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Halomonas maura is a physiologically versatile bacterium of both ecological and biotechnological interest

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Abstract

Halomonas maura is a bacterium of great metabolic versatility. We summarise in this work some of the properties that make it a very interesting microorganism both from an ecological and biotechnological point of view. It plays an active role in the nitrogen cycle, is capable of anaerobic respiration in the presence of nitrate and has recently been identified as a diazotrophic bacterium. Of equal interest is mauran, the exopolysaccharide produced by H. maura, which contributes to the formation of biofilms and thus affords the bacterium advantages in the colonisation of its saline niches. Mauran is highly viscous, shows thixotropic and pseudoplastic behaviour, has the capacity to capture heavy metals and exerts a certain immunomodulator effect in medicine. All these attributes have prompted us to make further investigations into its molecular characteristics. To date we have described 15 open reading frames (ORF’s) related to exopolysaccharide production, nitrogen fixation and nitrate reductase activity among others.

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References

  • Afendra A.S., Vargas C., Nieto J.J., Drainas C. (2004). Gene transfer and expression of recombinat proteins in moderately halophilic bacteria. Methods Mol. Biol. 267: 209–223

    PubMed  CAS  Google Scholar 

  • Amellal N., Burtin G., Bartoli F., Heulin T. (1998). Colonization of wheat roots by an exopolysaccharide-producing Pantoea agglomerans strain and its effect on rhizosphere soil aggregation. Appl. Environ. Microbiol. 64: 3740–3747

    PubMed  CAS  Google Scholar 

  • Anraku Y., Gennis R.B. (1987). The aerobic respiration chain of Escherichia coli. Trends Biochem. Sci. 12: 262–266

    Article  CAS  Google Scholar 

  • Arahal D.R., Ludwig W., Schleifer K.H., Ventosa A. (2002). Phylogeny of the family Halomonadaceae based on 23S and 16S rDNA sequence analyses. Int. J. Syst. Evol. Microbiol. 52: 241–249

    PubMed  CAS  Google Scholar 

  • Arco Y., Llamas I., Martínez-Checa F., Argandoña M., Quesada E., del Moral A. (2005). epsABCJ genes are involved in the biosynthesis of the exopolysaccharide mauran produced by Halomonas maura. Microbiology. 151: 2841–2851

    Article  PubMed  CAS  Google Scholar 

  • Argandoña A., Fernández-Carazo R., Llamas R., Martínez-Checa F., Caba J.M., Quesada E., del Moral A. (2005). The moderately halophilic bacterium Halomonas maura is a free-living diazotroph. FEMS Microbiol. Lett. 244: 69–74

    Article  PubMed  CAS  Google Scholar 

  • Argandoña M., Martínez-Checa F., Llamas I., Quesada E., del Moral A. (2003). Megaplasmids in Gram-negative, moderately halophilic bacteria. FEMS Microbiol. Lett. 227: 81–86

    Article  PubMed  CAS  Google Scholar 

  • Arias S., del Moral A., Ferrer M.R., Tallon R., Quesada E., Béjar V. (2003) Mauran, an exopolysaccharide produced by the halophilic bacterium Halomonas maura, with a novel composition and interesting properties for biotechnology. Extremophiles. 7: 319–326

    Article  PubMed  CAS  Google Scholar 

  • Arias S., Llamas I., Martínez-Checa F., Del Moral A., Ferrer M.R., Béjar V. and Quesada E. 2002. Halomonas maura TK26 (CECT 5720), un mutante que sintetiza con alto rendimiento el exopolisacárido maurano 26 de interés para la industria y el medio ambiente. No. P200202041. University of Granada (Spain)

  • Arvanitis N., Vargas C., Tegos G., Perysinakis A., Nieto J.J., Ventosa A., Drainas C. (1995). Development of a gene reporter system in moderately halophilic bacteria by employing the ice nucleation gene of Pseudomonas syringae. Appl. Environ. Microbiol. 61: 3821–3825

    PubMed  CAS  Google Scholar 

  • Barloy-Hubler F., Capela D., Barnett M., Kalman S., Federspie N.A., Long S.R., Galibert F. (2000). High-resolution physical map of the Sinorhizobium meliloti 1021 pSyma megaplasmid. J. Bacteriol. 182: 1185–1189

    Article  PubMed  CAS  Google Scholar 

  • Beck Von Bodman S., Bauer W.D., Coplin D.L. (2003). Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 41: 455–482

    Article  CAS  Google Scholar 

  • Beck Von Bodman S., Majerczak D.R., Coplin D.L. (1998). A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc. Natl. Acad. Sci. USA 95: 7687–7692

    Article  ADS  Google Scholar 

  • Béjar V., Llamas I., Calvo C., Quesada E. (1998). Characterization of exopolysaccharides produced by 19 halophilic strains of the species Halomonas eurihalina. J. Biotechnol. 61:135–141

    Article  Google Scholar 

  • Bott M., Preisig O., Hennecke H. (1992). Genes for a second terminal oxidase in Bradyrhizobium japonicum. Arch. Microbiol. 158: 335–343

    Article  PubMed  CAS  Google Scholar 

  • Bouchotroch S., Quesada E., del Moral A., Béjar V. (1999). Taxonomic study of exopolysaccharide-producing, moderately halophilic bacteria isolated from hypersaline environments in Morocco. Syst. Appl. Microbiol. 22: 412–419

    CAS  Google Scholar 

  • Bouchotroch S., Quesada E., del Moral A., Llamas I., Béjar V. (2001). Halomonas maura sp. nov., a novel moderately halophilic, exopolysaccharide-producing bacterium. Int. J. Syst. Evol. Microbiol. 5: 1625–1632

    Google Scholar 

  • Bouchotroch S., Quesada E., Izquierdo I., Rodríguez M., Béjar V. (2000). Bacterial exopolysaccharides produced by newly discovered bacteria belonging to the genus Halomonas, isolated from hypersaline habitats in Morocco. J. Ind. Microbiol. Biotechnol. 24: 374–378

    Article  CAS  Google Scholar 

  • Calvo C., Martínez-Checa F., Toledo F.L., Porcel J., Quesada E. (2002). Characteristics of bioemulsifiers synthesised in crude oil media by Halomonas eurihalina and their effectiveness in the isolation of bacteria able to grow in the presence of hydrocarbons. Appl. Microbiol. Biotechnol. 60: 347–351

    Article  PubMed  CAS  Google Scholar 

  • Cánovas D., Vargas C., Kneip S., Moron M.J., Ventosa A., Bremer E., Nieto J.J. (2000). Genes for the synthesis of the osmoprotectant glycine betaine from choline in the moderately halophilic bacterium Halomonas elongata DSM 3043, USA. Microbiology. 146:455–463

    PubMed  Google Scholar 

  • Cheng C., Jaunet A.M. (1992). Cryoscanning electron microscopy of microbial extracellular polysaccharides and their association with minerals. Scanning. 14: 360–364

    Google Scholar 

  • Cornwell J.C., Kemp W.M., Kana T. (1999). Denitrification in coastal ecosystems methods environmental control, and ecosystem level controls, a review. Aquat. Ecol. 33: 41–54

    Article  CAS  Google Scholar 

  • Coronado M.J., Vargas C., Mellado E., Tegos G., Drainas C., Nieto J.J., Ventosa A. (2000). The α-amylase gene amyH of the moderate halophile Halomonas meridiana: cloning and molecular characterization. Microbiology 146: 861–868

    PubMed  CAS  Google Scholar 

  • Costernon J.W., Cheng K.-J., Geesy G.G., Ladd T.I., Nickel J.G., Dasgupta M., Marrie T.J. (1987) Bacterial biofilms in nature and disease. Annu. Rev. Microbiol. 41: 435–464

    Article  Google Scholar 

  • Davey M.E., O’Toole G.A. (2000). Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64: 847–867

    Article  PubMed  CAS  Google Scholar 

  • Davies D.G., Parsek M.R., Pearson J.P., Iglewski B.H., Costerton J.W., Greenberg E.P. (1998). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295–298

    Article  PubMed  CAS  ADS  Google Scholar 

  • de Kievit T.R., Iglewski B.H. (2000). Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 68: 4839–4849

    Article  PubMed  Google Scholar 

  • Dobson S.J., Franzmann D. (1996). Unification of the genera Deleya (Barman et al. 1983), Halomonas (Vreeland et al. 1980) and Halovibrio (Fendrich, 1988) and the species Paracoccus halodenitrificans (Robinson and Gibons 1952) into a single genus, Halomonas, and placement of the genus Zymobacter in the family Halomonadaceae. Int. J. Syst. Bacteriol 46: 550–558

    CAS  Google Scholar 

  • Farrand S.K. (1998). Conjugation in Rhizobiaceae. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds), The Rhizobiaceae, Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic, Dordrecht, pp 199–233

    Google Scholar 

  • Fernández-Castillo R., Vargas C., Nieto J.J., Ventosa A., Ruiz-Berraquero F. (1992). Characterization of a plasmid from moderately halophilic eubacteria. J. Gen. Microbiol. 138: 1133–1137

    PubMed  Google Scholar 

  • Flanagan D.A., Gregory L.G., Carter P., Karacas-Sen A., Richardson D.J., Spiro S. (1999). Detection of genes for periplasmic nitrate reductase in nitrate respiring bacteria and in community DNA. FEMS Microbiol. Lett. 177: 263–270

    PubMed  CAS  Google Scholar 

  • Fuqua C., Parsek M.R., Greenberg E.P. (2001). Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 35: 439–468

    Article  PubMed  CAS  Google Scholar 

  • Fuqua W.C., Winans S.C., Greenberg E.P. (1994). Quorum sensing in bacteria: the LuxR–LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 176: 269–275

    PubMed  CAS  Google Scholar 

  • García M.T., Mellado E., Ostos J.C., Ventosa A. (2004). Halomonas organivorans sp. nov., a moderate halophile able to degrade aromatic compounds. Int. J. Syst. Evol. Microbiol. 54: 1723–1728

    Article  PubMed  CAS  Google Scholar 

  • González J.E., York G.M., Walker G.C. (1996). Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function. Gene. 179: 141–146

    Article  PubMed  Google Scholar 

  • Hammer B.K., Bassler B.L. (2003). Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50: 101–114

    Article  PubMed  CAS  Google Scholar 

  • Jones B.E. (2004). Industrial enzymes: do halophilic and alkaliphiles have a role to play?. In: Ventosa A (eds). Halophilic Microorganisms Springer Verlang, Heildeberg, pp. 275 – 284

    Google Scholar 

  • Kushner D.J., Kamekura M. (1988). Physiology of halophilic eubacteria. In: Rodriguez-Valera F. (eds). Halophilic Bacteria, Vol 1. CRC Press, Boca Raton FL, pp 109 – 138

    Google Scholar 

  • Llamas I., del Moral A., Béjar V., Girón M.D., Salto R., Quesada E. (1997). Plasmids from Halomonas eurihalina, a microorganism which produces an exopolysaccharide of biotechnological interest. FEMS Microbiol. Lett. 156: 251–257

    CAS  Google Scholar 

  • Llamas I., Quesada E., Martínez-Cánovas M.J., Gronquist M., Eberhard A., González J.E. (2005). Quorum sensing in halophilic bacteria: detection of N-acyl-homoserine lactones in the exopolysaccharide-producing species of Halomonas. Extremophiles. 9:333–341

    Article  PubMed  CAS  Google Scholar 

  • Llamas I., Sánchez M.J., Argandoña M., Béjar V., Quesada E., del Moral A. (2002). Analysis of the genome of the moderate halophile Halomonas eurihalina. Curr. Microbiol. 45: 233–239

    Article  PubMed  CAS  Google Scholar 

  • Llamas I., Suárez A., Quesada E., Béjar V., del Moral A. (2003). Identification and characterization of the carAB genes responsible for encoding carbamoylphosphate synthetase in Halomonas eurihalina. Extremophiles 7: 205–211

    PubMed  CAS  Google Scholar 

  • Louis P., Galinski E.A. (1997). Characterization of genes for the biosynthesis of the compatible solute ectoine from Marinococcus halophilus and osmoregulated expression in Escherichia coli. Microbiology 143: 1141–1149

    PubMed  CAS  Google Scholar 

  • Lynch M.J., Swift S., Kirke D.F., Keevil C.W., Dodd C.E.R., Williams P. (2002). The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ. Microbiol. 4: 18–28

    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 

  • Marketon M.M., Glenn S.A., Eberhard A., González J.E. (2003). Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J. Bacteriol. 185: 325–331

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Cánovas M.J., Béjar V., Martínez-Checa F., Quesada E. (2004a). Halomonas anticariensis sp. nov. from Fuente de Piedra a saline-wetland wild-fowl reserve and natural habitats of flamingos in Málaga (S. Spain). Int. J. Syst. Evol. Microbiol. 54:1329–1332

    Article  CAS  Google Scholar 

  • Martínez-Cánovas M.J., Quesada E., Llamas I., Béjar V. (2004b). Halomonas ventosae sp. nov., a moderately halophilic denitrifying exopolysaccharide-producing bacterium. Int. J. Syst. Evol. Microbiol. 54:733–737

    Article  CAS  Google Scholar 

  • Martínez–Cánovas M.J., Quesada E., Martínez-Checa F., Béjar V. (2004c). A taxonomic study to establish the relationship between exopolysaccharide-producing bacterial strains living in diverse hypersaline habitats. Curr. Microbiol. 48: 348–335

    Article  CAS  Google Scholar 

  • Martínez-Checa F., Béjar V., Martínez-Cánovas, J., Llamas I. and Quesada E. 2005. Halomonas almeriensis sp. nov., a moderately halophilic, exopolysaccharide-producing bacterium from Cabo de Gata, Almería, south-east Spain

  • Martínez-Checa F., Toledo F.L., Vilchez R., Quesada E., Calvo C. (2002). Yield production, chemical composition, and functional properties of emulsifier H28 synthesized by Halomonas eurihalina strain H-28 in media containing various hydrocarbons. Appl. Microbiol. Biotechnol. 58: 358–363

    Article  PubMed  CAS  Google Scholar 

  • Martins L.O., Sá-Correia I. (1993). Temperature profiles of gellan synthesis activities of biosynthetic enzymes. Biotechnol. Appl. Biochem. 20: 385–395

    Google Scholar 

  • Mata J.A., Martínez-Cánovas M.J., Quesada E., Béjar V. (2002). A detailed phenotypic characterization of the type strains of Halomonas species. Syst. Appl. Microbiol. 25: 360–375

    Article  PubMed  CAS  Google Scholar 

  • McClean K.H., Winson M.K., Fish L., Taylor A., Chhabra S.R., Camara M. Daykin M., Lamb J.H., Swift S., Bycroft B.W., Stewart G.S., Williams P. (1997). Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acyl homoserine lactones. Microbiology 143: 3703–3711

    PubMed  CAS  Google Scholar 

  • McNab R., Ford S.K., El-Sabaeny A., Barbieri B., Cook G.S., Lamont R.J. (2003). LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J. Bacteriol. 185: 274–284

    Article  PubMed  CAS  Google Scholar 

  • Mellado E., Garcia M.T., Roldan E., Nieto J.J., Ventosa A. (1998). Analysis of the genome of the Gram-negative moderate halophiles Halomonas and Chromohalobacter by using pulsed-field gel electrophoresis. Extremophiles 2: 435–438

    Article  PubMed  CAS  Google Scholar 

  • O‘Toole G.A., Kolter R. (1998). Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30: 295–304

    Article  PubMed  CAS  Google Scholar 

  • Oren A. (1999). Microbiology and Biogeochemistry of Hypersaline Environments. CRC Press, Boca Raton FL

    Google Scholar 

  • Oren A. (2002). Halophilic Microorganisms and their Environments. Kluwer Academic Publisher, Dorderecht

    Google Scholar 

  • Patrick O., Slawayk G., García N., Borin P. (1996). Evidence of denitrification and nitrate ammonification in sediments of two coastal lagoons in southern France. Hidrobiología 329:133–141

    Article  Google Scholar 

  • Quesada E., Valderrama M.J., Béjar V., Ventosa A., Gutiérrez M.C., Ruiz-Berraquero F., Ramos-Cormenzana A. (1990). Volcaniella eurihalina gen. nov., sp. nov., a moderately halophilic nonmotile Gram-negative rod. Int. J. Syst. Bacteriol. 40: 261–267

    CAS  Google Scholar 

  • Quesada E., Béjar V., Ferrer M.R., Calvo C., Llamas I., Martínez-Checa F., Arias A., Ruíz-Garcia C., Páez R., Martínez-Canovas M.J., del Moral A. (2004). Moderately halophilic, exopolysaccharide-producing bacteria. In: Ventosa A (eds). Halophilic Microorganisms. Springer Verlang, Heildeberg, pp. 297–314

    Google Scholar 

  • Ramos-Cormenzana A. (1993). Ecology of moderately halophilic bacteria. In: Vreeland R.H., Hochstein L.I. (eds). The Biology of Halophilic Bacteria. CRC Press, Inc., Boca Raton, FL, pp. 55–86

    Google Scholar 

  • Robertson E., Firestone M. (1992). Relationship between dessication and exopolysaccharide production in soil Pseudomonas sp. Appl. Environ. Microbiol. 58: 1284–1291

    Google Scholar 

  • Rodríguez-Valera F. (1993). Introduction to saline environments. In: Vreeland R.H., Hochstein L.I. (eds). The Biology of Halophilic Bacteria. CRC Press, Inc., Boca Raton, FL, pp. 1–23

    Google Scholar 

  • Skvortsov I.M., Ignatov V.V. (1998). Extracellular polysaccharides and polysaccharide – containing biopolymers from Azospirillum species: properties and the possible role in interaction with plants roots. FEMS Microbiol. Lett. 165: 223–229

    PubMed  CAS  Google Scholar 

  • Sutherland I.W. (2001). Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147: 3–9

    PubMed  CAS  Google Scholar 

  • Taghavi S., Mergeay M., Van der Lelie D. (1997). Genetic and physical map of the Alcaligenes euthropus CH34 megaplasmid pMOL28 and its derivative pMOL50 obtained after temperature induced mutagenesis and mortality. Plasmid 37: 22–34

    Article  PubMed  CAS  Google Scholar 

  • Tegos G., Vargas C., Perysinakis A., Koukkou A.I., Christogianni A., Nieto J.J., Ventosa A., Drainas C. (2000). Release of cell-free ice nuclei from Halomonas elongata expressing the ice nucleation gene inaZ of Pseudomonas syringae. J. Appl. Microbiol. 89: 785–792

    Article  PubMed  CAS  Google Scholar 

  • Tobias C.R., Anderson I.C., Camel A.C., Macko S.A. (2001). Nitrogen cycling through a fringing marsh-aquifer ecotone. Mar. Ecol. Prog. Ser. 210: 25–39

    CAS  Google Scholar 

  • Tripathi A.K., Nagarajan T., Verma S.C., Le Rudulier D. (2002). Inhibition of biosynthesis and activity of nitrogenase in Azospirillum brasilense Sp7 under salinity stress. Curr. Microbiol. 44: 363–367

    Article  PubMed  CAS  Google Scholar 

  • Vargas C., Fernández-Castillo R., Cánovas D., Ventosa A., Nieto J.J. (1995). Isolation of cryptic plasmids from moderately halophilic eubacteria of the genus Halomonas. Characterization of a small plasmid fromH. elongata and its use for shuttle vector construction. Mol. Gen. Genet. 246: 411–418

    Article  PubMed  CAS  Google Scholar 

  • Vartak N.B., Lin C.C., Cleary J.M., Fagan M.J., Saier Jr. M.H. (1995). Glucose metabolism in Shingomonas elodea: pathway engineering via construction of a glucose-65-phosphate dehydrogenase insertion mutant. Microbiology 141: 2339–2350

    Article  PubMed  CAS  Google Scholar 

  • Ventosa A., Nieto J.J., Oren A. (1998). Biology of moderately halophilic aerobic bacteria. Microbiol. Mol. Rev. 62: 504–544

    CAS  Google Scholar 

  • Vreeland R.H., Litchfield C.D., Martin E.L., Elliot E. (1980). Halomonas elongata, a new genus and species of extremely salt-tolerant bacteria. Int. J. Syst. Bacteriol. 30: 485–495

    Article  CAS  Google Scholar 

  • Williams P., Stewart G.S.A.B. (1994). Cell density dependent control of gene expression in bacteria-implications for biofilm development and control. In: Wimpenny J, Nichols W, Stickler D, Lappin-Scott H (eds). Bacterial Biofilms and their Control in Medicine and Industry. Bioline, Cardiff, pp. 9–12

    Google Scholar 

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Acknowledgements

This research was supported by grants from the Dirección General de Investigación Científica y Técnica (BOS2003–00498) and from the Plan Andaluz de Investigación, Spain. Thanks go to our colleague Dr. J. Trout for revising our English text.

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  1. Department of Microbiology, University of Granada, Campus Universitario de Cartuja s/n, 18071, Granada, Spain

    Inmaculada Llamas, Ana del Moral, Fernando Martínez-Checa, Yolanda Arco, Soledad Arias & Emilia Quesada

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  1. Inmaculada Llamas
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  2. Ana del Moral
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Correspondence to Ana del Moral.

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Llamas, I., Moral, A.d., Martínez-Checa, F. et al. Halomonas maura is a physiologically versatile bacterium of both ecological and biotechnological interest. Antonie Van Leeuwenhoek 89, 395–403 (2006). https://doi.org/10.1007/s10482-005-9043-9

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