Isolation and identification of two extremely halophilic archaea from sebkhas in the Algerian Sahara

Sakina Khallef; Roxane Lestini; Hannu Myllykallio; Karim Houali

doi:10.14715/cmb/2018.64.4.14

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Vol. 64 No. 4: Issue 4

Issue Published : April 2, 2018

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Isolation and identification of two extremely halophilic archaea from sebkhas in the Algerian Sahara

https://doi.org/10.14715/cmb/2018.64.4.14

Sakina Khallef

Laboratoire de Bio Ressources Sahariennes. Préservation et valorisation (BRS). Département des Sciences Biologiques, Faculté des Sciences de la Nature et de la Vie, Université Kasdi MERBAH de Ouargla, 30000, Algérie

Roxane Lestini

Laboratoire d'Optique et Biosciences (LOB), Ecole Polytechnique, CNRS UMR7645 - INSERM U696.Université Paris-Saclay, 91 128, Palaiseau Cedex, France

Hannu Myllykallio

Laboratoire d'Optique et Biosciences (LOB), Ecole Polytechnique, CNRS UMR7645 - INSERM U696.Université Paris-Saclay, 91 128, Palaiseau Cedex, France

Karim Houali

Laboratoire de Biochimie Analytiques et Biotehnologies (LABAB), Faculté des Sciences Biologiques et des Sciences Agronomiques. Université Mouloud MAMMERI de Tizi-Ouzou. Algérie

Corresponding Author(s) : Karim Houali

houalitizi@yahoo.fr

Cellular and Molecular Biology, Vol. 64 No. 4: Issue 4
Article Published : March 31, 2018

Abstract

In Algeria, many salt lakes are to be found spread from southern Tunisia up to the Atlas Mountains in northern Algeria. Oum Eraneb and Ain El beida sebkhas (salt lakes), are located in the Algerian Sahara. The aim of this study was to explore the diversity of the halobacteria in this type of habitats. The physicochemical properties of these shallow saline environments were examined and compared with other hypersaline and marine ecosystems. Both sites were relatively alkaline with a pH around 8.57- 8.74 and rich in salt at 13% and 16% (w/v) salinity for Oum Eraneb and Ain El beida, respectively, with dominant ions of sodium and chloride. The microbial approach revealed the presence of two halophilic archaea, strains JCM13561 and A33T in both explored sebkhas. Growth occurred between 10 and 25% (w/v) NaCl and the isolates grow optimally at 20% (w/v) NaCl. The pH range for growth was 6 to 9.5 with an optimum at pH 7.5 for the first strain and 7 to 9.5 with an optimum pH at 8.5-9 for the second strain. On the basis of 16S rRNA gene sequence analysis, strains JCM13561 and A33T were most closely related to Halorubrum litoreum and Natronorubrum bangense (99% and 96% similarity, respectively).

Keywords

Sebkha Hypersaline environments Extremely halophilic Archaea.

Khallef, S., Lestini, R., Myllykallio, H., & Houali, K. (2018). Isolation and identification of two extremely halophilic archaea from sebkhas in the Algerian Sahara. Cellular and Molecular Biology, 64(4), 83–91. https://doi.org/10.14715/cmb/2018.64.4.14

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References

Oren A. Life at High Salt Concentrations. Prokaryotes. 2006; 2:263-282. DOI: 10.1007/0-387-30742-7_9.
Ventosa A. Unusual micro-organisms from unusual habitats. SGM Symposium 66: Procaryotic diversity-mechanisms and significance. Editors N.A. Logan, H.M. Lappin- Scott & P.F. Oyston. Cambridge University Press. 2006; 223-253.
Oren, A. Ecology of halophiles. In: Extremophiles Handbook Horikoshi K, Antranikian G.Bull A, Robb F, Stetter K (eds). Springer, Heidelberg. 2011; 334-361.
Antunes A, Taborda M, Huber R, Moissl C, Nobre MF. and Dacosta MS. 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. 2008 ; 58: 215-220.
Oren A. Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev. 1999; 63: 334-348.
Echigo A, Hino M, Fukushima T, Mizuki T., Kamekura M. and Usami R. Endospores of halophilic bacteria of the family Bacillaceae isolated from non-saline Japanese soil may be transported by Kosa event (Asian dust storm). Saline Systems. 2005; 1:8.
Gibbons N, E. Family V. Halobacteriaceae fam. nov. In Bergey's Manuel of determinative Bacteriology. 1974; eighth ed. 269-273. Edited by R. E. Buchnan & N.E. Gibbons. Baltimore: Williams & Wilkins.
Norton CF. Rediscovering the ecology of halobacteria. In: The ecology of the extremely halophilic archaea. Oren A. FEMS Microbiology Reviews. 1994; 13: 415-440.
Bowers KJ, Mesbah NM, Wiegel. Biodiversity of polyextremophilic bacteria: does combining the extremes of high salt, alkaline pH and elevated temperature approach a physicochemical boundary for life? Saline Syst. 2009a ; 5-9.
Kurlansky M. Salt : A world history. In : Media and condidtions for the Growth of Halophilic and Halotolerant Bacteria and Archaea. Schneegurt MA. 2012; R. H. Vreeland (ed.), Advances in Understanding the Biology of Halophilic Microorganisms. DOI 10.1007/978-94-007-5539-0_2, © Springer
Shahmohammadi HR, Asgarini E, Terat H, Satio T, Ohyama Y, Gekko K, et al. Protective roles of bacterioruberin and intracellular KCl. In: Environmental Microbiology. Mc Genity JT, Gemmell RT, Grant WD, Stann-Lotter H. 2000; 2(3): 234-250.
Post FJ. The microbial ecology of the Great Salt Lake. In: The ecology of the extremely halophilic archaea. Oren A. FEMS Microbiology Reviews. 1994; 13: 415-440.
Hacene H, Fatima R, Nabila C, Boutaiba S, Tej B, Baratti J, Olivier, B. Biodiversity of prokaryotic microflora in el Golea Salt Lake, Algerian Sahara. Journal of Arid Environments. 2004; 58: 273-284.
Kharroub K, Ouesada T, Ferrer R, Fuentes S, Aguilera M, Boulahrouf A, Ramos-Cormenzana A, Monteoliva-Sanchez M. Halorrubrum ezzemoulenense sp. nov., a halophilic archaeon isolated from Ezzemoul sabkha, Algeria. Int J Syst Evol Microbiol. 2006; 56: 1583-1588.
Boutaiba S, Hacene H, Bidle KA, Maupin-Furlow JA. Microbial diversity of the hypersaline Sidi Ameur and Himalatt Salt Lakes of the Algerian Sahara. Arid Environments. 2011; 75 (10): 909-916.
D.G.F. Atlas des zones humides algériennes d'importance internationales. Alger : D.G.F. ed. 2004.
Rodier J, Bazin C, Broutin JP, Chambon P, Champseur H, Rodi L. L'analyse de l'eau : Eaux naturelles, eau résiduaire, eau de mer. 1996 ; Eighth ed. Dunod, Paris.
Shegal SN, Gibbons NE. Effect of metal ions on the growth of Halobacterium cutirubrum. Can. Journ. Microbiol. 1960; 6: 165-169.
Dussault HP. An improved technique for staining red halophilic bacteria. J. Bacteriol. 1955; 70: 484-485 PubMed.
Vreeland R. Taxonomy of Halophilic Bacteria. In: The biology of halophilic bacteria. Vreeland R.H. and Hochstein L.I. (eds), 1993; CRC. pRESS, USA. 105-134.
Takashima T, Hamamoto T, Otazai K, Grant WD, and Horikoshi K. Haloarcula japonica sp.nov. a new triangular halophilic archaebacterium. System. Appl. Microbiol. 1990; 13: 177-181.
Rodriguez MR, Russell H, Vreeland RH, Oren A, Kessel M, Betancourt C, Lopez G. Halogeometricum borinquense gen. nov. sp. nov. a novel halophilic archeon from Puerto Rico. Int. J. Syst. Bacteriol. 1998 ; 48 :1305-1312.
Tomlison GA, Hochstein LI. Halobacterium saccharovorum sp.nov., a carbohydrate- metabolizing, extremely halophilic bacteria. Can. J. Microbiol. 1976; 22:587-591.
Norris JR, Ribbons DW. Methods in Microbiology. 1971; Vol. 6A, Academic Press, 1-52: 0580-9517.
Oren A. Proposed minimal standards for description of new taxa in the order Halobacteriales. Int. J. Syst. Bacteriol. 1997; 47:233-236.
Upasani V, Desai S. Chemical composition of the brines and studies on haloalkaliphilic archabacteria. Arch Microbiol. 1990; 154: 589-593.
Trigui H, Masmoudi S, Brochier-Armanet C, Maalej S, and Dukan S. Characterization of Halorubrum sfaxense sp. nov., a New Halophilic Archaeon isolated from the Solar Saltern of Sfax in Tunisia. Hindawi Publishing Corporation. I. Journal of Microbiology Volume 2011.
Cui HL, Tohty D, Liu HC, Liu SJ, Oren A and Zhou PJ. Natronorubrum sulfidifaciens sp. nov., an extremely haloalkaliphilic archaeon isolated from Aiding salt lake in Xin-Jiang, China. Int J Syst and Evol Microbiol. 2007 ; 57 : 738–740.
Pesenti PT, Sikaroodi M, Gillevet PM, Sanchez-Porro C, Ventosa A, and Litchfield CD.
Halorrubrum californiens sp.nov., an extreme archaeal halophile isolated from a crystalizer pond at a solar salt plant in California, USA. Int J Syst Evol Microbiol. 2008; 58: 2710-2715.
Mancinelli RL, Landheim R, Sanchez-Porro C, Dornmayr-Pfaffenhuemer M, Gruber C, Legat A, an et al. H. Halorubrum chaoviator sp. nov., a haloarchaeon isolated from sea salt in Baja California, Mexico,Western Australia and Naxos, Greece. Int J Syst Evol Microbiol. 2009; 59: 1908–1913.
Gutierréz MC, Castillo AM, Corral P, Kamekura M, Ventosa A. Halorubrum aquaticum sp.nov., an archaeon isolated from hypersaline lakes. Int J Syst Evol Microbiol. 2011; 61: 1144-1148.
Yim KJ, Cha IT , Lee HW , Song HS, Kim KN , Lee SJ, an et al. Halorubrum halophilum sp. nov., an extremely halophilic archaeon isolated from a salt- from a salt-fermented seafood. Antonie van Leeuwenhoek. 2014; 105: 603–612.
Xu Y, Zhou P, and Tian X. Characterization of two novel haloalkaliphilic archaea Natronorubrurn bangense gen. nov., sp. nov. and Natronorubrurn tibetense gen. nov., sp. nov. Int J Syst Bacterio. 1999 ; 49: 26 1-266.
Gutierréz MC, Castillo AM, Corral P, Minegishi H. and Ventosa A. Natronorubrum sediminis sp. nov., an archaeon isolated from a saline lake. Int J Syst and Evol Microbiology. 2010; 60: 1802–1806.
Rodriguez-Valera F. Introduction to saline environments. In: The Biology of Halophilic Bacteria. Vreeland R.H. Hochstein L.I. (Eds.). 1993; Boca Raton, CRC Press.
Rodriguez-Valera F. Characteristics and microbial ecology of hypersaline environments. In Halophilic Bacteria. 1988; vol. 1, pp 3-30. Edited by F. Rodriguez-Valera. Boca Raton, FL: CRC Press.
Litchfield C. Survival strategies for microorganisms in hypersaline environments and their relevance to life on Mars. Meteorit planet. Sci. 1998; 33: 813-819.
McGenity, T. J. & Grant, W. D. Transfer of Halobacterium saccharovorum, Halobacterium sodomense, Halobacterium trapanicum NRC 34021 and Halobacterium lacusprofundi to the genus Halorubrum gen. nov., as Halorubrum saccharovorum comb. nov., Halorubrum sodomense comb. nov., Halorubrum trapanicum comb. nov., and Halorubrum lacusprofundi comb. nov. Syst Appl Microbiol. 1995; 18: 237–243.
Mesbah N, Wiegel J. Life under Multiple Extreme Conditions: Diversity and Physiology of the Halophilik Alkalithermophiles. AEM. 2012; vol. 28: 4047-4082.
Tortora GJ, Funke BR, Case CL. Introduction í la microbiologie. Ed. De Renouveau pédagogique Inc. 2003: 157-355.
Perry JJ, Staley SL. Microbiologie « Cours et questions de révision ». 2004 ; Ed. Dunod, 379-403.

References

Oren A. Life at High Salt Concentrations. Prokaryotes. 2006; 2:263-282. DOI: 10.1007/0-387-30742-7_9.

Ventosa A. Unusual micro-organisms from unusual habitats. SGM Symposium 66: Procaryotic diversity-mechanisms and significance. Editors N.A. Logan, H.M. Lappin- Scott & P.F. Oyston. Cambridge University Press. 2006; 223-253.

Oren, A. Ecology of halophiles. In: Extremophiles Handbook Horikoshi K, Antranikian G.Bull A, Robb F, Stetter K (eds). Springer, Heidelberg. 2011; 334-361.

Antunes A, Taborda M, Huber R, Moissl C, Nobre MF. and Dacosta MS. 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. 2008 ; 58: 215-220.

Oren A. Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev. 1999; 63: 334-348.

Echigo A, Hino M, Fukushima T, Mizuki T., Kamekura M. and Usami R. Endospores of halophilic bacteria of the family Bacillaceae isolated from non-saline Japanese soil may be transported by Kosa event (Asian dust storm). Saline Systems. 2005; 1:8.

Gibbons N, E. Family V. Halobacteriaceae fam. nov. In Bergey's Manuel of determinative Bacteriology. 1974; eighth ed. 269-273. Edited by R. E. Buchnan & N.E. Gibbons. Baltimore: Williams & Wilkins.

Norton CF. Rediscovering the ecology of halobacteria. In: The ecology of the extremely halophilic archaea. Oren A. FEMS Microbiology Reviews. 1994; 13: 415-440.

Bowers KJ, Mesbah NM, Wiegel. Biodiversity of polyextremophilic bacteria: does combining the extremes of high salt, alkaline pH and elevated temperature approach a physicochemical boundary for life? Saline Syst. 2009a ; 5-9.

Kurlansky M. Salt : A world history. In : Media and condidtions for the Growth of Halophilic and Halotolerant Bacteria and Archaea. Schneegurt MA. 2012; R. H. Vreeland (ed.), Advances in Understanding the Biology of Halophilic Microorganisms. DOI 10.1007/978-94-007-5539-0_2, © Springer

Shahmohammadi HR, Asgarini E, Terat H, Satio T, Ohyama Y, Gekko K, et al. Protective roles of bacterioruberin and intracellular KCl. In: Environmental Microbiology. Mc Genity JT, Gemmell RT, Grant WD, Stann-Lotter H. 2000; 2(3): 234-250.

Post FJ. The microbial ecology of the Great Salt Lake. In: The ecology of the extremely halophilic archaea. Oren A. FEMS Microbiology Reviews. 1994; 13: 415-440.

Hacene H, Fatima R, Nabila C, Boutaiba S, Tej B, Baratti J, Olivier, B. Biodiversity of prokaryotic microflora in el Golea Salt Lake, Algerian Sahara. Journal of Arid Environments. 2004; 58: 273-284.

Kharroub K, Ouesada T, Ferrer R, Fuentes S, Aguilera M, Boulahrouf A, Ramos-Cormenzana A, Monteoliva-Sanchez M. Halorrubrum ezzemoulenense sp. nov., a halophilic archaeon isolated from Ezzemoul sabkha, Algeria. Int J Syst Evol Microbiol. 2006; 56: 1583-1588.

Boutaiba S, Hacene H, Bidle KA, Maupin-Furlow JA. Microbial diversity of the hypersaline Sidi Ameur and Himalatt Salt Lakes of the Algerian Sahara. Arid Environments. 2011; 75 (10): 909-916.

D.G.F. Atlas des zones humides algériennes d'importance internationales. Alger : D.G.F. ed. 2004.

Rodier J, Bazin C, Broutin JP, Chambon P, Champseur H, Rodi L. L'analyse de l'eau : Eaux naturelles, eau résiduaire, eau de mer. 1996 ; Eighth ed. Dunod, Paris.

Shegal SN, Gibbons NE. Effect of metal ions on the growth of Halobacterium cutirubrum. Can. Journ. Microbiol. 1960; 6: 165-169.

Dussault HP. An improved technique for staining red halophilic bacteria. J. Bacteriol. 1955; 70: 484-485 PubMed.

Vreeland R. Taxonomy of Halophilic Bacteria. In: The biology of halophilic bacteria. Vreeland R.H. and Hochstein L.I. (eds), 1993; CRC. pRESS, USA. 105-134.

Takashima T, Hamamoto T, Otazai K, Grant WD, and Horikoshi K. Haloarcula japonica sp.nov. a new triangular halophilic archaebacterium. System. Appl. Microbiol. 1990; 13: 177-181.

Rodriguez MR, Russell H, Vreeland RH, Oren A, Kessel M, Betancourt C, Lopez G. Halogeometricum borinquense gen. nov. sp. nov. a novel halophilic archeon from Puerto Rico. Int. J. Syst. Bacteriol. 1998 ; 48 :1305-1312.

Tomlison GA, Hochstein LI. Halobacterium saccharovorum sp.nov., a carbohydrate- metabolizing, extremely halophilic bacteria. Can. J. Microbiol. 1976; 22:587-591.

Norris JR, Ribbons DW. Methods in Microbiology. 1971; Vol. 6A, Academic Press, 1-52: 0580-9517.

Oren A. Proposed minimal standards for description of new taxa in the order Halobacteriales. Int. J. Syst. Bacteriol. 1997; 47:233-236.

Upasani V, Desai S. Chemical composition of the brines and studies on haloalkaliphilic archabacteria. Arch Microbiol. 1990; 154: 589-593.

Trigui H, Masmoudi S, Brochier-Armanet C, Maalej S, and Dukan S. Characterization of Halorubrum sfaxense sp. nov., a New Halophilic Archaeon isolated from the Solar Saltern of Sfax in Tunisia. Hindawi Publishing Corporation. I. Journal of Microbiology Volume 2011.

Cui HL, Tohty D, Liu HC, Liu SJ, Oren A and Zhou PJ. Natronorubrum sulfidifaciens sp. nov., an extremely haloalkaliphilic archaeon isolated from Aiding salt lake in Xin-Jiang, China. Int J Syst and Evol Microbiol. 2007 ; 57 : 738–740.

Pesenti PT, Sikaroodi M, Gillevet PM, Sanchez-Porro C, Ventosa A, and Litchfield CD.

Halorrubrum californiens sp.nov., an extreme archaeal halophile isolated from a crystalizer pond at a solar salt plant in California, USA. Int J Syst Evol Microbiol. 2008; 58: 2710-2715.

Mancinelli RL, Landheim R, Sanchez-Porro C, Dornmayr-Pfaffenhuemer M, Gruber C, Legat A, an et al. H. Halorubrum chaoviator sp. nov., a haloarchaeon isolated from sea salt in Baja California, Mexico,Western Australia and Naxos, Greece. Int J Syst Evol Microbiol. 2009; 59: 1908–1913.

Gutierréz MC, Castillo AM, Corral P, Kamekura M, Ventosa A. Halorubrum aquaticum sp.nov., an archaeon isolated from hypersaline lakes. Int J Syst Evol Microbiol. 2011; 61: 1144-1148.

Yim KJ, Cha IT , Lee HW , Song HS, Kim KN , Lee SJ, an et al. Halorubrum halophilum sp. nov., an extremely halophilic archaeon isolated from a salt- from a salt-fermented seafood. Antonie van Leeuwenhoek. 2014; 105: 603–612.

Xu Y, Zhou P, and Tian X. Characterization of two novel haloalkaliphilic archaea Natronorubrurn bangense gen. nov., sp. nov. and Natronorubrurn tibetense gen. nov., sp. nov. Int J Syst Bacterio. 1999 ; 49: 26 1-266.

Gutierréz MC, Castillo AM, Corral P, Minegishi H. and Ventosa A. Natronorubrum sediminis sp. nov., an archaeon isolated from a saline lake. Int J Syst and Evol Microbiology. 2010; 60: 1802–1806.

Rodriguez-Valera F. Introduction to saline environments. In: The Biology of Halophilic Bacteria. Vreeland R.H. Hochstein L.I. (Eds.). 1993; Boca Raton, CRC Press.

Rodriguez-Valera F. Characteristics and microbial ecology of hypersaline environments. In Halophilic Bacteria. 1988; vol. 1, pp 3-30. Edited by F. Rodriguez-Valera. Boca Raton, FL: CRC Press.

Litchfield C. Survival strategies for microorganisms in hypersaline environments and their relevance to life on Mars. Meteorit planet. Sci. 1998; 33: 813-819.

McGenity, T. J. & Grant, W. D. Transfer of Halobacterium saccharovorum, Halobacterium sodomense, Halobacterium trapanicum NRC 34021 and Halobacterium lacusprofundi to the genus Halorubrum gen. nov., as Halorubrum saccharovorum comb. nov., Halorubrum sodomense comb. nov., Halorubrum trapanicum comb. nov., and Halorubrum lacusprofundi comb. nov. Syst Appl Microbiol. 1995; 18: 237–243.

Mesbah N, Wiegel J. Life under Multiple Extreme Conditions: Diversity and Physiology of the Halophilik Alkalithermophiles. AEM. 2012; vol. 28: 4047-4082.

Tortora GJ, Funke BR, Case CL. Introduction í la microbiologie. Ed. De Renouveau pédagogique Inc. 2003: 157-355.

Perry JJ, Staley SL. Microbiologie « Cours et questions de révision ». 2004 ; Ed. Dunod, 379-403.

Author Biographies

Sakina Khallef, Laboratoire de Bio Ressources Sahariennes. Préservation et valorisation (BRS). Département des Sciences Biologiques, Faculté des Sciences de la Nature et de la Vie, Université Kasdi MERBAH de Ouargla, 30000, Algérie

Département des Sciences Biologiques, Faculté des Sciences de la Nature et de la Vie

Roxane Lestini, Laboratoire d'Optique et Biosciences (LOB), Ecole Polytechnique, CNRS UMR7645 - INSERM U696.Université Paris-Saclay, 91 128, Palaiseau Cedex, France

Ecole Polytechnique, CNRS UMR7645

Hannu Myllykallio, Laboratoire d'Optique et Biosciences (LOB), Ecole Polytechnique, CNRS UMR7645 - INSERM U696.Université Paris-Saclay, 91 128, Palaiseau Cedex, France

Ecole Polytechnique, CNRS UMR7645

Karim Houali, Laboratoire de Biochimie Analytiques et Biotehnologies (LABAB), Faculté des Sciences Biologiques et des Sciences Agronomiques. Université Mouloud MAMMERI de Tizi-Ouzou. Algérie

Department of biochemistry and microbiology