Review Topical Sections

Halophilic microorganism resources and their applications in industrial and environmental biotechnology

  • Received: 16 December 2015 Accepted: 28 February 2016 Published: 01 March 2016
  • Hypersaline environments are extreme habitats on the planet and have a diverse microbial population formed by halophilic microorganisms. They are considered to be actual or potential sources for discovery bioactive compounds, compatible solutes including novel and/or extraordinarily enzymes. To date, a number of bioactive compounds for the use in various fields of biotechnology which show assorted biological activities ranging from antioxidant, sunscreen and antibiotic actions have been reported. In addition, some halophilic microorganisms are capable of producing massive amounts of compatible solutes that are useful as stabilizers for biomolecules or stress-protective agents. The present review will impart knowledge and discuss on (i) potential biotechnological applications of bioactive compounds, compatible solutes and some novel hydrolytic enzymes; (ii) recent efforts on discovery and utilization of halophiles for biotechnological interest; (iii) future perspective of aforementioned points.

    Citation: Rungaroon Waditee-Sirisattha, Hakuto Kageyama, Teruhiro Takabe. Halophilic microorganism resources and their applications in industrial and environmental biotechnology[J]. AIMS Microbiology, 2016, 2(1): 42-54. doi: 10.3934/microbiol.2016.1.42

    Related Papers:

  • Hypersaline environments are extreme habitats on the planet and have a diverse microbial population formed by halophilic microorganisms. They are considered to be actual or potential sources for discovery bioactive compounds, compatible solutes including novel and/or extraordinarily enzymes. To date, a number of bioactive compounds for the use in various fields of biotechnology which show assorted biological activities ranging from antioxidant, sunscreen and antibiotic actions have been reported. In addition, some halophilic microorganisms are capable of producing massive amounts of compatible solutes that are useful as stabilizers for biomolecules or stress-protective agents. The present review will impart knowledge and discuss on (i) potential biotechnological applications of bioactive compounds, compatible solutes and some novel hydrolytic enzymes; (ii) recent efforts on discovery and utilization of halophiles for biotechnological interest; (iii) future perspective of aforementioned points.


    加载中
    [1] Oren A (2015) Halophilic microbial communities and their environments. Curr Opin Biotechnol 33: 119–124. doi: 10.1016/j.copbio.2015.02.005
    [2] Oren A (2014) Taxonomy of halophilic Archaea: current status and future challenges. Extremophiles 18: 825–834. doi: 10.1007/s00792-014-0654-9
    [3] Gunde-Cimerman N, Ramos J, Plemenitas A (2009) Halotolerant and halophilic fungi. Mycol Res 113: 1231–1241. doi: 10.1016/j.mycres.2009.09.002
    [4] Hosseini TA, Shariati M (2009) Dunaliella Biotechnology: methods and applications. J Appl Microbiol 107: 14–35. doi: 10.1111/j.1365-2672.2009.04153.x
    [5] Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62: 504–544.
    [6] Waditee R, Bhuiyan MN, Rai V, et al. (2005) Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proc Natl Acad Sci USA 102: 1318–1323. doi: 10.1073/pnas.0409017102
    [7] DasSarma S, DasSarma P (2015) Halophiles and their enzymes: negativity put to good use. CurrOpinMicrobiol 25: 120–126.
    [8] Arakawa T, Tokunaga M (2005) Electrostatic and hydrophobic interactions play a major role in the stability and refolding of halophilic proteins. Protein Pept Lett 11: 125–132.
    [9] DasSarma S, Berquist BR, Coker JA, et al. (2006) Post-genomics of the model haloarchaeon Halobacterium sp. NRC-1. Saline Systems. 2:3. doi: 10.1186/1746-1448-2-3
    [10] Hutcheon GW, Vasisht N, Bolhuis A (2005) Characterization of a highly stable alpha-amylase from the halophilic archaeon Haloarcula hispanica. Extremophiles 9: 487–495. doi: 10.1007/s00792-005-0471-2
    [11] Fukushima T, Mizuki T, Echigo A, et al. (2005) Organic solvent tolerance of halophilic alpha-amylase from a Haloarchaeon, Haloarcula sp. strain S-1. Extremophiles 9: 85–89. doi: 10.1007/s00792-004-0423-2
    [12] Waditee-Sirisattha R, Kageyama H, Sopun W, et al. (2014) Identification and upregulation of biosynthetic genes required for accumulation of Mycosporine-2-glycine under salt stress conditions in the halotolerant cyanobacterium Aphanothece halophytica. Appl Environ Microbiol 80: 1763–1769. doi: 10.1128/AEM.03729-13
    [13] Chen D, Feng J, Huang L, et al. (2014) Identification and characterization of a new erythromycin biosynthetic gene cluster in Actinopolyspora erythraea YIM90600, a novel erythronolide-producing halophilic actinomycete isolated from salt field. PLoS One 9:e108129. doi: 10.1371/journal.pone.0108129
    [14] Falb M, Müller K, Königsmaier L, et al. (2008) Metabolism of halophilic archaea. Extremophiles 12: 177–196. doi: 10.1007/s00792-008-0138-x
    [15] Oren A (2013) Salinibacter: an extremely halophilic bacterium with archaeal properties. FEMS Microbiol Lett 342: 1–9. doi: 10.1111/1574-6968.12094
    [16] Gammone MA, Riccioni G, D'Orazio N (2015) Marine carotenoids against oxidative stress: Effects on human health. Mar Drugs 13: 6226–6246. doi: 10.3390/md13106226
    [17] Alvarado C, Alvarez P, Jiménez L, et al. (2005) Improvement of leukocyte functions in young prematurely aging mice after a 5-week ingestion of a diet supplemented with biscuits enriched in antioxidants. Antioxid Redox Signal 7: 1203–1210. doi: 10.1089/ars.2005.7.1203
    [18] Jehlička J, Edwards HG, Oren A (2013) Bacterioruberin and salinixanthin carotenoids of extremely halophilic Archaea and Bacteria: a Raman spectroscopic study. Spectrochim Acta A Mol Biomol Spectrosc 106: 99–103. doi: 10.1016/j.saa.2012.12.081
    [19] Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28: 663–692. doi: 10.1039/c0np00036a
    [20] Christaki E, Bonos E, Giannenas I, et al. (2013) Functional properties of carotenoids originating from algae. J Sci Food Agric 93: 5–11. doi: 10.1002/jsfa.5902
    [21] Ohyanagi N, Ishido M, Suzuki F, et al. (2009) Retinoid ameliorates experimental autoimmune myositis, with modulation of the cell differentiation and antibody production in vivo. Arthritis Rheum 60: 3118–3127. doi: 10.1002/art.24930
    [22] Vachali P, Bhosale P, Bernstein PS (2012) Microbial carotenoids. Methods Mol Biol 898: 41–59. doi: 10.1007/978-1-61779-918-1_2
    [23] Shumskaya M, Wurtzel ET (2013) The carotenoid biosynthetic pathway: thinking in all dimensions. Plant Sci 208: 58–63. doi: 10.1016/j.plantsci.2013.03.012
    [24] Massyuk NP (1966) Mass culture of the carotene containing alga Dunaliella salina. Teod Ukr Bot Zh 23: 12–19.
    [25] Borowitzka MA (1999) Commercial production of microalgae: ponds, tanks, tubes and fermenters. J Biotechnol 70:313–321. doi: 10.1016/S0168-1656(99)00083-8
    [26] Hejazi MA, Holwerda E, Wijffels RH (2004) Milking microalga Dunaliella salina for -carotene production in two-phase bioreactors. Biotechnol Bioeng 85:475–481. doi: 10.1002/bit.10914
    [27] Wichuk K, Brynjólfsson S, Fu W (2014) Biotechnological production of value-added carotenoids from microalgae: Emerging technology and prospects. Bioengineered 5:204–208. doi: 10.4161/bioe.28720
    [28] Papaioannou EH, Kyriakides ML, Karabelas AJ (2015) Natural origin lycopene and its 'green' downstream processing. Crit Rev Food Sci Nutr. DOI:10.1080/10408398.2013.817381.
    [29] Hong ME, Choi YY, Sim SJ (2016) Effect of red cyst cell inoculation and iron (II) supplementation on autotrophic astaxanthin production by Haematococcus pluvialis under outdoor summer conditions. J Biotechnol 218: 25–33. doi: 10.1016/j.jbiotec.2015.11.019
    [30] Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9: 791-802. doi: 10.1038/nrmicro2649
    [31] Shick JM and Dunlap WC (2002) Mycosporine-like amino acids and related gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262. doi: 10.1146/annurev.physiol.64.081501.155802
    [32] Carreto JI, Carignan MO (2011) Mycosporine-like amino acids: relevant secondary metabolites. Chemical and ecological aspects. Mar Drugs 9: 387–446.
    [33] Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J Phycol 34: 418–430. doi: 10.1046/j.1529-8817.1998.340418.x
    [34] Nazifi E, Wada N, Yamaba M, et al. (2013) Glycosylated porphyra-334 and palythine-threonine from the terrestrial cyanobacterium Nostoc commune. Mar Drugs 11: 3124–3154. doi: 10.3390/md11093124
    [35] Matsui K, Nazifi E, Kunita S, et al. (2011) Novel glycosylated mycosporine-like amino acids with radical scavenging activity from the cyanobacterium Nostoc commune. J Photochem Photobiol B 105: 81–89. doi: 10.1016/j.jphotobiol.2011.07.003
    [36] Rastogi RP, Sinha RP, Moh SH, et al. (2014) Ultraviolet radiation and cyanobacteria. J Photochem Photobiol B 141: 154–169. doi: 10.1016/j.jphotobiol.2014.09.020
    [37] Llewellyn CA, White DA, Martinez-Vincente V, et al. (2012) Distribution of mycosporine-like amino acids along a surface water meridional transect of the Atlantic. Microb Ecol 64: 320–333. doi: 10.1007/s00248-012-0038-6
    [38] Rastogi RP, Richa, Sinha RP, et al. (2010) Photoprotective compounds from marine organisms. J Ind Microbiol Biotechnol 37: 537–358. doi: 10.1007/s10295-010-0718-5
    [39] Carreto JI, Carignan MO (2011) Mycosporine-like amino acids: relevant secondary metabolites. Chemical and ecological aspects. (2011) Mar Drugs 9: 387–446.
    [40] Volkmann M, Gorbushina AA, Kedar L, et al. (2006) Structure of euhalothece-362, a novel red-shifted mycosporine-like amino acid, from a halophiliccyanobacterium (Euhalothece sp.). FEMS Microbiol Lett 258: 50–54. doi: 10.1111/j.1574-6968.2006.00203.x
    [41] Oren A (1997) Mycosporine-like amino acids as osmotic solutes in a community of halophilic cyanobacteria. Geomicrobiol J 14:231–240. doi: 10.1080/01490459709378046
    [42] Ryu J, Park SJ, Kim IH, et al. (2014) Protective effect of porphyra-334 on UVA-induced photoaging in human skin fibroblasts. Int J Mol Med 34: 796–803.
    [43] Suh SS, Hwang J, Park M, et al. (2014) Anti-inflammation activities of mycosporine-like amino acids (MAAs) in response to UV radiation suggest potential anti-skin aging activity. Mar Drugs 12: 5174–5187. doi: 10.3390/md12105174
    [44] Torres A, Enk CD, Hochberg M, et al. (2006) Porphyra-334, a potential natural source for UVA protective sunscreens. PhotochemPhotobiolSci 5: 432–435.
    [45] Masaki K, Dunlap WC, Yamamoto Y, et al. (1996) Toyo Suisan Kaisha Pty. Ltd, Japanese Patent Application 9604230.
    [46] Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environment perspective. J Phycol 34: 418–430. doi: 10.1046/j.1529-8817.1998.340418.x
    [47] Hershkovitz N, Oren A, Cohen Y (1991) Accumulation of trehalose and sucrose in cyanobacteria exposed to matric water stress. Appl Environ Microbiol 57: 645–648.
    [48] Bolen DW, Baskakov IV (2001) Theosmophobic effect: natural selection of a thermodynamic force in protein folding. J Mol Biol 310:955–963. doi: 10.1006/jmbi.2001.4819
    [49] Hagemann M, Pade, N (2015) Heterosides - compatible solutes occurring in prokaryotic and eukaryotic phototrophs. Plant Biol 17: 927–934. doi: 10.1111/plb.12350
    [50] Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44: 357–384. doi: 10.1146/annurev.pp.44.060193.002041
    [51] Klahn S, Hagemann M (2011) Compatible solute biosynthesis in cyanobacteria. Environ Microbiol 13: 551–562. doi: 10.1111/j.1462-2920.2010.02366.x
    [52] Higo A, Katoh H, Ohmori K, et al. (2006) The role of a gene cluster for trehalose metabolism in dehydration tolerance of the filamentous cyanobacterium Anabaena sp. PCC 7120. Microbiology 152: 979–987.
    [53] Kolman MA, Nishi CN, Perez-Cenci M, et al. (2015) Sucrose in cyanobacteria: from a salt-response molecule to play a key role in nitrogen fixation. Life (Basel) 5: 102–126.
    [54] Hagemann M, Richter S, Mikkat S (1997) TheggtA gene encodes a subunit of the transport system for the osmoprotective compound glucosylglycerol in Synechocystis sp. strain PCC 6803. J Bacteriol 179: 714–720.
    [55] Fulda S, Mikkat S, Huang F, et al. (2006) Proteome analysis of salt stress response in the cyanobacterium Synechocystissp. strain PCC 6803. Proteomics 6: 2733–2745.
    [56] Ferjani A, Mustardy L, Sulpice R, et al. (2003) Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131: 1628–1637. doi: 10.1104/pp.102.017277
    [57] Klahn S, Hagemann M (2011) Compatible solute biosynthesis in cyanobacteria. Environ Microbiol 13: 551–562. doi: 10.1111/j.1462-2920.2010.02366.x
    [58] Goh F, Barrow KD, Burns BP, et al. (2010) Identification and regulation of novel compatible solutes from hypersalinestromatolite-associated cyanobacteria. Arch Microbiol 192: 1031–1038. doi: 10.1007/s00203-010-0634-0
    [59] Roberts MF, Lai MC, Gunsalus RP (1992) Biosynthetic pathways of the osmolytes N epsilon-acetyl-beta-lysine, beta-glutamine, and betaine in Methanohalophilus strain FDF1 suggested by nuclear magnetic resonance analyses. J Bacteriol 174:6688–6693.
    [60] Laloknam S, Tanaka K, Buaboocha T, et al. (2006) Halotolerant cyanobacterium Aphanothece halophytica contains a betaine transporter active at alkaline pH and high salinity. Appl Environ Microbiol 72:6018–6026. doi: 10.1128/AEM.00733-06
    [61] Lentzen G, Schwarz T (2006) Extremolytes: natural compounds from extremophiles for versatile applications. Appl Microbiol Biotechnol 72: 623–634. doi: 10.1007/s00253-006-0553-9
    [62] Graf R, Anzali S, Buenger J, et al. (2008) The multifunctional role of ectoine as a natural cell protectant. Clin Dermatol 26: 326–333. doi: 10.1016/j.clindermatol.2008.01.002
    [63] Beyer N, Driller H, Bünger J (2000) Ectoine - a innovative, multi-functional active substance for the cosmetic industry. Seifen ÖleFette Wachse J 126: 26–29.
    [64] Barth S, Huhn M, Matthey B, et al. (2000) Compatible-solute-supported periplasmic expression of functional recombinant proteins under stress conditions. Appl Environ Microbiol 66: 1572–1579. doi: 10.1128/AEM.66.4.1572-1579.2000
    [65] Kunte, HJ, Lentzen, G, Galinski, EA (2014) Industrial production of the cell protectant ectoine: protection mechanisms, processes, and products. Curr >B>iotechnol 3: 10–25.
    [66] Grammann, K, Volke, A, Kunte, HJ (2002) New type of osmoregulated solute transporter identified in halophilic members of the bacteria domain: TRAP transporter TeaABCmediates uptake of ectoine and hydroxyectoine in Halomonas elongata DSM 2581(T). J Bacteriol 184:3078–3085. doi: 10.1128/JB.184.11.3078-3085.2002
    [67] Schwibbert K, Marin-Sanguino A, Bagyan I, et al. (2011) A blueprint of ectoine metabolism from the genome of the industrial producer Halomonas elongata DSM 2581 T. Environ Microbiol 13:1973–1994. doi: 10.1111/j.1462-2920.2010.02336.x
    [68] Jaeger K-E, Eggert T (2002) Lipases for biotechnology. CurrOpinBiotechnol 13: 390–397.
    [69] Pérez-Pomares F, Bautista V, Ferrer J, et al. (2003) Amylase activity from the halophilic archaeon Haloferax mediterranei. Extremophiles 7: 299–306. doi: 10.1007/s00792-003-0327-6
    [70] Pérez-Pomares F, Díaz S, Bautista V, et al. (2009) Identification of several intracellular carbohydrate-degrading activities from the halophilic archaeon Haloferax mediterranei. Extremophiles 13: 633–641. doi: 10.1007/s00792-009-0246-2
    [71] Pérez D, Martín S, Fernández-Lorente G, et al. (2011) A novel halophilic lipase, LipBL, showing high efficiency in the production of eicosapentaenoic acid (EPA). PLoS One 6:e23325. doi: 10.1371/journal.pone.0023325
    [72] Amoozegar MA, Salehghamari E, Khajeh K, et al. (2008) Production of an extracellular thermohalophilic lipase from a moderately halophilic bacterium, Salinivibrio sp. strain SA-2. J Basic Microbiol 48: 160–167. doi: 10.1002/jobm.200700361
    [73] Karbalaei-Heidari HR, Amoozegar MA, Hajighasemi M, et al. (2009) Production, optimization and purification of a novel extracellular protease from the moderately halophilic bacterium Halobacillus karajensis. J Ind Microbio Biotechnol 36: 21–27. doi: 10.1007/s10295-008-0466-y
    [74] Dang H, Zhu H, Wang J, et al. (2009) Extracellular hydrolytic enzyme screening of culturable heterotrophic bacteria from deep-sea sediments of the Southern Okinawa Trough. World J Microbiol Biotechnol 25: 71–79. doi: 10.1007/s11274-008-9865-5
    [75] Moreno ML, Piubeli F, Bonfá MR, et al. (2012) Analysis and characterization of cultivable extremophilic hydrolytic bacterial community in heavy-metal-contaminated soils from the Atacama Desert and their biotechnological potentials. J Appl Microbiol 113: 550–559. doi: 10.1111/j.1365-2672.2012.05366.x
    [76] Hedlund BP, Dodsworth JA, Murugapiran SK, et al. (2014) Impact of single-cell genomics and metagenomics on the emerging view of extremophile "microbial dark matter". Extremophiles 18: 865–875. doi: 10.1007/s00792-014-0664-7
    [77] López-Pérez M, Ghai R, Leon MJ, et al. (2013) Genomes of "Spiribacter", a streamlined, successful halophilic bacterium. BMC Genomics 14: 787. doi: 10.1186/1471-2164-14-787
    [78] Yakovleva I, Bhagooli R, Takemura A, et al. (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. CompBiochem Physiol B 139:721–730. doi: 10.1016/j.cbpc.2004.08.016
    [79] Helbling EW, Chalker BE, Dunlap WC, et al. (1996) Photoacclimation of Antarctic marine diatoms to solar ultraviolet radiation. J Exp Mar Biol Ecol 204:85–101. doi: 10.1016/0022-0981(96)02591-9
    [80] Vale P (2015) Effects of light and salinity stresses in production of mycosporine-like amino acids by Gymnodinium catenatum(dinophyceae). Photochem Photobiol 91:1112–1122. doi: 10.1111/php.12488
  • Reader Comments
  • © 2016 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(10103) PDF downloads(2227) Cited by(54)

Article outline

Figures and Tables

Tables(1)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog