Abstract
An inverse linear relationship (P < 0.01) was detected between the cell surface hydrophobicity (CSH) and survival of ethanologenic bacteria Zymomonas mobilis 113S exposed to elevated (2.55 M) ethanol concentration. In the same way, viable cell counts of relatively hydrophobic Z. mobilis were less diminished by growing (0.85–3.40 M) ethanol concentrations as compared to more hydrophobic bacteria. Very similar inverse relationships (P < 0.01) were observed between the CSH of intact Z. mobilis and survival of cells subjected to subsequent freeze-drying or freezing/thawing cycles thereby affinity substantially lowered ability of hydrophobic bacteria to survive under adverse environments. Observed relationships were supported by significant correlations between independent analytical data of the carbohydrate content within fractions of lipopolysaccharide and surface proteins extracted from cells of varied hydrophobicity. The results suggest that the CSH could be of value to predict the ability of intact bacteria to endure stress conditions and should be monitored towards lower values during cultivation in order to reduce subsequent unwanted structural and physiological disturbances provoked by multiple stress factors.
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References
Aono R, Kobayashi H (1997) Cell surface properties of organic solvent-tolerant mutants of Escherichia coli K-12. Appl Environ Microbiol 63:3637–3642
Bekers M, Shvinka J, Pankova L, Laivenieks M, Mezhbarde I (1990) A simultaneous sucrose bioconversion into ethanol and levan by Zymomonas mobilis. Appl Biochem Biotechnol 24(25):265–274. doi:10.1007/BF02920251
Bekers M, Shvinka J, Raipulis J, Laivenieks M, Pankova L, Mezhbarde I (1993) Strain Zymomonas mobilis—producent of levan. Latvian Patent LV 5709
Bekers M, Laivenieks M, Karsakevich A, Ventina E, Kaminska E, Upite D et al (2001) Levan-ethanol biosynthesis using Zymomonas mobilis cells immobilized by attachment and entrapment. Process Biochem 36:979–986. doi:10.1016/S0032-9592(01)00140-6
Blyholder G, Adhikar C, Proctor A (1995) Structure and orientation of oleic acid absorbed onto silica gel. Congress infrared studies of surface and adsorbed species. ACS meeting N 208, Washington DC 105(1):151–158
Doelle HW, Kirk L, Crittenden R, Toh H, Doelle MB (1993) Zymomonas mobilis—science and industrial application. Crit Rev Biotechnol 13:57–98. doi:10.3109/07388559309069198
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356. doi:10.1021/ac60111a017
Dyé F, Delmotte FM (1997) Purification of a protein from Agrobacterium tumefaciens strain A348 that binds phenolic compounds. Biochem J 321:319–324
Geertsema-Doornbusch GI, van der Mei HC, Busscher HJ (1993) Microbial cell surface hydrophobicity. The involvement of electrostatic interactions in microbial adhesion to hydrocarbons (MATH). J Microbiol Methods 18:61–68. doi:10.1016/0167-7012(93)90072-P
Gunasekaran P, Chandra Raj K (1999) Ethanol fermentation technology—Zymomonas mobilis. Curr Sci 77(1):56–68
Hammarström S, Carlsson HE, Perlmann P, Svensson S (1971) Immunochemistry of the common antigen of enterobacteriaceae (kunin) relation to lipopolysaccharide core structure. J Exp Med 134(3):565–576. doi:10.1084/jem.134.3.565
Hobley TJ, Pamment NB (2004) Differences in response of Zymomonas mobilis and Saccharomyces cerevisiae to changes in extracellular ethanol concentration. Biotechnol Bioeng 43:155–158. doi:10.1002/bit.260430208
Ingram LO (1981) Mechanism of lysis of Escherichia coli by ethanol and other chaotropic agents. J Bacteriol 146(1):331–336
Karkhanis YD, Zeltner JY, Jackson JJ, Carlo DJ (1978) A new and improved microassay to determine 2-keto-3-deoxyoctonate in lipopolysaccharide of Gram-negative bacteria. Anal Biochem 85(2):595–601. doi:10.1016/0003-2697(78)90260-9
Leverette CL, Dluhy RA (2004) Vibrational characterization of a planar-supported model bilayer system utilizing surface-enhanced Raman scattering (SERS) and infrared reflection-absorption spectroscopy (IRRAS). Coll Surf A 243:157–167. doi:10.1016/j.colsurfa.2004.05.020
Lodowska J, Wolny D, Jaworska-Kik M, Weglarz L, Dzierzewicz Z, Wilczok T (2007) Interstrain diversity of 2-keto-3-deoxyoctonate content in lipopolysaccharides of Desulfovibrio desulfuricans. J Thromb Haemost 5(Suppl 1):08
Miyamoto-Shinohara Y, Sukenobe J, Imaizumi T, Nakahara T (2008) Survival of freeze-dried bacteria. J Gen Appl Microbiol 54:9–24. doi:10.2323/jgam.54.9
Montenecourt BS (1985) Zymomonas, a uniqe genus of bacteria. Biology of industrial micoorganisms.. The Benjamin/Cumings publishing company, California, pp 261–289
Naumann D (2002) Infrared spectroscopy in microbiology. In: Meyers RA (ed) Encyclopedia of analytical chemistry. Wiley, Chichester, pp 102–131
Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656. doi:10.1128/MMBR.67.4.593-656.2003
Nowak J (2000) Ethanol yield and productivity of Zymomonas mobilis in various fermentation methods. Elect J Pol Agric Univ Food Sci Technol 3(2):4
Osborn MJ, Gander JE, Parisi E, Carson J (1972) Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem 247(12):3962–3972
Osman YA, Ingram LO (1985) Mechanism of ethanol inhibition of fermentation in Zymomonas mobilis CP4. J Bacteriol 164:173–180
Panesar PS, Marwaha SS, Kennedy (2006) Zymomonas mobilis: an alternative ethanol producer. J Chem Technol Biotechnol 81:623–625
Pembrey RS, Marshall KC, Schmider RP (1999) Cell surface analysis techniques: what do cell preparation protocols do to cell surface properties? Appl Environ Microbiol 65(7):1877–1894
Piater LA (2005) Identification and characterization of mutagen activated protein kinases in leaf tissue of Nicotinia tabacum in response to elicitation by lipopolysaccharides. South Africa, Johannesburg, PhD thesis
Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58(4):755–805
Rogers PL, Jeon YJ, Lee KJ, Lawford HG (2007) Zymomonas mobilis for fuel ethanol and higher value products. Adv Biochem Eng Biotechnol 108:263–288
Rosenberg M, Doyle RJ (1990) Microbial cell surface hydrophobicity: history, measurement, and significance. In: Doyle RJ, Rosenberg M (eds) Microbial cell surface hydrophobicity. American Society for Microbiology, Washington, pp 1–37
Sedmak JJ, Grosberg SE (1997) A rapid, sensitive assay for protein using Comassie Brilliant blue G 250. Anal Biochem 79:544–552. doi:10.1016/0003-2697(77)90428-6
Sato K, Goto M, Yano J, Honda K, Kodali DR, Small DM (2001) Atomic resolution structure analysis of β′ polymorph crystal of a triacylglycerol: 1, 2-dipalmitoyl-3-myristoyl-sn-glycerol. J Lipid Res 42:338–345
Tornabene TG, Holzer G, Bittner AS, Grohmann K (1982) Characterization of the total extractable lipids of Zymomonas mobilis var. mobilis. Can J Microbiol 28:1107–1118
Tsonka UD, Todor D (2005) Anabiosis and conservation of microorganisms. J Cult Collect 4:17–28
Vanhaecke E, Remon JP, Moors M, Raes F, de Rudder D, van Peteghem A (1990) Kinetics of Pseudomonas aeruginosa adhesion to 304 and 316-L stainless steel: role of cell surface hydrophobicity. Appl Environ Microbiol 56:788–795
Venkataraman NV, Vasudevan S (2001) Hydrocarbon chain conformation in an intercalated surfactant monolayer and bilayer. J Chem Sci 113(5&6):539–558. doi:10.1007/BF02708789
Westphal O, Lüderitz O, Bister F (1952) Über die Extraction von Bacterien mit Phenol/Wasser. Z Naturforsch [B] 7b:148–155
Zikmanis P, Shakirova L, Auzina L, Andersone I (2007) Hydrophobicity of bacteria Zymomonas mobilis under varied environmental conditions. Process Biochem 42(4):745–750. doi:10.1016/j.procbio.2007.01.002
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This study was supported by the grant No. 04.1099 from the Latvian Council of Science.
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Shakirova, L., Auzina, L., Grube, M. et al. Relationship between the cell surface hydrophobicity and survival of bacteria Zymomonas mobilis after exposures to ethanol, freezing or freeze-drying. J Ind Microbiol Biotechnol 35, 1175–1180 (2008). https://doi.org/10.1007/s10295-008-0397-7
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DOI: https://doi.org/10.1007/s10295-008-0397-7