoogle Scholar
  10. Gorlenko VM, Bryantseva IA, Rabold S, Tourova TP, Rubtsova D, Smirnova E, Thiel V, Imhoff JF (2009) Ectothiorhodospira variabilis sp. nov., an alkaliphilic and halophilic purple sulfur bacterium from soda lakes. Int J Syst Evol Microbiol 59:658–664PubMedCrossRefGoogle Scholar
  11. Hirayama J, Imamoto Y, Shichida Y, Kamo N, Tomioka H, Yoshizawa T (1992) Photocycle of phoborhodopsin from haloalkaliphilic bacterium (Natronobacterium pharaonis) studied by low-temperature spectrophotometry. Biochemistry 31:2093–2098PubMedCrossRefGoogle Scholar
  12. Imhoff JH, Süling J (1996) The phylogenetic relationship among Ectothiorhodospiraceae: a reevaluation of their taxonomy on the basis of 16S rDNA analyses. Arch Microbiol 165:106–113PubMedCrossRefGoogle Scholar
  13. Imhoff JH, Trüper HG (1977) Ectothiorhodospira halochloris sp. nov., a new extremely halophilic phototrophic bacterium containing bacteriochlorophyll b. Arch Microbiol 114:115–121CrossRefGoogle Scholar
  14. Imhoff JH, Trüper HG (1981) Ectothiorhodospira abdelmalekii sp. nov., a new halophilic and alkaliphilic phototrophic bacterium. Zbl Bakt Hyg I Abt Orig C 2:228–234Google Scholar
  15. Imhoff JF, Hashwa F, Trüper HG (1978) Isolation of extremely halophilic phototrophic bacteria from the alkaline Wadi Natrun, Egypt. Arch Hydrobiol 84:381–388Google Scholar
  16. Imhoff JF, Sahl HG, Soliman GSH, Trüper HG (1979) The Wadi Natrun: chemical composition and microbial mass developments in alkaline brines of eutrophic desert lakes. Geomicrobiol J 1:219–234CrossRefGoogle Scholar
  17. Jannasch HW (1957) Die bakterielle Rotfärbung der Salzseen des Wadi Natrun (Ägypten). Arch Hydrobiol 53:425–433Google Scholar
  18. Javor B (1989) Hypersaline environments. Microbiology and biogeochemistry. Springer, BerlinCrossRefGoogle Scholar
  19. Jeon CO, Lim JM, Lee JM, Xu LH, Jiang CL, Kim CJ (2005) Reclassification of Bacillus haloalkaliphilus Fritze 1996 as Alkalibacillus haloalkaliphilus gen. nov., comb. nov. and the description of Alkalibacillus salilacus sp. nov., a novel halophilic bacterium isolated from a salt lake in China. Int J Syst Evol Microbiol 55:1891–1896PubMedCrossRefGoogle Scholar
  20. Kulcsár A, Groma GI, Lanyi JK, Váró G (2000) Characterization of the proton-transporting photocycle of pharaonis halorhodopsin. Biophys J 79:2705–2713PubMedCrossRefGoogle Scholar
  21. Lanyi JK, Duschl A, Hatfield GW, Oesterhelt D (1990) The primary structure of a halorhodopsin from Natronobacterium pharaonis. J Biol Chem 265:1253–1260PubMedGoogle Scholar
  22. Mesbah NM, Wiegel J (2005) Halophilic thermophiles: a novel group of extremophiles. In: Satyanarayana T, Johri BN (eds) Microbial diversity: current perspectives and potential applications. I.K. Publishing House, New Delhi, pp 91–118Google Scholar
  23. Mesbah NM, Wiegel J (2008) Life at extreme limits. The anaerobic halophilic alkalithermophiles. Ann N Y Acad Sci 1125:44–57PubMedCrossRefGoogle Scholar
  24. Mesbah NM, Wiegel J (2009) Natronovirga wadinatrunensis gen. nov., sp. nov. and Natranaerobius trueperi sp. nov., halophilic, alkalithermophilic micro-organisms from soda lakes of the Wadi An Natrun, Egypt. Int J Syst Evol Microbiol 59:2042–2048PubMedCrossRefGoogle Scholar
  25. Mesbah NM, Wiegel J (2011) Halophiles exposed concomitantly to multiple stressors: adaptive mechanisms of halophilic alkalithermophiles. In: Ventosa A, Oren A, Ma Y (eds) Halophiles and halophilic environments: current research and future trends. Springer, Berlin, pp 249–274CrossRefGoogle Scholar
  26. Mesbah NM, Abou-El-Ela SH, Wiegel J (2007a) Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microb Ecol 54:598–617PubMedCrossRefGoogle Scholar
  27. Mesbah NM, Hedrick DB, Peacock AD, Rohde M, Wiegel J (2007b) 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 57:2507–2512PubMedCrossRefGoogle Scholar
  28. Oren A (1990) Formation and breakdown of glycine betaine and trimethylamine in hypersaline environments. Antonie van Leeuwenhoek 58:291–298PubMedCrossRefGoogle Scholar
  29. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348PubMedGoogle Scholar
  30. Oren A (2002) Halophilic microorganisms and their environments. Kluwer Scientific, DordrechtCrossRefGoogle Scholar
  31. Oren A (2006) Life at high salt concentrations. 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 263–282Google Scholar
  32. Oren A (2010) Industrial and environmental applications of halophilic microorganisms. Environ Technol 31:825–834PubMedCrossRefGoogle Scholar
  33. Oren A. (2011a) Two centuries of microbiological studies in the Wadi Natrun, Egypt: a model system for the study of the ecology, physiology, and taxonomy of haloalkaliphilic microorganisms. In: Extremophiles. Key to bioenergy? A symposium in Honor of Distinguished Research Professor Juergen Wiegel. Book of Abstracts. The Georgia Center, University of Georgia, Athens, GA, p 16Google Scholar
  34. Oren A (2011b) Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 13:1908–1923PubMedCrossRefGoogle Scholar
  35. 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
  36. Pliny (1963) Natural history, vol VIII (trans: Jones WHS). William Heinemann/Harvard University Press, London/Cambridge, MAGoogle Scholar
  37. Schweinfurth G, Lewin L (1898) Beiträge zur Topographie und Geochemie des ägyptischen Natron-Thals. Zeitschr Ges Erdk 33:1–25Google Scholar
  38. Sickenberger E (1892) Briefe aus Egypten. I. Wady Atrun. Das Natronthal. Chemiker-Zeitung 16:1645–1646 and 16:1691Google Scholar
  39. Soliman GSH, Trüper HG (1982) Halobacterium pharaonis sp. nov., a new, extremely haloalkaliphilic archaebacterium with low magnesium requirement. Zbl Bakt Hyg I Abt Orig C 3:318–329Google Scholar
  40. Sorokin DY, Tourova TP, Lysenko AM, Mityushina LL, Kuenen JG (2002) Thioalkalivibrio thiocyanoxidans sp. nov. and Thioalkalivibrio paradoxus sp. nov., novel alkaliphilic, obligately autotrophic, sulfur-oxidizing bacteria capable of growth on thiocyanate, from soda lakes. Int J Syst Evol Microbiol 52:657–664PubMedGoogle Scholar
  41. Sorokin DY, Tourova TP, Sjollema KA, Kuenen JG (2003) Thioalkalivibrio nitratireducens sp. nov., a nitrate-reducing member of the autotrophic denitrifying consortium from a soda lake. Int J Syst Evol Microbiol 53:1779–1783PubMedCrossRefGoogle Scholar
  42. Sorokin DY, Tourova TP, Antipov AN, Muyzer G, Kuenen JG (2004) Anaerobic growth of the haloalkaliphilic denitrifying sulfur-oxidizing bacterium Thialkalivibrio thiocyanodenitrificans sp. nov. with thiocyanate. Microbiol UK 150:2435–2442CrossRefGoogle Scholar
  43. Sorokin DY, Tourova TP, Henstra AM, Stams AJM, Galinski EA, Muyzer G (2008a) Sulfidogenesis under extremely haloalkaline conditions by Desulfonatronospira thiodismutans gen. nov., sp. nov., and Desulfonatronospira delicata sp. nov. – a novel lineage of Deltaproteobacteria from hypersaline soda lakes. Microbiology (UK) 154:1444–1453Google Scholar
  44. Sorokin DY, Tourova TP, Muyzer G, Kuenen JG (2008b) Thiohalospira halophila gen. nov., sp. nov. and Thiohalospira alkaliphila sp. nov., novel obligately chemolithoautotrophic, halophilic, sulfur-oxidizing gammaproteobacteria from hypersaline habitats. Int J Syst Evol Microbiol 58:1685–1692PubMedCrossRefGoogle Scholar
  45. Sorokin ID, Zadorina EV, Kravchenko IK, Boulygina IS, Tourova TP, Sorokin D (2008c) Natronobacillus azotifigens gen. nov., sp. nov., an anaerobic diazotrophic haloalkaliphile from soda-rich environments. Extremophiles 12:819–827PubMedCrossRefGoogle Scholar
  46. Stocker O (1927) Das Wadi Natrun. Vegetationsbilder 18. Reihe 1. Gustav Fischer Verlag, JenaGoogle Scholar
  47. Strabo (1967) The geography of Strabo (trans: Jones WHS). William Heinemann/Harvard University Press, London/Cambridge, MAGoogle Scholar
  48. Taher AG (1999) Inland salt lakes of Wadi El Natrun depression, Egypt. Int J Salt Lake Res 8:149–169Google Scholar
  49. Teodoresco EC (1905) Organisation et développement du Dunaliella, nouveau genre de Volvocacée-Polyblépharidée. Bot Centralbl 18:215–232Google Scholar
  50. Tomioka H, Sasabe H (1995) Isolation and photochemically active archaebacterial photoreceptor, pharaonis phoborhodopsin from Natronobacterium pharaonis. Biochim Biophys Acta 1234:261–267PubMedCrossRefGoogle Scholar
  51. Weisser J, Trüper HG (1985) Osmoregulation in a new haloalkalophilic bacillus from the Wadi Natrun (Egypt). Syst Appl Microbiol 6:7–11CrossRefGoogle Scholar
  52. Wiegel J (2011) Anaerobic alkaliphiles and alkaliphilic polyextremophiles. In: Horikoshi K (ed) Handbook of extremophiles. Springer, Tokyo, pp 81–98CrossRefGoogle Scholar
  53. Zhao B, Mesbah NM, Dalin E, Goodwin L, Nolan M, Pitluck S, Chertkov O, Brettin TS, Han J, Larimer FW, Land ML, Hauser L, Kyrpides N, Wiegel J (2011) Complete genome sequence of the anaerobic, halophilic alkalithermophilic Natranaerobius thermophilus. J Bacteriol 193:4023–4024PubMedCrossRefGoogle 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