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Enzymes from Halophilic Archaea: Open Questions

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Halophiles and Hypersaline Environments

Abstract

During the past few decades, the microbial communities inhabiting extreme environments have become a focus on scientific interest owing to the unique properties of the biocatalysts they produce (extremozymes). These extremozymes can cope with industrial process conditions (high temperatures, high salt concentrations, low water availability, etc.) due to their extreme stability under the mentioned parameters. For this reason, the extremozymes are in demand for large-scale production in several chemical industries, biotransformation and in the field of bioremediation. In that context, halophilic Archaea are a valuable source of novel enzymes for biotechnology. Their peculiar physiology involving extreme adaptation to the salty environments have led to the development of applied interests in haloarchaeal enzymes, mainly in those processes carried out in non-aqueous media. In this chapter, we present and discuss the recent knowledge on halophilic enzymes from haloarchaea and some of their biotechnological applications.

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References

  • Banat IM, Makkar RS, Cameotra SS (2000) Potential commercial applications of microbial surfactants. Appl Microbiol Biotechnol 53:495–508

    Article  PubMed  CAS  Google Scholar 

  • Ben-Mahrez K, Thierry D, Sorokine I, Danna-Muller A, Kohiyama M (1988) Detection of circulating antibodies against c-myc protein in cancer patient sera. Br J Cancer 57:529–534

    Article  PubMed  CAS  Google Scholar 

  • Bini E (2010) Archaeal transformation of metals in the environment. FEMS Microbiol Ecol 73:1–16

    PubMed  CAS  Google Scholar 

  • Bonete MJ, Camacho M, Martínez-Espinosa RM, Esclapez J, Bautista V, Pire C, Zafrilla B, Díaz S, Pérez-Pomares F, Llorca F (2007) In the light of the haloarchaea metabolism. In: Méndez-Vilas A (ed) Communicating current research and educational topics and trends in applied microbiology. Formatex, Badajoz, pp 170–183

    Google Scholar 

  • Bonete MJ, Martínez-Espinosa RM, Pire C, Zafrilla B, Richardson DJ (2008) Nitrogen metabolism in haloarchaea. Saline Systems 4:9

    Article  PubMed  Google Scholar 

  • Boutaiba S, Bhatnagar T, Hacene H, Mitchell DA, Baratti JC (2006) Preliminary characterization of a lipolytic activity from an extremely halophilic archaeon, Natronococcus sp. J Mol Catal B Enzym 41:21–26

    Article  CAS  Google Scholar 

  • Britton KL, Baker PJ, Ficher M, Ruzheinnikov S, Gilmour DJ, Bonete MJ, Ferrer J, Pire C, Esclapez J, Rice DW (2006) Analysis of protein solvent interactions in glucose dehydrogenase from the extreme halophile Haloferax mediterranei. Proc Natl Acad Sci USA 103:4846–4851

    Article  PubMed  CAS  Google Scholar 

  • Cabello P, Roldán MD, Moreno-Vivián C (2004) Nitrate reduction and the nitrogen cycle in archaea. Microbiology 150:3527–3546

    Article  PubMed  CAS  Google Scholar 

  • Calo P, de Miguel T, Sieiro C, Velazquez JB, Villa TG (1995) Ketocarotenoids in halobacteria: 3-hydroxy-echinenone and trans-astaxanthin. J Appl Microbiol 79:282–285

    Article  CAS  Google Scholar 

  • Cao Y, Liao L, Xu XW, Oren A, Wu M (2008a) Aldehyde dehydrogenase of the aloalkaliphilic archaeon Natronomonas pharaonis and its function in ethanol metabolism. Extremophiles 12:849–854

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Liao L, Xu XW, Oren A, Wang C, Zhu XF, Wu M (2008b) Characterization of alcohol dehydrogenase from the haloalkaliphilic archaeon Natronomonas pharaonis. Extremophiles 12:471–476

    Article  PubMed  CAS  Google Scholar 

  • D’Souza SE, Altekar W, D’Souza SF (1997) Immobilization of Haloferax mediterranei aldolase by cross-linking in a proteinic matrix: stability and halophilic characteristics. World J Microbiol Biotechnol 13:561–564

    Article  Google Scholar 

  • De Castro RE, Ruiz DM, Giménez MI, Silveyra MX, Paggi RA, Maupin-Furlow JA (2008) Gene cloning and heterologous synthesis of a haloalkaliphilic extracellular protease of Natrialba magadi (Nep). Extremophiles 12:677–687

    Article  PubMed  Google Scholar 

  • Dinçkaya E, Akyilmaz E, Sezgintürk MK, Ertaş FN (2010) Sensitive nitrate determination in water and meat samples by amperometric biosensor. Prep Biochem Biotechnol 40:119–128

    Article  PubMed  Google Scholar 

  • Ding JY, Lai MC (2010) The biotechnological potential of the extreme halophilic archaea Haloterrigena sp. H13 in xenobiotic metabolism using a comparative genomics approach. Environ Technol 31:905–914

    Article  PubMed  CAS  Google Scholar 

  • Don TM, Chen CW, Chan TH (2006) Preparation and characterization of poly(hydroxyalkanoate) from the fermentation of Haloferax mediterranei. J Biomater Sci Polym 17:1425–1438

    Article  CAS  Google Scholar 

  • Esclapez J, Bonete MJ, Camacho M, Ferrer J, Pire C, Bautista V, Martínez-Espinosa RM, Zafrilla B, Pérez-Pomares F, Díaz S (2006) An optimized method to produce halophilic proteins in Escherichia coli. Microb Cell Fact 2006, 5(Suppl 1):S22

    Article  Google Scholar 

  • Esclapez J, Pire C, Bautista V, Martínez-Espinosa RM, Ferrer J, Bonete MJ (2007) Analysis of acidic surface of Haloferax mediterranei glucose dehydrogenase by site-directed mutagenesis. FEBS Lett 581:837–842

    Article  PubMed  CAS  Google Scholar 

  • Falb M, Müller K, Königsmaier L, Oberwinkler T, Horn P, von Gronau S, Gonzalez O, Pfeiffer F, Bornberg-Bauer E, Oesterhelt D (2008) Metabolism of halophilic archaea. Extremophiles 12:177–196

    Article  PubMed  CAS  Google Scholar 

  • Fang CJ, Ku KL, Lee MH, Su NW (2010) Influence of nutritive factors on C50 carotenoids production by Haloferax mediterranei ATCC 33500 with two-stage cultivation. Bioresour Technol 101:6487–6493

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Castillo R, Rodríguez-Valera F, Gonzalez-Ramos J, Ruiz-Berraquero F (1986) Accumulation of poly(β-hydroxybutyrate) by halobacteria. Appl Environ Microbiol 51:214–216

    PubMed  CAS  Google Scholar 

  • Ferrer J, Pérez-Pomares F, Bonete MJ (1996) NADP-glutamate dehydrogenase from the halophilic archaeon Haloferax mediterranei: enzyme purification. N-terminal sequence and stability. FEMS Microbiol Lett 141:59–63

    Article  PubMed  CAS  Google Scholar 

  • Good WA, Hartman PA (1970) Properties of the amylase from Halobacterium halobium. J Bacteriol 104:601–603

    PubMed  CAS  Google Scholar 

  • Greer FR, Shannon M (2005) Infant methemoglobinemia: the role of dietary nitrate in food and water. Pediatrics 116:784–786

    Article  PubMed  Google Scholar 

  • Han J, Lu Q, Zhou L, Liu H, Xiang H (2009) Identification of the polyhydroxyalkanoate (PHA)-specific acetoacetyl coenzyme A reductase among multiple FabG paralogs in Haloarcula hispanica and reconstruction of the PHA biosynthetic pathway in Haloferax volcanii. Appl Environ Microbiol 75:6168–6175

    Article  PubMed  CAS  Google Scholar 

  • Han J, Li M, Hou J, Wu L, Zhou J, Xiang H (2010) Comparison of four phaC genes from Haloferax mediterranei and their function in different PHBV copolymer biosyntheses in Haloarcula hispanica. Saline Systems 6:9

    Article  PubMed  Google Scholar 

  • Hough DW, Danson MJ (1999) Extremozymes. Curr Opin Chem Biol 3:39–46

    Article  PubMed  CAS  Google Scholar 

  • Howarth RW (2004) Human acceleration of the nitrogen cycle: drivers, consequences, and steps toward solutions. Water Sci Technol 49:7–13

    PubMed  CAS  Google Scholar 

  • Johnsen U, Dambeck M, Zaiss H, Fuhrer T, Soppa J, Sauer U, Schönheit P (2009) D-Xylose degradation pathway in the halophilic archaeon Haloferax volcanii. J Biol Chem 284:27290–27303

    Article  PubMed  CAS  Google Scholar 

  • Joo WA, Kim CW (2005) Proteomics of halophilic archaea. J Chromatogr B Analyt Technol Biomed Life Sci 815:237–250

    Article  PubMed  CAS  Google Scholar 

  • Karadzic IM, Maupin-Furlow JA (2005) Improvement of two-dimensional gel electrophoresis proteome maps of the haloarchaeon Haloferax volcanii. Proteomics 5:354–359

    Article  PubMed  CAS  Google Scholar 

  • Kirkland PA, Humbard MA, Daniels CJ, Maupin-Furlow JA (2008) Shotgun proteomics of the haloarchaeon Haloferax volcanii. J Proteome Res 7:5033–5039

    Article  PubMed  CAS  Google Scholar 

  • Klibanov AM (1989) Enzymatic catalysis in anhydrous organic solvents. Trends Biochem Sci 14:141–144

    Article  PubMed  CAS  Google Scholar 

  • Legat A, Gruber C, Zangger K, Wanner G, Stan-Lotter H (2010) Identification of polyhydroxyalkanoates in Halococcus and other haloarchaeal species. Appl Microbiol Biotechnol 87:1119–1127

    Article  PubMed  CAS  Google Scholar 

  • Lillo JG, Rodríguez-Valera F (1990) Effects of culture conditions on poly(beta-hydroxybutyric acid) production by Haloferax mediterranei. Appl Environ Microbiol 56:2517–2521

    PubMed  Google Scholar 

  • Litchfield CD (1998) Survival strategies for microorganisms in hypersaline environments and their relevance to life on early Mars. Meteorit Planet Sci 33:813–819

    Article  PubMed  CAS  Google Scholar 

  • Lledó B, Martínez-Espinosa RM, Marhuenda-Egea FC, Bonete MJ (2004) Respiratory nitrate reductase from haloarchaeon Haloferax mediterranei: biochemical and genetic analysis. Biochim Biophys Acta 1674:50–59

    PubMed  Google Scholar 

  • Lu Q, Han J, Zhou L, Zhou J, Xiang H (2008) Genetic and biochemical characterization of the poly(3-hydroxybutyrate-co-3-hydroxyvalerate) synthase in Haloferax mediterranei. J Bacteriol 190:4173–4180

    Article  PubMed  CAS  Google Scholar 

  • Mancinelli RL, Landheim R, Sánchez-Porro C, Dornmayr-Pfaffenhuemer M, Gruber C, Legat A, Ventosa A, Radax C, Ihara K, White MR, Stan-Lotter H (2009) Halorubrum chaoviator sp. nov., a haloarchaeon isolated from sea salt in Baja California, Mexico, Western Australia and Naxos, Greece. Int J Syst Evol Microbiol 59:1908–1913

    Article  PubMed  CAS  Google Scholar 

  • Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–83

    Article  PubMed  CAS  Google Scholar 

  • Marhuenda-Egea FC, Bonete MJ (2002) Extreme halophilic enzymes in organic solvents. Curr Opin Biotechnol 13:385–389

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Espinosa RM, Richardson DJ, Butt JN, Bonete MJ (2006) Respiratory nitrate and nitrite pathway in the denitrifier haloarchaeon Haloferax mediterranei. Biochem Soc Trans 34:115–117

    Article  PubMed  Google Scholar 

  • Martínez-Espinosa RM, Dridge EJ, Bonete MJ, Butt JN, Butler CS, Sargent F, Richardson DJ (2007a) Look on the positive side! The orientation, identification and bioenergetics of ‘Archaeal’ membrane-bound nitrate reductases. FEMS Microbiol Lett 276:129–139

    Article  PubMed  Google Scholar 

  • Martínez-Espinosa RM, Zafrilla B, Camacho M, Bonete MJ (2007b) Nitrate and nitrite removing from salted water by Haloferax mediterranei. Biocatal Biotransform 25:295–300

    Article  Google Scholar 

  • Martínez-Espinosa RM, Lledó B, Marhuenda-Egea FC, Díaz S, Bonete MJ (2009) NO −3 /NO −2 assimilation in halophilic archaea: physiological analysis, nasA and nasD expressions. Extremophiles 13:785–792

    Article  PubMed  Google Scholar 

  • Mevarech M, Frolow F, Gloss LM (2000) Halophilic enzymes: proteins with a grain of salt. Biophys Chem 86:155–164

    Article  PubMed  CAS  Google Scholar 

  • O’Connor EM, Shand RF (2002) Halocins and sulfolobicins: the emerging story of archaeal protein and peptide antibiotics. J Ind Microbiol Biotechnol 28:23–31

    PubMed  Google Scholar 

  • Olsson-Francis K, Cockella CS (2010) Experimental methods for studying microbial survival in extraterrestrial environments. J Microbiol Methods 80:1–13

    Article  PubMed  CAS  Google Scholar 

  • Oren A (1994) Enzyme diversity in halophilic archaea. Microbiologia 10:217–228

    PubMed  CAS  Google Scholar 

  • Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63

    PubMed  CAS  Google Scholar 

  • Oren A (2005) A hundred years of Dunaliella research: 1905–2005. Saline Systems 1:2

    Article  PubMed  Google Scholar 

  • Oren A (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Systems 4:2

    PubMed  Google Scholar 

  • Oren A (2010) Industrial and environmental applications of halophilic microorganisms. Environ Technol 31:825–834

    Article  PubMed  CAS  Google Scholar 

  • Parolis LAS, Boan IF, Rodríguez-Valera F, Widmalm G, Manca MC, Jansson PE, Sutherland IW (1996) The structure of the exopolysaccharide produced by the halophilic archaeon Haloferax mediterranei strain R1 (ATCC 33500). Carbohydr Res 295:147–156

    PubMed  CAS  Google Scholar 

  • Patzelt H, Kessler B, Oesterhelt D (2001) Descomposición de hidrocarburos halogenados por bacterias Archaea halófilas. Patent 16.09.2001-2159119. BOPI: 16.09.2001. Spain

    Google Scholar 

  • Peeters Z, Vos D, ten Kate IL, Selch F, van Sluis CA, Sorokin DY, Muijzer G, Stan-Lotter H, van Loosdrecht MC, Ehrenfreund P (2010) Survival and death of the haloarchaeon Natronorubrum strain HG-1 in a simulated martian environment. Adv Space Res 46:1149–1155

    Article  CAS  Google Scholar 

  • Pérez-Pomares F, Bautista V, Ferrer J, Pire C, Marhuenda-Egea FC, Bonete MJ (2003) α-amylase activity from the halophilic archaeon Haloferax mediterranei. Extremophiles 7:299–306

    Article  PubMed  Google Scholar 

  • Pérez-Pomares F, Díaz S, Bautista V, Pire C, Bravo G, Esclapez J, Zafrilla B, Bonete MJ (2009) Identification of several intracellular carbohydrate-degrading activities from the halophilic archaeon Haloferax mediterranei. Extremophiles 13:633–641

    Article  PubMed  Google Scholar 

  • Pire C, Marhuenda-Egea FC, Esclapez J, Alcaraz L, Ferrer J, Bonete MJ (2004) Stability and enzymatic studies of glucose dehydrogenase from the archaeon Haloferax mediterranei in reverse micelles. Biocatal Biotransform 22:17–23

    Article  CAS  Google Scholar 

  • Pire C, Esclapez J, Diaz S, Pérez-Pomares F, Ferrer J, Bonete MJ (2009) Alteration of coenzyme specificity in halophilic NAD(P)+ glucose dehydrogenase by site-directed mutagenesis. J Mol Catal B Enzym 59:261–265

    Article  CAS  Google Scholar 

  • Rodríguez-Valera F (1992) Biotechnological potential of halobacteria. Biochem Soc Symp 58:135–147

    PubMed  Google Scholar 

  • Schiraldi C, Giuliano M, De Rosa M (2002) Perspectives on biotechnological applications of archaea. Archaea 1:75–86

    Article  PubMed  CAS  Google Scholar 

  • Silveira CM, Gomes SP, Araújo AN, Montenegro MC, Todorovic S, Viana AS, Silva RJ, Moura JJ, Almeida MG (2010) An efficient non-mediated amperometric biosensor for nitrite determination. Biosens Bioelectron 25:2026–2032

    Article  PubMed  CAS  Google Scholar 

  • Tadeo X, López-Méndez B, Trigueros T, Laín A, Castaño D, Millet O (2009) Structural Basis for the amino acid composition of proteins from halophilic archaea. PLoS Biol 7:e1000257

    Article  PubMed  Google Scholar 

  • van den Burg B (2003) Extremophiles as a source for novel enzymes. Curr Opin Microbiol 6:213–218

    Article  PubMed  Google Scholar 

  • van Grinsven HJ, Rabl A, de Kok TM (2010) Estimation of incidence and social cost of colon cancer due to nitrate in drinking water in the EU: a tentative cost-benefit assessment. Environ Health 9:58

    Article  PubMed  Google Scholar 

  • Verhees CH, Kengen SWM, Tuininga JE, Schut GJ, Adams MWW, de Vos WM, van der Oost J (2003) The unique features of glycolytic pathways in Archaea. Biochem J 375:231–246

    Article  PubMed  CAS  Google Scholar 

  • Vidyasagar M, Prakash SB (2006) Optimization of culture conditions for the production of haloalkaliphilic thermostable protease from an extremely halophilic archaeon Halogeometricum sp. TSS101. Lett Appl Microbiol 43:385–391

    Article  PubMed  CAS  Google Scholar 

  • Wang G, Kennedy SP, Fasiludeen S, Rensing C, DasSarma S (2004) Arsenic resistance in Halobacterium sp. strain NRC-1 examined by using an improved gene knockout system. J Bacteriol 186:3187–3194

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms-proposal for the domains Archaea, Bacteria and Eukarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  PubMed  CAS  Google Scholar 

  • Yoshimatsu K, Iwasaki T, Fujiwara T (2002) Sequence and electron paramagnetic resonance analyses of nitrate reductase NarGH from a denitrifying halophilic euryarchaeote Haloarcula marismortui. FEBS Lett 516:145–150

    Article  PubMed  CAS  Google Scholar 

  • Zafrilla B, Martínez-Espinosa RM, Esclapez J, Pérez-Pomares F, Bonete MJ (2010) SufS protein from Haloferax volcanii involved in Fe-S cluster assembly in haloarchaea. Biochim Biophys Acta 1084:1476–1482

    Google Scholar 

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Authors and Affiliations

  1. División de Bioquímica y Biología Molecular, Facultad de Ciencias, Universidad de Alicante, Ap. 99, E-03080, Alicante, Spain

    María José Bonete & Rosa María Martínez-Espinosa

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  1. María José Bonete
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  2. Rosa María Martínez-Espinosa
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Correspondence to María José Bonete .

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Editors and Affiliations

  1. Faculty of Pharmacy, Department of Microbiology, University of Sevilla, Profesor García González 2, Sevilla, 41012, Spain

    Antonio Ventosa

  2. The Institute of Life Sciences, Department of Plant and Environmental Sc, The Hebrew University of Jerusalem, Jerusalem, 91904, Israel

    Aharon Oren

  3. , Insitute of Microbiology, Chinese Academy of Sciences, Beichen West Road 1, Beijing, China, People's Republic

    Yanhe Ma

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Bonete, M.J., Martínez-Espinosa, R.M. (2011). Enzymes from Halophilic Archaea: Open Questions. In: Ventosa, A., Oren, A., Ma, Y. (eds) Halophiles and Hypersaline Environments. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20198-1_19

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