Advertisement

Halocin Diversity Among Halophilic Archaea and Their Applications

  • Vijay Kumar
  • Santosh Kumar Tiwari
Chapter

Abstract

Haloarchaea and their metabolites show unusual properties such as stability under extreme conditions and create special interest for the search of novel products. In recent years, studies on systematics have intensified and identified many new genera and species. Haloarchaea belonging to class Halobacteria are divided into three orders: Halobacteriales, Haloferacales, and Natrialbales consisting of more than 48 genera and 216 species. Haloarchaea and their metabolites are useful for various industrial applications. Halophilic proteins and enzymes produced by haloarchaea remain functional under high salt concentrations, extreme pH, and high temperature at which bacterial counterparts denature. These features make haloarchaea an attractive source of a wide variety of biotechnological products, such as retinal proteins, osmolytes, carotenoids, various hydrolytic enzymes, polyhydroxyalkanoates (PHAs), and exopolysaccharides. The biomolecules produced by haloarchaea have important role in manufacturing of bioplastics, photoelectric devices, artificial retinas, holograms, bioremediation process, and numerous other potential applications in biotechnology. Further study is more focused to develop a low-cost platform for low-cost downstream process with better yield at larger scale. Halocins are the proteinaceous antimicrobial proteins/peptides (AMPs) secreted by several members of haloarchaea. The production, purification, and characterization of halocins have been studied from various members of haloarchaea to understand the unique importance for their possible applications. The therapeutic potential of halocins needs more exploration to decipher an alternate to clinical antibiotics.

Keywords

Haloarchaea Extremophiles Carotenoids Halocins Purification Antibiotics Applications 

References

  1. Adrio J, Demain A (2014) Microbial enzymes: tools for biotechnological processes. Biomol Ther 4:117–139Google Scholar
  2. Akolkar AV, Durai D, Desai AJ (2010) Halobacterium sp. SP1(1) as a starter culture for accelerating fish sauce fermentation. J Appl Microbiol 109:44–53PubMedPubMedCentralGoogle Scholar
  3. Alsafadi D, Al-Mashaqbeh O (2017) A one-stage cultivation process for the production of poly-3-(hydroxybutyrate-co-hydroxyvalerate) from olive mill wastewater by Haloferax mediterranei. New Biotechnol 34:47–53CrossRefGoogle Scholar
  4. Amoozegar MA, Ghasemi A, Razavi MR, Naddaf S (2007) Evaluation of hexavalent chromium reduction by chromate-resistant moderately halophile, Nesterenkonia sp. strain MF2. Process Biochem 42:1475–1479CrossRefGoogle Scholar
  5. Amoozegar MA, Siroosi M, Atashgahi S, Smidt H, Ventosa A (2017) Systematics of haloarchaea and biotechnological potential of their hydrolytic enzymes. Microbiology 163(5):623–645PubMedCrossRefPubMedCentralGoogle Scholar
  6. Anobom CD, Pinheiro AS, De-Andrade RA, Aguieiras ECG, Andrade GC, Moura MV, Almeida RV, Freire DM (2014) From structure to catalysis: recent developments in the biotechnological applications of lipases. Biomed Res Int 2014:1–11CrossRefGoogle Scholar
  7. Baati H, Guermazi S, Gharsallah N, Sghir A, Ammar E (2010) Novel prokaryotic diversity in sediments of Tunisian multipond solar saltern. Res Microbiol 161:573–582PubMedCrossRefPubMedCentralGoogle Scholar
  8. Balasubramanian S, Pal S, Bagchi B (2002) Hydrogen-bond dynamics near a micellar surface: origin of the universal slow relaxation at complex aqueous interfaces. Phys Rev Lett 89:115505PubMedCrossRefPubMedCentralGoogle Scholar
  9. Banat IM, Makkar RS, Cameotra SS (2000) Potential commercial applications of microbial surfactants. Appl Microbiol Biotechnol 53:495–508PubMedCrossRefPubMedCentralGoogle Scholar
  10. Berlendis S, Cayol JL, Verhe F, Laveau S, Tholozan JL, Ollivier B, Auria R (2009) First evidence of aerobic biodegradation of BTEX compounds by pure cultures of Marinobacter. Appl Biochem Biotechnol 160:1992–1999PubMedCrossRefPubMedCentralGoogle Scholar
  11. Besse A, Peduzzi J, Rebuffat S, Carre-Mlouka A (2015) Antimicrobial peptides and proteins in the face of extremes lessons from archaeocins. Biochimie 118:344–355PubMedCrossRefPubMedCentralGoogle Scholar
  12. Bidle K, Amadio W, Oliveira P, Paulish T, Hicks S, Earnest C (2005) A phylogenetic analysis of haloarchaea found in a solar saltern. Bios 76:89–96CrossRefGoogle Scholar
  13. Birbir M, Calli B, Mertoglu B, Bardavid RE, Oren A, Ogmen MN, Ogan A (2007) Extremely halophilic archaea from Tuz Lake, Turkey, and the adjacent Kaldirim and Kayacik salterns. World J Microbiol Biotechnol 23(3):309–316CrossRefGoogle Scholar
  14. Bonete MJ, Martinez-Espinosa RM, Pire C, Zafrilla B, Richardson DJ (2008) Nitrogen metabolism in haloarchaea. Saline Syst 4:9PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bonete MJ, Bautista V, Esclapez J, García-Bonete MJ, Pire C, Camacho M, Torregrosa-Crespo J, Martínez-Espinosa RM (2015) New uses of haloarchaeal species in bioremediation processes. In: Shiomi N (ed) Advances in bioremediation of wastewater and polluted soil. InTech, Rijeka, pp 23–49Google Scholar
  16. 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(1–2):21–26CrossRefGoogle Scholar
  17. Bozic N, Ruiz J, Santin JL, Vujic Z (2011) Production and properties of the highly efficient raw starch digesting α-amylase from a Bacillus licheniformis ATCC 9945a. Biochem Eng J 53:203–209CrossRefGoogle Scholar
  18. Britton KL, Baker PJ, Fisher M, Ruzheinikov 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 U S A 103:4846–4851PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bugnicourt E, Cinelli P, Lazzeri A, Álvarez V (2014) Polyhydroxyalkanoate (PHA): review of synthesis, characteristics, processing and potential applications in packaging. Express Polym Lett 8(11):791–808CrossRefGoogle Scholar
  20. Burg MB, Ferraris JD (2008) Intracellular organic osmolytes: function and regulation. J Biol Chem 283:7309–7313PubMedPubMedCentralCrossRefGoogle Scholar
  21. Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML (2004) Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl Environ Microbiol 70(9):5258–5265PubMedPubMedCentralCrossRefGoogle Scholar
  22. Capiralla H, Hiroi T, Hirokawa T, Maeda S (2002) Purification and characterization of a hydrophobic amino acid-specific endopeptidase from Halobacterium halobium S9 with potential application in debittering of protein hydrolysates. Process Biochem 38:571–579CrossRefGoogle Scholar
  23. Chang HW, Kim KH, Nam YD, Roh SW, Kim MS, Jeon CO, Oh HM, Bae JW (2008) Analysis of yeast and archaeal population dynamics in kimchi using denaturing gradient gel electrophoresis. Int J Food Microbiol 126:159–166PubMedCrossRefPubMedCentralGoogle Scholar
  24. Charlesworth J, Burns BP (2016) Extremophilic adaptations and biotechnological applications in diverse environments. AIMS Microbiol 2(3):251–261CrossRefGoogle Scholar
  25. Cheung J, Danna KJ, O’Connor EM, Price LB, Shand RF (1997) Isolation, sequence, and expression of the gene encoding halocin H4, a bacteriocin from the halophilic archaeon H. mediterranei R4. J Bacteriol 179:548–551PubMedPubMedCentralCrossRefGoogle Scholar
  26. Coronado MJ, Vargas C, Mellado E, Tegos G, Drainas C, Nieto JJ, Ventosa A (2000) The α-amylase gene amyH of the moderate halophile Halomonas meridiana: cloning and molecular characterization. Microbiology 146:861–868PubMedCrossRefPubMedCentralGoogle Scholar
  27. Dahiya N, Tewari R, Hoondal GS (2006) Biotechnological aspects of chitinolytic enzymes: a review. Appl Microbiol Biotechnol 71:773–782PubMedCrossRefPubMedCentralGoogle Scholar
  28. DasSarma S, Arora P (1997) Genetic analysis of the gas vesicle gene cluster in haloarchaea. FEMS Microbiol Lett 153:1–10CrossRefGoogle Scholar
  29. DasSarma S, Arora P (2001) Halophiles. In: Encyclopedia of life sciences. Nature Publishing Group, Basingstoke, pp 1–9. www.els.net Google Scholar
  30. DasSarma S, DasSarma P (2012) Halophiles. In: eLS. Wiley.  https://doi.org/10.1002/9780470015902.a0000394.pub3
  31. DasSarma P, Coker JA, Huse V, DasSarma S (2010) Halophiles, industrial applications. In: Flickinger MC (ed) Encyclopedia of industrial biotechnology: bioprocess, bioseparation, and cell technology, vol 7. Wiley, New York, pp 2769–2777Google Scholar
  32. DasSarma S, DasSarma P (2015) Halophiles and their enzymes: negativity put to good use. Curr Opin Microbiol 25:120–126PubMedPubMedCentralCrossRefGoogle Scholar
  33. Delgado-Vargas F, Jiménez AR, Paredes-López O (2000) Natural pigments: carotenoids, anthocyanins, and betalains—characteristics, biosynthesis, processing, and stability. Crit Rev Food Sci Nutr 40:173–289PubMedCrossRefPubMedCentralGoogle Scholar
  34. Don TM, Chen CW, Chan TH (2006) Preparation and characterization of poly(hydroxyalkanoate) from the fermentation of Haloferax mediterranei. J Biomater Sci Polym Ed 17(12):1425–1438PubMedCrossRefPubMedCentralGoogle Scholar
  35. Ebert K, Goebel W, Rdest U, Surek B (1986) Genes and genome structures in the archaebacteria. Syst Appl Microbiol 7:30–35CrossRefGoogle Scholar
  36. Eichler J (2001) Biotechnological uses of archaeal extremozymes. Biotechnol Adv 19(4):261–278PubMedCrossRefPubMedCentralGoogle Scholar
  37. Ellen AF, Rohulya OV, Fusetti F, Wagner M, Albers SV, Driessen AJ (2011) The sulfolobicin genes of Sulfolobus acidocaldarius encode novel antimicrobial proteins. J Bacteriol 193:4380–4387PubMedPubMedCentralCrossRefGoogle Scholar
  38. El-Sayed WS, Takaichi S, Saida H, Kamekura M, Abu-Shady M, Seki H, Kuwabara T (2002) Effects of light and low oxygen tension on pigment biosynthesis in Halobacterium salinarum, revealed by a novel method to quantify both retinal and carotenoids. Plant Cell Physiol 43:379–383PubMedCrossRefPubMedCentralGoogle Scholar
  39. Elshahed MS, Savage KN, Oren A, Gutierrez MC, Ventosa A, Krumholz LR (2004) Haloferax sulfurifontis sp. nov., a halophilic archaeon isolated from a sulfide- and sulfur-rich spring. Int J Syst Evol Microbiol 54:2275–2279PubMedCrossRefPubMedCentralGoogle Scholar
  40. Enache M, Itoh T, Kamekura M, Teodosiu G, Dumitru L (2007) Haloferax prahovense sp. nov., an extremely halophilic archaeon isolated from a Romanian salt lake. Int J Syst Evol Microbiol 57:393–397PubMedCrossRefPubMedCentralGoogle Scholar
  41. Essen LO (2002) Halorhodopsin: light-driven ion pumping made simple? Curr Opin Struct Biol 12:516–522PubMedCrossRefPubMedCentralGoogle Scholar
  42. Fassett RG, Coombes JS (2012) Astaxanthin in cardiovascular health and disease. Molecules 17:2030–2048PubMedPubMedCentralCrossRefGoogle Scholar
  43. Fernandez AB, Vera-Gargallo B, Sanchez-Porro C, Ghai R, Papke RT, Rodriguez-Valera F, Ventosa A (2014) Comparison of prokaryotic community structure from Mediterranean and Atlantic saltern concentrator ponds by a metagenomic approach. Front Microbiol 5:196PubMedPubMedCentralCrossRefGoogle Scholar
  44. Fiedor J, Burda K (2014) Potential role of carotenoids as antioxidants in human health and disease. Nutrients 6:466–488PubMedPubMedCentralCrossRefGoogle Scholar
  45. Ghanmi F, Carre-Mlouka A, Vandervennet M, Boujelben I, Frikha D, Ayadi H, Peduzzi J, Rebuffat S, Maalej S (2016) Antagonistic interactions and production of halocin antimicrobial peptides among extremely halophilic prokaryotes isolated from the solar saltern of Sfax, Tunisia. Extremophiles 20(3):363–374PubMedCrossRefPubMedCentralGoogle Scholar
  46. Gibbons NE (1974) Family V. Halobacteriaceae fam. nov. In: Buchanan RE, Gibbons NE (eds) Bergey’s manual of determinative bacteriology. Williams & Wilkins, Baltimore, pp 269–273Google Scholar
  47. Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordan JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359PubMedPubMedCentralCrossRefGoogle Scholar
  48. Grant WD, Kamekura M, McGenity TJ, Ventosa A (2001) Class III. Halobacteria class. Nov. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 1. Springer-Verlag, New York, pp 294–334Google Scholar
  49. Guan Z, Naparstek S, Calo D, Eichler J (2012) Protein glycosylation as an adaptive response in archaea: growth at different salt concentrations leads to alterations in Haloferax volcanii S-layer glycoprotein N-glycosylation. Environ Microbiol 14:743–753PubMedCrossRefPubMedCentralGoogle Scholar
  50. Guo J, Zhou J, Wang D, Tian C, Wang P, Uddin MS (2008) A novel moderately halophilic bacterium for decolorizing azo dye under high salt condition. Biodegradation 19:15–19PubMedCrossRefPubMedCentralGoogle Scholar
  51. Gupta RS, Naushad S, Baker S (2015) Phylogenomic analyses and molecular signatures for the class Halobacteria and its two major clades: a proposal for division of the class Halobacteria into an emended order Halobacteriales and two new orders, Haloferacales ord. nov. and Natrialbales ord. nov., containing the novel families Haloferacaceae fam. nov. and Natrialbaceae fam. nov. Int J Syst Evol Microbiol 65:1050–1069PubMedCrossRefPubMedCentralGoogle Scholar
  52. Guzman H, Van-Thuoc D, Martin J, Hatti-Kaul R, Quillaguaman J (2009) A process for the production of ectoine and poly (3-hydroxybutyrate) by Halomonas boliviensis. Appl Microbiol Biotechnol 84:1069–1077PubMedCrossRefPubMedCentralGoogle Scholar
  53. Han J, Lu Q, Zhou L, Zhou J, Xiang H (2007) Molecular characterization of the phaECHm genes, required for biosynthesis of poly(3-hydroxybutyrate) in the extremely halophilic archaeon Haloarcula marismortui. Appl Environ Microbiol 73(19):6058–6065PubMedPubMedCentralCrossRefGoogle Scholar
  54. Haseltine C, Hill T, Montalvo-Rodriguez R, Kemper SK, Shand RF, Blum P (2001) Secreted euryarchaeal microhalocins kill hyperthermophilic crenarchaea. J Bacteriol 183:287–291PubMedPubMedCentralCrossRefGoogle Scholar
  55. Hatori Y, Sato M, Orishimo K, Yatsunami R, Endo K, Fukui T, Nakamura S (2006) Characterization of recombinant family 18 chitinase from extremely halophilic archaeon Halobacterium salinarum strain NRC-1. Chitin Chitosan Res 12:201Google Scholar
  56. Hezayen FF, Rehm BH, Tindall BJ, Steinbüchel 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 51:1133–1142PubMedCrossRefPubMedCentralGoogle Scholar
  57. Hilhorst R, Dunnewind B, Orsel R, Stegeman P, Vliet T, Gruppen H, Schols HA (1999) Baking performance, rheology, and chemical composition of wheat dough and gluten affected by xylanase and oxidative enzymes. J Food Sci 64:808–813CrossRefGoogle Scholar
  58. Hiraga K, Nishikata Y, Namwong S, Tanasupawat S, Takada K, Oda K (2005) Purification and characterization of serine proteinase from a halophilic bacterium, Filobacillus sp. RF2-5. Biosci Biotechnol Biochem 69:38–44PubMedCrossRefPubMedCentralGoogle Scholar
  59. Hong FT (1986) The bacteriorhodopsin model membrane system as a prototype molecular computing element. Biosystems 19:223–236PubMedCrossRefPubMedCentralGoogle Scholar
  60. Hou J, Han J, Cai L, Zhou J, Lü Y, Jin C, Liu J, Xiang H (2014) Characterization of genes for chitin catabolism in Haloferax mediterranei. Appl Microbiol Biotechnol 98:1185–1194PubMedCrossRefPubMedCentralGoogle Scholar
  61. Hutcheon GW, Vasisht N, Bolhuis A (2005) Characterization of a highly stable α-amylase from the halophilic archaeon Haloarcula hispanica. Extremophiles 9:487–495CrossRefGoogle Scholar
  62. Imadalou-Idres N, Carre-Mlouka A, Vandervennet M, Yahiaoui H, Peduzzi J, Rebuffat S (2013) Diversity and antimicrobial activity of cultivable halophilic archaea from three Algerian sites. J Life Sci 10:1057–1069Google Scholar
  63. Jain S, Caforio A, Fodran P, Lolkema JS, Minnaard AJ, Driessen AJM (2014) Identification of CDP-archaeol synthase, a missing link of ether lipid biosynthesis in archaea. Chem Biol 21:1392–1401PubMedCrossRefPubMedCentralGoogle Scholar
  64. Jarrell KF, Ding Y, Meyer BH, Albers SV, Kaminski L, Eichler J (2014) N-linked glycosylation in archaea: a structural, functional, and genetic analysis. Microbiol Mol Biol Rev 78:304–341PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kamekura M, Kates M (1999) Structural diversity of membrane lipids in members of halobacteriaceae. Biosci Biotechnol Biochem 63:969–972PubMedCrossRefPubMedCentralGoogle Scholar
  66. Karan R, Capes MD, DasSarma P, DasSarma S (2013) Cloning, overexpression, purification, and characterization of a polyextremophilic β-galactosidase from the Antarctic haloarchaeon Halorubrum lacusprofundi. BMC Biotechnol 13:3PubMedPubMedCentralCrossRefGoogle Scholar
  67. Karthikeyan P, Bhat SG, Chandrasekaran M (2013) Halocin SH10 production by an extreme haloarchaeon Natrinema sp. BTSH10 isolated from salt pans of South India. Saudi J Biol Sci 20:205–212PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kavitha P, Lipton AP, Sarika AR, Aishwarya MS (2011) Growth characteristics and halocin production by a new isolate, H. volcanii KPSl from Kovalam solar saltern (India). Res J Biol Sci 6:257–262Google Scholar
  69. Kebbouche-Gana S, Gana ML, Khemili S, Fazouane-Naimi F, Bouanane NA, Penninckx M, Hacene H (2009) Isolation and characterization of halophilic archaea able to produce biosurfactants. J Ind Microbiol Biotechnol 36:727–738PubMedCrossRefPubMedCentralGoogle Scholar
  70. Kelly M, Jensen SL (1967) Bacterial carotenoids. XXVI. C50-carotenoids. 2. Bacterioruberin. Acta Chem Scand 21(9):2578–2580PubMedCrossRefPubMedCentralGoogle Scholar
  71. Keshri J, Mishra A, Jha B (2013) Microbial population index and community structure in saline–alkaline soil using gene targeted metagenomics. Microbiol Res 168(3):165–173PubMedCrossRefPubMedCentralGoogle Scholar
  72. Kim J, Dordick JS (1997) Unusual salt and solvent dependence of a protease from an extreme halophile. Biotechnol Bioeng 55:471–479PubMedCrossRefPubMedCentralGoogle Scholar
  73. Kim KK, Lee KC, Lee JS (2011) Halogranum salarium sp. nov., a halophilic archaeon isolated from sea salt. Syst Appl Microbiol 34:576–580PubMedCrossRefPubMedCentralGoogle Scholar
  74. Klare J, Chizhov I, Engelhard M (2008) Microbial rhodopsins: scaffolds for ion pumps, channels, and sensors. Bioenergetics. Results Probl Cell Differ 45:73–122PubMedCrossRefPubMedCentralGoogle Scholar
  75. Kumar V, Tiwari SK (2017a) Halocin HA1: an archaeocin produced by the haloarchaeon Haloferax larsenii HA1. Process Biochem 61:202–208CrossRefGoogle Scholar
  76. Kumar V, Tiwari SK (2017b) Activity-guided separation and characterization of new halocin HA3 from fermented broth of Haloferax larsenii HA3. Extremophiles 21:609–621PubMedCrossRefPubMedCentralGoogle Scholar
  77. Kumar V, Saxena J, Tiwari SK (2016) Description of a halocin-producing Haloferax larsenii HA1 isolated from Pachpadra salt lake in Rajasthan. Arch Microbiol 198:181–192PubMedCrossRefPubMedCentralGoogle Scholar
  78. Kushner DJ, Kamekura M (1998) Physiology of halophilic eubacteria. In: Rodriguez-Valera F (ed) Halophilic bacteria, vol 1. CRC Press, Inc, Boca Raton, pp 109–138Google Scholar
  79. Kushwaha SC, Kramer JK, Kates M (1975) Isolation and characterization of C50-carotenoid pigments and other polar isoprenoids from Halobacterium cutirubrum. Biochim Biophys Acta 398:303–314PubMedCrossRefPubMedCentralGoogle Scholar
  80. Labes A, Karlsson EN, Fridjonsson OH, Turner P, Hreggvidson GO, Kristjansson JK, Holst O, Schönheit P (2008) Novel members of glycoside hydrolase family 13 derived from environmental DNA. Appl Environ Microbiol 74:1914–1921PubMedPubMedCentralCrossRefGoogle Scholar
  81. Laycock B, Halley P, Pratt S, Werker A, Lant P (2013) The petrochemical properties of microbial polyhydroxyalkanoates. Prog Polym Sci 38:536–583CrossRefGoogle Scholar
  82. Lee HS (2013) Diversity of halophilic archaea in fermented foods and human intestines and their application. J Microbiol Biotechnol 23:1645–1653PubMedCrossRefPubMedCentralGoogle Scholar
  83. Lequerica JL, O’Connor JE, Such L, Alberola A, Meseguer I, Dolz M, Torreblanca M, Moya A, Colom F, Soria B (2006) A halocin acting on Na+/H+ exchanger of Haloarchaea as a new type of inhibitor in NHE of mammals. J Physiol Biochem 62:253–262PubMedCrossRefPubMedCentralGoogle Scholar
  84. Li X, Yu HY (2014) Characterization of an organic solvent-tolerant lipase from Haloarcula sp. G41 and its application for biodiesel production. Folia Microbiol 59(6):455–463CrossRefGoogle Scholar
  85. Li Y, Xiang H, Liu J, Zhou M, Tan H (2003) Purification and bio- logical caracterization of halocin C8, a novel peptide antibiotic from Halobacterium strain AS7092. Extremophiles 7:401–407PubMedCrossRefPubMedCentralGoogle Scholar
  86. Liebgott PP, Labat M, Casalot L, Amouric A, Lorquin J (2007) Bioconversion of tyrosol into hydroxytyrosol and 3,4-dihydroxyphenylacetic acid under hypersaline conditions by the new Halomonas sp. strain HTB24. FEMS Microbiol Lett 276:26–33PubMedCrossRefPubMedCentralGoogle Scholar
  87. LPSN (2016) List of prokaryotic names with standing in nomenclature. http://www.bacterio.net/
  88. 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(12):4173–4180PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lynch EA, Langille MGI, Darling A, Wilbanks EG, Haltiner C, Shao KSY, Starr MO, Teiling C, Harkins TT, Edwards RA, Eisen JA, Facciotti MT (2012) Sequencing of seven haloarchaeal genomes reveals patterns of genomic flux. PLoS One 7:e41389PubMedPubMedCentralCrossRefGoogle Scholar
  90. Ma Y, Galinski EA, Grant WD, Oren A, Ventosa A (2010) Halophiles 2010: life in saline environments. Appl Environ Microbiol 76:6971–6981PubMedPubMedCentralCrossRefGoogle Scholar
  91. Madern D, Ebel C, Zaccai G (2000) Halophilic adaptation of enzymes. Extremophiles 4:91–98PubMedCrossRefPubMedCentralGoogle Scholar
  92. Maturrano L, Santos F, Rosselló-Mora R, Antón J (2006) Microbial diversity in Maras salterns, a hypersaline environment in the Peruvian Andes. Appl Environ Microbiol 72:3887–3895PubMedPubMedCentralCrossRefGoogle Scholar
  93. McCool GJ, Cannon MC (2001) PhaC and PhaR are required for polyhydroxyalkanoic acid synthase activity in Bacillus megaterium. J Bacteriol 183(14):4235–4243PubMedPubMedCentralCrossRefGoogle Scholar
  94. McGenity TJ, Gemmell RT, Grant WD, Stan-Lotter H (2000) Origins of halophilic microorganisms in ancient salt deposits. Environ Microbiol 2(3):243–250PubMedCrossRefPubMedCentralGoogle Scholar
  95. Meng DC, Shen R, Yao H, Chen JC, Wu Q, Chen GQ (2014) Engineering the diversity of polyesters. Curr Opin Biotechnol 29:24–33PubMedCrossRefPubMedCentralGoogle Scholar
  96. Meseguer I, Rodriguez-Valera F (1985) Production and purification of halocin H4. FEMS Microbiol Lett 28:177–182CrossRefGoogle Scholar
  97. Minegishi H, Kamekura M, Itoh T, Echigo A, Usami R, Hashimoto T (2010) Further refinement of the phylogeny of the Halobacteriaceae based on the full-length RNA polymerase subunit B’ (rpoB’) gene. Int J Syst Evol Microbiol 60(10):2398–2408PubMedCrossRefPubMedCentralGoogle Scholar
  98. Mormile MR, Biesen MA, Gutierrez MC, Ventosa A, Pavlovich JB, Onstott TC, Fredrickson JK (2003) Isolation of Halobacterium salinarum retrieved directly from halite brine inclusions. Environ Microbiol 5:1094–1102PubMedCrossRefPubMedCentralGoogle Scholar
  99. Moschetti G, Aponte M, Blaiotta G, Casaburi A, Chiurazzi M, Ventorino V, Villani F (2006) Characterization of halophilic archaea isolated from different hypersaline ecosystems. Ann Microbiol 56(2):119–127CrossRefGoogle Scholar
  100. Mozejko-Ciesielska J, Kiewisz R (2016) Bacterial polyhydroxyalkanoates: still fabulous? Microbiol Res 192:271–282PubMedCrossRefPubMedCentralGoogle Scholar
  101. Muller-Santos M, de Souza EM, Pedrosa FD, Mitchell DA, Longhi S, Carriere F, Canaan S, Krieger N (2009) First evidence for the salt-dependent folding and activity of an esterase from the halophilic archaea Haloarcula marismortui. Biochim Biophys Acta 1791:719–729PubMedCrossRefPubMedCentralGoogle Scholar
  102. Munawar N, Engel PC (2013) Halophilic enzymes: characteristics, structural adaptation and potential applications for biocatalysis. Curr Biotechnol 2(4):334–344CrossRefGoogle Scholar
  103. Najera-Fernandez C, Zafrilla B, Bonete MJ, Martınez- Espinosa RM (2012) Role of the denitrifying Haloarchaea in the treatment of nitrite-brines. Int Microbiol 15(3):111–119PubMedPubMedCentralGoogle Scholar
  104. Namwong S, Hiraga K, Takada K, Tsunemi M, Tanasupawat S, Oda K (2006) A halophilic serine proteinase from Halobacillus sp. SR5-3 isolated from fish sauce: purification and characterization. Biosci Biotechnol Biochem 70:1395–1401PubMedCrossRefPubMedCentralGoogle Scholar
  105. Naziri D, Hamidi M, Hassanzadeh S, Vahideh T, Zanjani BM, Nazemyieh H, Hejazi MA, Hejazi MS (2014) Analysis of carotenoid production by Halorubrum sp. TBZ126: an extremely halophilic archaeon from Urmia Lake. Adv Pharm Bull 4:61–67PubMedPubMedCentralGoogle Scholar
  106. Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8:68–82PubMedCrossRefPubMedCentralGoogle Scholar
  107. Norton CF, Grant WD (1988) Survival of halobacteria within fluid inclusions of salt crystals. J Gen Microbiol 134:1365–1373Google Scholar
  108. O’Connor EM, Shand RF (2002) Halocins and sulfolobicins: the emerging story of archaeal protein and peptide antibiotics. J Ind Microbiol Biotechnol 28:23–31PubMedCrossRefPubMedCentralGoogle Scholar
  109. Obayashi A, Hiraoka N, Kita K, Nakajima H, Shuzo T (1988) US Patent 4:724, 209, US Cl. 435/199Google Scholar
  110. Oh D, Porter K, Russ B, Burns D, Dyall-Smith M (2010) Diversity of Haloquadratum and other haloarchaea in three, geographically distant, Australian saltern crystallizer ponds. Extremophiles 141:161–169CrossRefGoogle Scholar
  111. Olivera ER, Arcos M, Naharro G, Luengo JM (2010) Unusual PHA biosynthesis. In: Chen GQ (ed) Plastics from bacteria, vol 14. Microbiology Monographs, Springer, Berlin/Heidelberg, pp 133–186CrossRefGoogle Scholar
  112. Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63CrossRefGoogle Scholar
  113. 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, 3rd edn. Springer, New York, pp 263–282Google Scholar
  114. Oren A (2010) Industrial and environmental applications of Halophilic microorganisms. Environ Technol 31:825–834CrossRefGoogle Scholar
  115. Oren A (2011) Diversity of halophiles. In: Horikoshi K (ed) Extremophiles handbook, vol 1. Springer, Tokyo, pp 310–322Google Scholar
  116. Oren A (2012) Taxonomy of the family Halobacteriaceae: a paradigm for changing concepts in prokaryote systematics. Int J Syst Evol Microbiol 62:263–271PubMedCrossRefPubMedCentralGoogle Scholar
  117. Oren A (2013) Life at high salt concentrations, intracellular KCl concentrations, and acidic proteomes. Front Microbiol 4:315PubMedPubMedCentralCrossRefGoogle Scholar
  118. Oren A (2014) Taxonomy of halophilic archaea: current status and future challenges. Extremophiles 18:825–834PubMedCrossRefPubMedCentralGoogle Scholar
  119. Oren A, Rodríguez-Valera F (2001) The contribution of halophilic bacteria to the red coloration of saltern crystallizer ponds. FEMS Microbiol Ecol 36:123–130PubMedPubMedCentralGoogle Scholar
  120. Oren A, Ventosa A, Grant WD (1997) Proposal of minimal standards for the description of new taxa in the order Halobacteriales. Int J Syst Bacteriol 47:233–238CrossRefGoogle Scholar
  121. Oren A, Arahal DR, Ventosa A (2009) Emended descriptions of genera of the family Halobacteriaceae. Int J Syst Evol Microbiol 59:637–642PubMedCrossRefPubMedCentralGoogle Scholar
  122. Oxley APA, Lanfranconi MP, Würdemann D, Ott S, Schreiber S, McGenity TJ, Timmis KN, Nogales B (2010) Halophilic archaea in the human intestinal mucosa. Environ Microbiol 12(9):2398–2410PubMedCrossRefPubMedCentralGoogle Scholar
  123. Palczewski G, Amengual J, Hoppel CL, von Lintig J (2014) Evidence for compartmentalization of mammalian carotenoid metabolism. FASEB J 28:4457–4469PubMedPubMedCentralCrossRefGoogle Scholar
  124. Park EJ, Chang HW, Kim KH, Nam YD, Roh SW, Bae JW (2009) Application of quantitative real-time PCR for enumeration of total bacterial, archaeal, and yeast populations in kimchi. J Microbiol 47:682–685PubMedCrossRefPubMedCentralGoogle Scholar
  125. Parka GT, Son HJ (2007) Keratinolytic activity of Bacillus megaterium F7–1, a feather-degrading mesophilic bacterium. Microbiol Res 164:478–485CrossRefGoogle Scholar
  126. Pasic L, Velikonja BH, Ulrih NP (2008) Optimization of the culture conditions for the production of a bacteriocin from halophilic archaeon Sech7a. Prep Biochem Biotechnol 38:229–245PubMedCrossRefPubMedCentralGoogle Scholar
  127. 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 7:299–306CrossRefGoogle Scholar
  128. Pfeifer F (2015) Haloarchaea and the formation of gas vesicles. Life (Basel) 5(1):385–402Google Scholar
  129. Platas G, Meseguer I, Amils R (2002) Purification and biological characterization of halocin H1 from Haloferax mediterranei M2a. Int Microbiol 5:15–19PubMedCrossRefPubMedCentralGoogle Scholar
  130. Poli A, Di Donato P, Abbamondi GR, Nicolaus B (2011) Synthesis, production, and biotechnological applications of exopolysaccharides and polyhydroxyalkanoates by archaea. Archaea 2011:693253PubMedPubMedCentralCrossRefGoogle Scholar
  131. Prangishvili D, Holz I, Stieger E, Nickell S, Kristjansson JK, Zillig W (2000) Sulfolobicins, specific proteinaceous toxins produced by strains of the extremely thermophilic archaeal genus Sulfolobus. J Bacteriol 182:2985–2988PubMedPubMedCentralCrossRefGoogle Scholar
  132. Price LB, Shand RF (2000) Halocin S8: a 36-amino-acid microhalocin from the haloarchaeal strain S8a. J Bacteriol 182:4951–4958PubMedPubMedCentralCrossRefGoogle Scholar
  133. Purdy KJ, Cresswell-Maynard TD, Nedwell DB, McGenity TJ, Grant WD, Timmis KN, Embley TM (2004) Isolation of haloarchaea that grow at low salinities. Environ Microbiol 6:591–595PubMedCrossRefPubMedCentralGoogle Scholar
  134. Quillaguamán J, Guzmán H, Van-Thuoc D, Hatti-Kaul R (2010) Synthesis and production of polyhydroxyalkanoates by halophiles: current potential and future prospects. Appl Microbiol Biotechnol 85:1687–1696PubMedCrossRefPubMedCentralGoogle Scholar
  135. Ratnakar D (2013) Use of halophile physiology and adaptations in various industrial applications. Res J Biotechnol 8(2):1Google Scholar
  136. Rdest U, Sturm M (1987) Bacteriocins from halobacteria. In: Burgess R (ed) Protein purification: micro to macro. Alan R Liss, New York, pp 271–278Google Scholar
  137. Rehm BH (2003) Polyester synthases: natural catalysts for plastics. Biochem J 376:15–33PubMedPubMedCentralCrossRefGoogle Scholar
  138. Rivera SM, Canela-Garayoa R (2012) Analytical tools for the analysis of carotenoids in diverse materials. J Chromatogr A 1224:1–10PubMedCrossRefPubMedCentralGoogle Scholar
  139. Rodrigo-Baños M, Garbayo I, Vílchez C, Bonete MJ, Martínez-Espinosa RM (2015) Carotenoids from haloarchaea and their potential in biotechnology. Mar Drugs 13:5508–5532PubMedPubMedCentralCrossRefGoogle Scholar
  140. Rodriguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A (1981) Characteristics of the heterotrophic bacterial populations in hypersaline environments of different salt concentrations. Microb Ecol 7(3):235–243PubMedCrossRefPubMedCentralGoogle Scholar
  141. Rodriguez-Valera F, Juez G, Kushner DJ (1982) Halocins: salt – dependent bacteriocins produced by extremely halophilic rods. Can J Microbiol 28:151–154CrossRefGoogle Scholar
  142. Roh SW, Bae JW (2009) Halorubrum cibi sp. nov., an extremely halophilic archaeon from salt-fermented seafood. J Microbiol 47:162–166PubMedCrossRefPubMedCentralGoogle Scholar
  143. Roh SW, Kim KH, Nam YD, Chang HW, Park EJ, Bae JW (2010) Investigation of archaeal and bacterial diversity in fermented seafood using barcoded pyrosequencing. ISME J 4:1–16PubMedCrossRefPubMedCentralGoogle Scholar
  144. Ross RP, Morgan S, Hill C (2002) Preservation and fermentation: past, present and future. Int J Food Microbiol 79:3–16PubMedCrossRefPubMedCentralGoogle Scholar
  145. Samuel BS, Hansen EE, Manchester JK, Coutinho PM, Henrissat B, Fulton R, Latreille P, Kim K, Wilson RK, Gordon JI (2007) Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut. Proc Natl Acad Sci U S A 104:10643–10648PubMedPubMedCentralCrossRefGoogle Scholar
  146. Schiraldi C, Giuliano MT, de Rosa M (2002) Perspectives on biotechnological applications of archaea. Archaea 1:75–86PubMedPubMedCentralCrossRefGoogle Scholar
  147. Schreck SD, Grunden AM (2014) Biotechnological applications of halophilic lipases and thioesterases. Appl Microbiol Biotechnol 98:1011–1021PubMedCrossRefPubMedCentralGoogle Scholar
  148. Schubert BA, Lowenstein TK, Timofeeff MN, Parker MA (2010) Halophilic cultured from ancient halite, Death Valley, California. Environ Microbiol 12(2):440–454Google Scholar
  149. Shand RF, Leyva KJ (2007) Peptide and protein antibiotics from the domain archaea: halocins and sulfolobicins. In: Riley MA, Chavan MA (eds) Bacteriocins: ecology and evolution. Springer, Berlin/Heidelberg/New York, pp 93–109CrossRefGoogle Scholar
  150. Shand RF, Leyva KJ (2008) Archaeal antimicrobials: an undiscovered country. In: Blum P (ed) Archaea: new models for prokaryotic biology. Caister Academic Press, Norfolk, pp 233–243Google Scholar
  151. Shimane Y, Hatada Y, Minegishi H, Echigo A, Nagaoka S, Miyazaki M, Ohta Y, Maruyama T, Usami R, Grant WD, Horikoshi K (2011) Salarchaeum japonicum gen. Nov., sp. nov., an aerobic, extremely halophilic member of the archaea isolated from commercial salt. Int J Syst Evol Microbiol 61:2266–2270PubMedCrossRefPubMedCentralGoogle Scholar
  152. Shimoshige H, Yamada T, Minegishi H, Echigo A, Shimane Y, Kamekura M, Itoh T, Usami R (2013) Halobaculum magnesiiphilum sp. nov., a magnesium dependent haloarchaeon isolated from commercial salt. Int J Syst Evol Microbiol 63:861–866PubMedCrossRefPubMedCentralGoogle Scholar
  153. Soppa J, Oesterhelt D (1989) Halobacterium sp. GRB: a species to work with!? Can J Microbiol 35(1):205–209PubMedCrossRefPubMedCentralGoogle Scholar
  154. Spudich JL, Luecke H (2002) Sensory rhodopsin II: functional insights from structure. Curr Opin Struct Biol 12:540–546PubMedCrossRefPubMedCentralGoogle Scholar
  155. Sun C, Li Y, Mei S, Lu Q, Zhou L, Xiang H (2005) A single gene directs both production and immunity of halocin C8 in a haloarchaeal strain AS7092. Mol Microbiol 57:537–549PubMedCrossRefPubMedCentralGoogle Scholar
  156. Syutkin AS, Pyatibratov MG, Fedorov OV (2014) Flagella of halophilic archaea: differences in supramolecular organization. Biochem Mosc 79:1470–1482CrossRefGoogle Scholar
  157. Tapingkae W, Tanasupawat S, Parkin KL, Benjakul S, Visessanguan W (2010) Degradation of histamine by extremely halophilic archaea isolated from high salt-fermented fishery products. Enzym Microb Technol 46:92–99CrossRefGoogle Scholar
  158. Taran M, Amirkhani H (2010) Strategies of poly(3-hydroxybutyrate) synthesis by Haloarcula sp. IRU1 utilizing glucose as a carbon source: optimization of culture conditions by Taguchi methodology. Int J Biol Macromol 47:632–634PubMedCrossRefPubMedCentralGoogle Scholar
  159. Thombre R, Joshi V, Oke R (2016) Halophiles: pharmaceutical potential and biotechnological applications. In: Thangadurai D, Sangeetha J (eds) Industrial biotechnology: sustainable production and bioresource utilization. Apple Academic Press, Waretown, pp 111–139CrossRefGoogle Scholar
  160. Torreblanca M, Meseguer I, Rodriguez-Valera F (1989) Halocin H6, a bacteriocin from H. gibbonsii. J Gen Microbiol 135:2655–2661Google Scholar
  161. Veldman A, Vahl HA (1994) Xylanase in broiler diets with differences in characteristics and content of wheat. Br Poult Sci 35:537–550PubMedCrossRefPubMedCentralGoogle Scholar
  162. Vílchez C, Forján E, Cuaresma M, Bédmar F, Garbayo I, Vega JM (2011) Marine carotenoids: biological functions and commercial applications. Mar Drugs 9:319–333PubMedPubMedCentralCrossRefGoogle Scholar
  163. Vitali B, Ndagijimana M, Cruciani F, Carnevali P, Candela M, Guerzoni ME, Brigidi P (2010) Impact of a synbiotic food on the gut microbial ecology and metabolic profiles. BMC Microbiol 10:4PubMedPubMedCentralCrossRefGoogle Scholar
  164. Vsevolodov NN, Dyukova TV (1994) Retinal-protein complexes as optoelectronic components. Trends Biotechnol 12:81–88PubMedCrossRefPubMedCentralGoogle Scholar
  165. 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 186:3187–3194PubMedPubMedCentralCrossRefGoogle Scholar
  166. Wang Y, Yin J, Chen GQ (2014) Polyhydroxyalkanoates, challenges and opportunities. Curr Opin Biotechnol 30:59–65PubMedCrossRefPubMedCentralGoogle Scholar
  167. Woodward J, Wiseman A (1984) Topics in enzyme and fermentation biotechnology, vol 8. Wiley, New York, pp 9–30Google Scholar
  168. Yatsunami R, Ando A, Yang Y, Takaichi S, Kohno M, Matsumura Y, Ikeda H, Fukui T, Nakasone K, Fujita N, Sekine M, Takashina T, Nakamura S (2014) Identification of carotenoids from the extremely halophilic archaeon Haloarcula japonica. Front Microbiol 5:100–105PubMedPubMedCentralCrossRefGoogle Scholar
  169. Yin J, Chen JC, Wu Q, Chen GQ (2015) Halophiles, coming stars for industrial biotechnology. Biotechnol Adv 33(7):1433–1442PubMedCrossRefPubMedCentralGoogle Scholar
  170. Zafrilla B, Martınez-Espinosa RM, Esclapez J, Perez-Pomares F, Bonete MJ (2010) SufS protein from Haloferax volcanii involved in Fe-S cluster assembly in haloarchaea. Biochim Biophys Acta 1084:1476–1482CrossRefGoogle Scholar
  171. Zhang T, Datta S, Eichler J, Ivanova N, Axen SD, Kerfeld CA, Chen F, Kyrpides N, Hugenholtz P, Cheng J-F, Sale KL, Simmons B, Rubin E (2011) Identification of a haloalkaliphilic and thermostable cellulase with improved ionic liquid tolerance. Green Chem 13:2083–2090CrossRefGoogle Scholar
  172. Zhang J, Sun Z, Sun P, Chen T, Chen F (2014) Microalgal carotenoids: beneficial effects and potential in human health. Food Funct 5:413–425PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Vijay Kumar
    • 1
  • Santosh Kumar Tiwari
    • 1
  1. 1.Department of GeneticsMaharshi Dayanand UniversityRohtakIndia

Personalised recommendations