Gluconeotrehalose is the principal organic solute in the psychrotolerant bacterium Carnobacterium strain 17-4

Springer Science and Business Media LLC - Tập 15 - Trang 463-472 - 2011
Pedro Lamosa1,2, Ana I. Mingote1, Tatiana Groudieva3, Barbara Klippel3, Ksenia Egorova3, Dina Jabbour3, Helena Santos, Garabed Antranikian3
1Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal
2Centro de Ressonância Magnética António Xavier, ITQB-UNL, Oeiras, Portugal
3Institute of Technical Microbiology, Hamburg University of Technology, Hamburg, Germany

Tóm tắt

A high proportion of microorganisms that colonise cold environments originate from marine sites; hence, they must combine adaptation to low temperature with osmoregulation. However, little or nothing is known about the nature of compatible solutes used by cold-adapted organisms to balance the osmotic pressure of the external medium. We studied the intracellular accumulation of small organic solutes in the Arctic isolate Carnobacterium strain 17-4 as a function of the growth temperature and the NaCl concentration in the medium. Data on 16S rDNA sequence and DNA–DNA hybridisation tests corroborate the assignment of this isolate as a new species of the bacterial genus Carnobacterium. The growth profiles displayed maximal specific growth rate at 30°C in medium without NaCl, and maximal values of final biomass at growth temperatures between 10 and 20°C. Therefore, Carnobacterium strain 17-4 exhibits halotolerant and psychrotolerant behaviours. The solute pool contained glycine-betaine, the main solute used for osmoregulation, and an unknown compound whose structure was identified as α-glucopyranosyl-(1-3)-β-glucopyranosyl-(1-1)-α-glucopyranose (abbreviated as gluconeotrehalose), using nuclear magnetic resonance and mass spectrometry. This unusual solute consistently accumulated to high levels (0.35 ± 0.05 mg/mg cell protein) regardless of the growth temperature or salinity. The efficiency of gluconeotrehalose in the stabilisation of four model enzymes against heat damage was also assessed, and the effects were highly protein dependent. The lack of variation in the gluconeotrehalose content observed under heat stress, osmotic stress, and starvation provides no clue for the physiological role of this rare solute.

Tài liệu tham khảo

Biniukov VI, Kharatian EF, Ostrovsky DN, Shashkov AS (1989) Derivatives of glutamic acid and trehalose which can be transformed into long-living free radicals by the loss of an electron are identified in some bacteria. Biofactors 2:95–97

Borges N, Ramos A, Raven ND, Sharp RJ, Santos H (2002) Comparative study of the thermostabilizing properties of mannosylglycerate and other compatible solutes on model enzymes. Extremophiles 6:209–216

Brown AD (1976) Microbial water stress. Bacteriol Rev 40:803–846

Buchholz-Cleven BEE, Rattunde B, Straub KL (1997) Screening for genetic diversity of isolates of anaerobic Fe(II)-oxidizing bacteria using DGGE and whole-cell hybridization. System Appl Microbiol 20:301–309

Carbonero ER, Sassaki GL, Stuelp PM, Gorin PA, Woranovicz-Barreira SM, Iacomini M (2001) Comparative studies of the polysaccharides isolated from lichenized fungi of the genus Cladonia: significance as chemotypes. FEMS Microbiol Lett 194:65–69

Cavicchioli R (2006) Cold-adapted archaea. Nat Rev Microbiol 4:331–343

Cavicchioli R, Thomas T, Curmi PM (2000) Cold stress response in Archaea. Extremophiles 4:321–331

Costa J, Empadinhas N, Gonçalves L, Lamosa P, Santos H, da Costa MS (2006) Characterization of the biosynthetic pathway of glucosylglycerate in the archaeon Methanococcoides burtonii. J Bacteriol 188:1022–1030

D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389

da Costa MS, Santos H, Galinski EA (1998) An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Adv Biochem Eng Biotechnol 61:117–153

de Virgilio C, Hottiger T, Dominguez J, Boller T, Wiemken A (1994) The role of trehalose synthesis for the acquisition of thermotolerance in yeast. Genetic evidence that trehalose is a thermoprotectant. Eur J Biochem 219:179–186

Dudman NP, Zerner B (1975) Carboxylesterases from pig and ox liver. Meth Enzymol 35:190–208

Erickson A, Deibel RH (1973) Turbidimetric assay of staphylococcal nuclease. Appl Microbiol 25:337–341

Esch SW, Morton MD, Williams TD, Buller CS (1999) A novel trisaccharide glycolipid biosurfactant containing trehalose bears ester-linked hexanoate, succinate, and acyloxyacyl moieties: NMR and MS characterization of the underivatized structure. Carbohydr Res 319:112–123

Faria TQ, Lima JC, Bastos M, Maçanita AL, Santos H (2004) Protein stabilization by osmolytes from hyperthermophiles: effect of mannosylglycerate on the thermal unfolding of recombinant nuclease a from Staphylococcus aureus studied by picosecond time-resolved fluorescence and calorimetry. J Biol Chem 279:48680–48691

Faria TQ, Mingote A, Siopa F, Ventura R, Maycock C, Santos H (2008) Design of new enzyme stabilizers inspired by glycosides of hyperthermophilic microorganisms. Carbohydr Res 343:3025–3033

Fisher W, Krieglstein J (1966) A new glucotriose, isolated from Streptococcus faecalis. Hoppe Seylers Z Physiol Chem 344:113–123

Groudieva T, Kambourova M, Yusef H, Royter M, Grote R, Trinks H, Antranikian G (2004) Diversity and cold-active hydrolytic enzymes of culturable bacteria associated with Arctic sea ice, Spitzbergen. Extremophiles 8:475–488

Hendrix DL, Salvucci ME (2001) Isobemisiose: an unusual trisaccharide abundant in the silver leaf whitefly, Bemisia argentifolii. J Insect Physiol 47:423–432

Hottiger T, Schmutz P, Wiemken A (1987) Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J Bacteriol 169:5518–5522

Jorge CD, Lamosa P, Santos H (2007) Alpha-d-mannopyranosyl-(1→2)-alpha-d-glucopyranosyl-(1→2)-glycerate in the thermophilic bacterium Petrotoga miotherma—structure, cellular content and function. FEBS J 274:3120–3127

Kandror O, DeLeon A, Goldberg AL (2002) Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99:9727–9732

Lamosa P, Martins LO, Da Costa MS, Santos H (1998) Effects of temperature, salinity, and medium composition on compatible solute accumulation by Thermococcus spp. Appl Environ Microbiol 64:3591–3598

Lamosa P, Burke A, Peist R, Huber R, Liu M-Y, Silva G, Rodrigues-Pousada C, LeGall J, Maycock C, Santos H (2000) Thermostabilization of proteins by diglycerol phosphate, a new compatible solute from the hyperthermophile Archaeoglobus fulgidus. Appl Environ Microbiol 66:1974–1979

Lamosa P, Turner DL, Ventura R, Maycock C, Santos H (2003) Protein stabilization by compatible solutes. Effect of diglycerol phosphate on the dynamics of Desulfovibrio gigas rubredoxin studied by NMR. Eur J Biochem 270:4606–4614

Lippert K, Galinski EA (1992) Enzyme stabilization by ectoine-type compatible solutes: protection against heating, freezing and drying. Appl Microbiol Biotechnol 37:61–65

Martins LO, Santos H (1995) Accumulation of mannosylglycerate and di-myo-inositol-phosphate by Pyrococcus furiosus in response to salinity and temperature. Appl Environ Microbiol 61:3299–3303

Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G + C content of deoxyribonucleic acid by high performance liquid chromatography. Int J Syst Bacteriol 39:159–167

Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39:144–167

Ohta M, Pan YT, Laine RA, Elbein AD (2002) Trehalose-based oligosaccharides isolated from the cytoplasm of Mycobacterium smegmatis. Relation to trehalose-based oligosaccharides attached to lipid. Eur J Biochem 269:3142–3149

Pikuta EV, Hoover RB, Tang J (2007) Microbial extremophiles at the limits of life. Crit Rev Microbiol 33:183–209

Ramos A, Raven NDH, Sharp RJ, Bartolucci S, Rossi M, Cannio R, Lebbink J, van der Oost J, de Vos WM, Santos H (1997) Stabilization of enzymes against thermal stress and freeze-drying by mannosylglycerate. Appl Environ Microbiol 63:4020–4025

Santos H, da Costa MS (2001) Organic solutes from thermophiles and hyperthermophiles. Meth Enzymol 334:302–315

Santos H, Lamosa P, Borges N, Gonçalves LG, Pais TM, Rodrigues MV (2011) Organic compatible solutes of prokaryotes that thrive in hot environments: the importance of ionic compounds for thermostabilization. In: Horikoshi K, Antranikian G, Bull AT, Robb FT, Stetter KO (eds) Extremophiles handbook, Part 4. Springer, Tokyo, pp 497–520

Sanz ML, González M, de Lorenzo C, Sanz J, Martínez-Castro I (2004) Carbohydrate composition and physico chemical properties of artisanal honeys from Madrid (Spain): occurrence of Echium sp. honey. J Sci Food Agric 84:1577–1584

Shugar D (1952) The measurement of lysozyme activity and the ultra-violet inactivation of lysozyme. Biochim Biophys Acta 8:302–309

Swallow KW, Low NH (1990) Analysis and quantitation of the carbohydrates in honey using high-performance liquid chromatography. J Agric Food Chem 38:1828–1832

Tamaoka J, Komagata K (1984) Determination of DNA base composition by reverse-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128

Thomas T, Kumar N, Cavicchioli R (2001) Effects of ribosomes and intracellular solutes on activities and stabilities of elongation factor 2 proteins from psychrotolerant and thermophilic methanogens. J Bacteriol 183:1974–1982

Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

Winkler UK, Stuckmann M (1979) Glycogen, hyaluronate, and some other polysaccharides greatly enhance the formation of exolipase by Serratia marcescens. J Bacteriol 138:663–670

Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, van der Heide T, Smith LT (2001) Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol A Mol Integr Physiol 130:437–460

Yoshikatsu M, Takashi S, Hiroto C (1996) Process for preparing neotrehalose and its uses. European patent no EP0486315

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Springer Science and Business Media LLC

Tập 15

463-472

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