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BY-NC-ND 3.0 license Open Access Published by De Gruyter Open Access December 1, 2007

Excess turbulence as a cause of turbohypobiosis in cultivation of microorganisms

  • Maris Rikmanis EMAIL logo , Andrejs Berzinš and Uldis Viesturs
From the journal Open Life Sciences

Abstract

The present review describes the influence of different types of mixing systems under excess turbulence conditions on microorganisms. Turbohypobiosis phenomena were described by applying a method for measurement of the kinetic energy of flow fluctuations based on the piezoeffect. It can be assumed that the shear stress effect (the state of turbohypobiosis) plays a role mainly when alternative mechanisms in cells cannot ensure a normal physiological state under stress conditions. Practically any system (inner construction of a bioreactor, culture and cultivation conditions, including mixing) requires its own optimisation to achieve the final goal, namely, the maximum product and/or biomass yields from substrate (YP/S or/and YX/S), respectively. Data on the biotechnological performance of cultivation as well as power input, kinetic energy (e) of flow fluctuations, air consumption rate, rotational speed, tip speed, etc. do not correlate directly if the mixing systems (impellers-baffles) are dissimilar. Even the widely used specific power consumption cannot be relied upon for scaling up the cultivation performance using dissimilar mixing systems. A biochemical explanation for substrate and product transport via cell walls, carbon pathways, energy generation and utilisation, etc. furnishes insight into cellular interactions with turbulence of different origin for different types of microorganisms (single cells, mycelia forming cells, etc.).

[1] U.E. Viesturs, A.J. Berzinš, M.K. Toma and M.A. Rikmanis: “Mass transfer and shear effects in bioreactors at increased concentration of solids”, In: Proc. Third European Congress on Biotechnology, Munchen, Federal Republic of Germany, 10–14 September 1984, Verlag Chemie, Vol. II, 1984, pp. 293–297. Search in Google Scholar

[2] D.A.J. Wase and Y.R.J. Patel: “Variations in the volumes of microbial cells with change in the agitation rates of chemostat cultures”, J. Gen. Microbiol., Vol. 131, (1985), pp. 725–736. Search in Google Scholar

[3] S.N. Basu and P.N. Pal: “An unfavourable effect of shaking on fungal cellulase”, Nature, Vol. 178, (1956), pp. 312–318. http://dx.doi.org/10.1038/178312b010.1038/178312b0Search in Google Scholar

[4] D.C. Augenstein, A.J. Sinskey and D.I.C. Wang: “Effect of shear on the death of two strains of mammalian tissue cells”, Biotechnol. Bioeng., Vol. 13, (1971), pp. 409–418. http://dx.doi.org/10.1002/bit.26013030810.1002/bit.260130308Search in Google Scholar

[5] L.B. Leverett, J.D. Hellums, C.P. Alfrey and E.C. Lynch: “Red blood cell damage by shear stress”, Biophys. J., Vol. 12, (1972), pp. 257–273. http://dx.doi.org/10.1016/S0006-3495(72)86085-510.1016/S0006-3495(72)86085-5Search in Google Scholar

[6] M. Tirrel and S. Middleman: “Shear modification of enzyme kinetics”, Biotechnol. Bioeng., Vol. 17, (1975), pp. 299–303. http://dx.doi.org/10.1002/bit.26017021810.1002/bit.260170218Search in Google Scholar

[7] H. Tanaka: “Studies on the effect of agitation on mycelia in submerged culture”, J. Ferment. Technol., Vol. 54, (1976), pp. 818–829. Search in Google Scholar

[8] E. Ujcova, Z. Fencl and M. Musilkova: “Dependence of release of nucleotides from fungi on fermentor turbine speed”, Biotechnol. Bioeng., Vol. 22, (1980), pp. 237–241. http://dx.doi.org/10.1002/bit.26022011910.1002/bit.260220119Search in Google Scholar

[9] E.T. Reese and D.Y. Ryu: “Shear inactivation of cellulase of Trichoderma reesei”, Enz. Microb. Technol., Vol. 2, (1980), pp. 239–240. http://dx.doi.org/10.1016/0141-0229(80)90054-X10.1016/0141-0229(80)90054-XSearch in Google Scholar

[10] J.C. van Suijdam and B. Metz: “Fungal pellet break up as a function of shear in a fermentor”, J. Ferment. Technol., Vol. 59, (1981), pp. 329–333. Search in Google Scholar

[11] R. Bronnenmeier and H. Markl: “Hydrodynamic stress capacity of microorganisms”, Biotechnol. Bioeng., Vol. 24, (1982), pp. 553–578. http://dx.doi.org/10.1002/bit.26024030410.1002/bit.260240304Search in Google Scholar PubMed

[12] S. Mukataka, M. Tada and J. Takahashi: “Effects of agitation on enzymatic hydrolysis of cellulose in a stirred tank reactor”, J. Ferment. Technol., Vol. 61, (1983), pp. 615–621. Search in Google Scholar

[13] U. Viesturs, M. Toma, M. Ruklisha and M. Rikmanis: “Optimization of medium agitation intensity in lysine synthesis by Brevibacterium flavum”, In: Abstr. of the 8th United USSR & GDR Symposium on Contemporary Problems of Biochemistry and Biotechnology, Riga, 1985, p. 218 (in Russian). Search in Google Scholar

[14] A.R. Wechezak, R.F. Viggers and L.R. Sauvage: “Fibronectin and F-actin redistribution in cultured endothelial cells exposed to shear stress”, Lab. Invest., Vol. 53, (1985), pp. 639–647. Search in Google Scholar

[15] H. Markl and R. Bronnenmeier: “Mechanical stress and microbial production”, In: Vol. 2, H. Brauer (Ed.): Biotechnology: A Comprehensive Treatise in 8 Volumes, Deerfield Beach VCH, Weinheim, 1985, pp. 369–392. Search in Google Scholar

[16] N.A. Stathopoulos and J.D. Hellums: “Shear stress effects on human embryonic kidney cells in vitro”, Biotechnol. Bioeng., Vol. 27, (1985), pp. 1021–1026. http://dx.doi.org/10.1002/bit.26027071310.1002/bit.260270713Search in Google Scholar PubMed

[17] T.C. Dodge and W.S. Hu: “Growth of hybridoma cells under different agitation conditions”, Biotechnol. Lett., Vol. 8, (1986), pp. 683–686. http://dx.doi.org/10.1007/BF0103256110.1007/BF01032561Search in Google Scholar

[18] R.S. Cherry and E.T. Papoutsakis: “Hydrodynamic effects on cells in agitated tissue culture reactors”, Bioproc. Eng., Vol. 1, (1986), pp. 29–41. http://dx.doi.org/10.1007/BF0036946210.1007/BF00369462Search in Google Scholar

[19] P.F. Davies, A. Remuzzi, E.J. Gordon, C.F. Dewey Jr. and M.A. Gimbone: “Turbulent shear stress induces vascular endothelial cell turnover in vivo”, Proc. Nat. Acad. Sci. USA, Vol. 83, (1986), pp. 2114–2117. http://dx.doi.org/10.1073/pnas.83.7.211410.1073/pnas.83.7.2114Search in Google Scholar

[20] J. Tramper, J.B. Williams, D. Joustra and J.M. Vlak: “Shear sensitivity of insect cells in suspension”, Enz. Microb. Technol., Vol. 8, (1986), pp. 33–36. http://dx.doi.org/10.1016/0141-0229(86)90007-410.1016/0141-0229(86)90007-4Search in Google Scholar

[21] M.M. Toma, U. Viesturs, M. Ruklisha, M. Rikmanis and J. Vanags: “Turbohypobiosis (approbation of the term and indication methods)”, In: Abstr. of the 4th Symposium of Soc. Countries on Biotechnology, Varna, Bulgaria, 1986, p. 266. Search in Google Scholar

[22] K. Trinh, M. Garcia-Briones, J.J. Chalmers and F. Hink: “Quantification of damage to suspended insect cells as a result of bubble rupture”, Biotech. Bioeng., Vol. 43, (1994), pp. 37–45. http://dx.doi.org/10.1002/bit.26043010610.1002/bit.260430106Search in Google Scholar

[23] M. Rikmanis, V. Krikis, I. Sturmanis, V. Savenkovs and U. Viesturs: “Determination of pulsing component of conductivity in fermenter”, In: Fermentation Equipment, Zinatne, Riga, 1980, pp. 93–98 (in Russian). Search in Google Scholar

[24] F. Magelli, D. Fajner, M. Nocentini and G. Pasquali: “Solid distribution in vessels stirred with multiple impellers”, Chem. Eng. Sci., Vol. 45, (1990), pp. 615–625. http://dx.doi.org/10.1016/0009-2509(90)87005-D10.1016/0009-2509(90)87005-DSearch in Google Scholar

[25] A. Brucato, F. Magelli, M. Nocentini and L. Rizzuti: “An application of the network-of-zones model to solids suspension in multiple impeller mixers”, Chem. Eng. Res. Des., Vol. 69, (1991), pp. 43–52. Search in Google Scholar

[26] C.P.J. Bennington and V.K. Thangavel: “The use of a mixing-sensitive chemical reactions for the study of pulp fibre suspension mixing”, Can. J. Chem. Eng., Vol. 71, (1993), pp. 667–675. Search in Google Scholar

[27] C.M. McFarlane, Xue-Ming Zhao and A.W. Nienow: “Studies of high solidity ratio hydrofoil impellers for aerated bioreactors. 2. Air-water studies”, Biotechnol. Prog., Vol. 11, (1995), pp. 608–618. http://dx.doi.org/10.1021/bp00036a00210.1021/bp00036a002Search in Google Scholar

[28] By Chen-Yu Cheng, J.F. Atkinson and MI Bursik: “Direct measurement of turbulence structures in mixing jar using PIV”, J. Environ. Eng., (1997), pp. 115–125. Search in Google Scholar

[29] P. Vrabel, R.G.J.M. van der Lans, K.C.A.M. Luyben, L. Boon and A.W. Nienow: “Mixing in large-scale vessels stirred with multiple radial or radial and axial uppumping impellers: modelling and measurements”, Chem. Eng. Sci., Vol. 55, (2000), pp. 5881–5896. http://dx.doi.org/10.1016/S0009-2509(00)00175-510.1016/S0009-2509(00)00175-5Search in Google Scholar

[30] D. Cacaval, C. Oniscu, A.I. Galaction and L.F. Dumitru: “Characterization of mixing efficiency in bioreactors”, Roum. Biotechnol. Lett., Vol. 6, (2001), pp. 281–291. Search in Google Scholar

[31] S.D. Vlaev: “Potentials of a nickel/aluminium alloy tracer for solid phase flow identification in suspension mixing vessels”, In: Proc. 15th Congress CHISA 2002, lecture F4.2. Search in Google Scholar

[32] T. Saito, S. Yamamoto, T. Yamashita, M. Fukawa and H. Kusano: “Bubble measurement and characterization using optical fiber probe: relationship between measuring accuracy and bubble interfacial deformation”, In: Proc. 15th Congress CHISA 2002, lecture E1.3. Search in Google Scholar

[33] U. Viesturs, M. Rikmanis and J. Levitan: “Energy consumption and distribution in bioreactors”, In: Proc. 3rd European Congress on Biotechnology, Vol. 2, Dechema, Verlag Chemie, 1984, pp. 263–268. Search in Google Scholar

[34] M. Rikmanis, J. Vanags, M. Zeltina, M. Leite and U. Viesturs: “Design peculiarities and energy distribution in bioreactors for mycelial cultures”, In: Proc. 9th International Congress of Chemical Engineering, Chemical Equipment Design and Automation CHISA’ 87, Praha, Czechoslovakia, 1987, paper A6-136. Search in Google Scholar

[35] M. Rikmanis, J. Vanags, E. Ushkans and U. Viesturs: “Stirring characteristics in bioreactors”, In: Proc. Congress CHISA’ 87, 1987, paper E9-137. Search in Google Scholar

[36] M. Rikmanis, J. Vanags and U. Viesturs: “Determination of stirring characteristics in bioreactors”, Biotehnologija, Vol. 3, (1987), pp. 70–78 (in Russian). Search in Google Scholar

[37] J. Vanags, M. Rikmanis, E. Uschkans, J. Grants and U. Viesturs: “Entwicklung eines Gerätes zur Messung der Vermichungsintensität in Bioreaktoren”, 4. Heiligenstädter Kolloquium Wissenschaftliche Geräte für die Biotechnologie, DDR, Heiligenstadt, 1988, pp. 282–287 (in German). Search in Google Scholar

[38] J. Vanags and M. Rikmanis: “The use of hydrodynamic data in the evaluation of bioreactor efficiency”, In: Proc. 10th Congress CHISA’ 90, 1990, paper A7-79. Search in Google Scholar

[39] U. Viesturs, M. Rikmanis and J. Vanags: “Comparison of bioreactors and their choice”, In: Proc. 10th Congress CHISA’ 90, 1990, paper A8-5. Search in Google Scholar

[40] M. Rikmanis, J. Vanags, J. Grants and E. Ushkans: “The optimum stirring regime during microorganism cultivation”, In: Proc. 10th Congress CHISA’ 90, 1990, paper J4-3. Search in Google Scholar

[41] J. Vanags, M. Rikmanis, E. Ushkans and U. Viesturs: “Stirring characteristics in bioreactors”, AIChE J., Vol. 36, (1990), pp. 1361–1370. http://dx.doi.org/10.1002/aic.69036090910.1002/aic.690360909Search in Google Scholar

[42] I. Fort, J. Libal, J. Vanags, M. Rikmanis and U. Viesturs: “Distribution of kinetic energy of turbulence in agitated system with axial high-speed impeller and baffles”, In: Proc. International Meeting on Chemical Engineering and Biotechnology, 23rd Exhibition-Congress ACHEMA’ 91, Frankfurt am Main, 1991. Search in Google Scholar

[43] J. Vanags, U. Viesturs, M. Rikmanis and I. Fort: “Mixing characteristics in bioreactors using piezoelectrical transducers”, In: Proc. 7th European Congress on Mixing, Brugge, Belgium, 1991, pp. 403–408. Search in Google Scholar

[44] I. Fort, P. Ettler, F. Kolin, J. Vanags and M. Rikmanis: “Studies on mixing”, Collect. Czech. Chem. Commun., Vol. 57, (1992), pp. 1057–1060. Search in Google Scholar

[45] A. Bakker and H.E.A. van den Akker: “A computational model for the gas-liquid flow in stirred reactors”, Chem. Eng. Res. Des., Vol. 72, (1994), pp. 594–606. Search in Google Scholar

[46] H. Dekker: “Theory of turbulent shear stress”, Mod. Phys. Lett. B, Vol. 14, (2000), pp. 781–784. http://dx.doi.org/10.1142/S021798490000098710.1142/S0217984900000987Search in Google Scholar

[47] K. J. Bittorf and K. Johnson: “Computer aided mixing modeling using the Galerkin least-squares finite element technique”, www.acusim.com/papers/mixing with gls.pdf. Search in Google Scholar

[48] G. Locher, U. Hahnemann, B. Sonnleitner and A. Fiechter: “Automatic bioprocess control. 5. Biologically and technically caused effects during cultivation”, J. Biotechnol., Vol. 29, (1993), pp. 75–89. http://dx.doi.org/10.1016/0168-1656(93)90041-K10.1016/0168-1656(93)90041-KSearch in Google Scholar

[49] F. Delvigne, J. Destain and P. Thonart: “Bioreactor hydrodynamic effect on Escherichia coli physiology: experimental results and stochastic simulations”, Bioproc. Biosyst. Eng., Vol. 28, (2005), pp. 131–137. http://dx.doi.org/10.1007/s00449-005-0018-z10.1007/s00449-005-0018-zSearch in Google Scholar PubMed

[50] A. Berzinš, U. Viesturs, M. Rikmanis and S. Tzonkov: “Studies of the Saccharomyces cerevisiae cultivation under oscillatory mixing conditions”, Bioautomation, Vol. 3, (2005), pp. 36–42. Search in Google Scholar

[51] Wei-Cho Huang, C.S. Gong and G.T. Tsao: “Enhancement of oxygen transfer by pressure pulsation in aqueous glycerol fermentation”, Appl. Biochem. Biotechnol., Vol. 98-100, (2002), pp. 909–920. http://dx.doi.org/10.1385/ABAB:98-100:1-9:90910.1385/ABAB:98-100:1-9:909Search in Google Scholar

[52] M. Rikmanis, M.-M. Toma, A. Berzinš and U. Viesturs: “New possibilities in process control and some results of their use”, In: Proc. Congress CHISA’ 93, 1993, paper H7-4. Search in Google Scholar

[53] M. Assirelli, W. Bujalski, A.W. Nienow and A. Eaglesham: “Study of micromixing in a stirred tank using a Rushton turbine: comparison of feed positions and other mixing devices”, In: Proc. Congress CHISA 2002, Paper F 3.7. 10.1205/026387602321143390Search in Google Scholar

[54] A. Berzins, M. Rikmanis, U. Viesturs, M. Toma and B. Viskere: “The stirring oscillation method for study of the bioprocess”, In: Proc. Congress CHISA 2002, paper P5.154. Search in Google Scholar

[55] A. Berzins, M. Rikmanis, U. Viesturs, M. Toma and B. Viskere: “The stirring oscillation method for study of the bioprocess”, In: 15th International Congress of Chemical and Process Engineering CHISA 2002, Praha, Czech Republic, Vol. 3, (2002), p. 245. Search in Google Scholar

[56] M. Priede and U. Viesturs: “Effect of pulsing mixing interruptions on the Aspergillus niger morphology and citric acid production”, Chem. Biochem. Eng. Q., Vol. 19, (2005), pp. 359–366. Search in Google Scholar

[57] C. Born, Z. Zhang, M. Al-Rubeai and C.R. Thomas: “Estimation of disruption of animal cells by laminar shear stress”, Biotechnol. Bioeng., Vol. 40, (1992), pp. 1004–1010. http://dx.doi.org/10.1002/bit.26040090310.1002/bit.260400903Search in Google Scholar

[58] J.-J. Zhong, K. Fujiyama, T. Seki and T. Yoshida: “A quantitative analysis of shear effects on cell suspension and cell culture of Perilla frutescens in bioreactors”, Biotech. Bioeng., Vol. 44, (1996), pp. 649–654. http://dx.doi.org/10.1002/bit.26044051210.1002/bit.260440512Search in Google Scholar

[59] X. Sun and J.C. Linden: “Shear stress effects on plant cell suspension in rotating wall vessel bioreactor”, J. Ind. Microbiol. Biotech., Vol. 22, (1999), pp. 44–47. http://dx.doi.org/10.1038/sj.jim.290060010.1038/sj.jim.2900600Search in Google Scholar

[60] D.D. Sowana, D.R.G. Williams, E.H. Dunlop, B.B. Dally, B.K. O’Neill and D.F. Fletcher: “Turbulent shear stress effects on plant cell suspension cultures”, Chem. Eng. Res. Des., Vol. 79, (2001), pp. 867–875. http://dx.doi.org/10.1205/0263876015272137010.1205/02638760152721370Search in Google Scholar

[61] H. Deveci: “Effect of particle size and shape of solids on the viability of acidophilic bacteria during mixing in stirred tank reactors”, Hydrometallurgy, Vol. 71, (2004), pp. 385–396. http://dx.doi.org/10.1016/S0304-386X(03)00112-910.1016/S0304-386X(03)00112-9Search in Google Scholar

[62] S. Chamsartra, C.J. Hewitt and A.W. Nienow: “The impact of fluid mechanical stress on Corinebacterium glutamicum during continuous cultivation in an agitated bioreactor”, Biotech. Lett., Vol. 27, (2005), pp. 693–700. http://dx.doi.org/10.1007/s10529-005-4690-510.1007/s10529-005-4690-5Search in Google Scholar

[63] C. Brindley Alias, M.C. Garcia-Malea Lopez, F.G. Acien Fernandez, J.M. Fernandez Sevilla, J.L. Garcia Sanchez and E. Molina Grima: “Influence of power supply in the feasibility of Phaeodactilum tricornutum cultures”, Biotech. Bioeng., Vol. 87, (2004), pp. 723–732. http://dx.doi.org/10.1002/bit.2017910.1002/bit.20179Search in Google Scholar

[64] P. Ayazi Shamlou, H.Y. Makagiansar, A.P. Ison and M.D. Lilly: “Turbulent breakage of filamentous microorganisms in submerged culture in mechanically stirred bioreactors”, Chem. Eng. Sci., Vol. 49, (1994), pp. 2621–2631. http://dx.doi.org/10.1016/0009-2509(94)E0079-610.1016/0009-2509(94)E0079-6Search in Google Scholar

[65] U. Rau, E. Gura, E. Olszewski and F. Wagner: “Enhanced glucan formation of filamentous fungi by effective mixing, oxygen limitation and fed-batch processing”, J. Ind. Microbiol., Vol. 9, (1992), pp. 19–26. http://dx.doi.org/10.1007/BF0157636410.1007/BF01576364Search in Google Scholar

[66] J.J. Vanags, M.A. Priede and U.E. Viesturs: “Studies of the mixing character and flow distribution in mycelial fermentation broth”, Acta Biotech., Vol. 15, (1995), pp. 355–366. http://dx.doi.org/10.1002/abio.37015040810.1002/abio.370150408Search in Google Scholar

[67] M.A. Priede, J.J. Vanags and U.E. Viesturs: “Mixing intensity studies by SIMD using dissimilar stirrers. Case study: production of fusicoccin by the fungus Fusicoccum aamygdali del.”, Biotechnology & Biotechnological Equipment, Vol. 9, (1995), pp. 75–83. Search in Google Scholar

[68] L.H. Grimm, S. Kelly, I.I. Völkerding, R. Krull and D.C. Hempel: “Influence of mechanical stress and surface interaction on the aggregation of Aspergillus niger conidia”, Biotech. Bioeng., Vol. 92, (2005), pp. 879–888. http://dx.doi.org/10.1002/bit.2066610.1002/bit.20666Search in Google Scholar

[69] M.A. Priede, J.J. Vanags, U.E. Viesturs, K.G. Tucker, W. Bujalski and C.R. Thomas: “Hydrodynamic, physiological, and morphological characteristics of Fusarium moniliforme in geometrically dissimilar stirred bioreactors”, Biotech. Bioeng., Vol. 48, (1995), pp. 266–277. http://dx.doi.org/10.1002/bit.26048031310.1002/bit.260480313Search in Google Scholar

[70] A. Apsite, U. Viesturs, V. Steinberga and M. Toma: “Morphology and antifungal action of the genus Trichoderma cultivated in geometrically dissimilar bioreactors”, World J. Microbiol. Biotech., Vol. 14, (1998), pp. 23–29. http://dx.doi.org/10.1023/A:100881213065410.1023/A:1008812130654Search in Google Scholar

[71] A. Berzins, M. Toma, M. Rikmanis and U. Viesturs: “Influence of micromixing on microorganisms and products”, Acta Biotechnol., Vol. 21, (2001), pp. 155–170. http://dx.doi.org/10.1002/1521-3846(200105)21:2<155::AID-ABIO155>3.0.CO;2-Q10.1002/1521-3846(200105)21:2<155::AID-ABIO155>3.0.CO;2-QSearch in Google Scholar

[72] J.A. Rocha-Valadez, M. Hassan, G. Corkidi, C. Flores, E. Galindo and L. Serrano-Carreon: “6-pentyl-α-pyrone production by Trichoderma harzianum: the influence of energy dissipation rate and its implications on fungal physiology”, Biotech. Bioeng., Vol. 91, (2005), pp. 55–61. http://dx.doi.org/10.1002/bit.2048910.1002/bit.20489Search in Google Scholar

[73] P. Justen: “Dependence of Penicillium chrysogenum growth, morphology, vacuolation and productivity on impeller type and agitation intensity”, In: Thesis D. Phil. degree, School of Chemical Engineering, University of Birmingham, March 1997. Search in Google Scholar

[74] A. Apsite, A. Berzinš, M. Toma, V. Šteinberga, M. Rikmanis and U. Viesturs: “Effect of cultivation conditions on Trichoderma viride LL-333 growth”, Proc. Latv. Acad. Sci., Vol. 9/10, (1995), pp. 121–127. Search in Google Scholar

[75] N. Edwards, S. Beeton, A.T. Bull and J.C. Merchuk: “A novel device for the assessment of shear effects on suspended microbial cultures”, Appl. Microbiol. Biotechnol., Vol. 30, (1989), pp. 190–195. http://dx.doi.org/10.1007/BF0026401010.1007/BF00264010Search in Google Scholar

[76] M.A. Priede, J.J. Vanags and U.E. Viesturs: “Performance of Aspergillus niger cultivation in geometrically dissimilar bioreactors evaluated on the basis of morphological analyses”, Food Technol. Biotechnol., Vol. 40, (2002), pp. 57–66. Search in Google Scholar

[77] E.H. Dunlop and P.K. Namdev: “Effect of fluid shear forces on plant cell suspensions”, Chem. Eng. Sci., Vol. 49, (1994), pp. 2263–2276. http://dx.doi.org/10.1016/0009-2509(94)E0043-P10.1016/0009-2509(94)E0043-PSearch in Google Scholar

[78] M.K. Toma, M.P. Ruklisha, J.J. Vanags, M.O. Zeltina, M.P. Leite, N.I. Galinina, U.E. Viesturs and R.P. Tengerdy: “Inhibition of microbial growth and metabolism by excess turbulence”, Biotech. Bioeng., Vol. 38, (1991), pp. 552–556. http://dx.doi.org/10.1002/bit.26038051410.1002/bit.260380514Search in Google Scholar

[79] M. Rikmanis, M. Toma, A. Berzinsh and U. Viesturs: “Some effects of fluid dynamics at non-destructive stirring regimes”, In: Proc. 3rd International Conference on Bioreactor and Bioprocess Fluid Dynamics, Robinson College, Cambridge, UK, 1993, pp. 305–312. Search in Google Scholar

[80] M.R. Marten, S. Velkovska, S.A. Khan and D.F. Ollis: “Rheological, mass transfer and mixing characterization of cellulase-producing Trichoderma reesei suspensions”, Biotechnol. Prog., Vol. 12, (1996), pp. 602–611. http://dx.doi.org/10.1021/bp950066b10.1021/bp950066bSearch in Google Scholar

[81] B.O. Yepez Silva-Santisteban and F. Maugeri Filho: “Agitation, aeration and shear stress as key factors in inulinase production by Kluyveromyces marxianus”, Enzyme and Microbial Technol., Vol. 36, (2005), pp. 717–724. http://dx.doi.org/10.1016/j.enzmictec.2004.12.00810.1016/j.enzmictec.2004.12.008Search in Google Scholar

[82] R.S. Ghadge, A.W. Patwardhan, S.B. Sawant and J.B. Joshi: “Effect of flow pattern on cellulase deactivation in stirred tank bioreactors”, Chem. Eng. Sci., Vol. 60, (2005), pp. 1067–1083. http://dx.doi.org/10.1016/j.ces.2004.09.06910.1016/j.ces.2004.09.069Search in Google Scholar

[83] M.P. Ruklisha, J.J. Vanags, M.A. Rikmanis, M.K. Toma and U.E. Viesturs: “Biochemical reactions of Brevibacterium flavum depending on medium stirring intensity and flow structure”, Acta Biotechnol., Vol. 9, (1989), pp. 565–575. http://dx.doi.org/10.1002/abio.37009061510.1002/abio.370090615Search in Google Scholar

[84] F. Kaya, J.A. Heitmann Jr. and T.W. Joyce: “Deactivation of cellulase and hemicellulase in high shear fields”, Cellulose Chem. Technol., Vol. 30, (1996), pp. 49–56. Search in Google Scholar

[85] M. Priede, R. Karklinš, U. Viesturs and L. Krasnopolskaya: “Fusicoccin production by fungus Fusicoccum amygdali DEL. at different agitation/aeration regimes”, Proc. Latv. Acad. Sci. B., (1993), Vol. 548, pp. 56–60. Search in Google Scholar

[86] J. Audet, H. Gagnen, M. Lounes and J. Thibault: “Polysaccharide production: experimental comparison of the performance of four mixing devices”, Bioproc. Eng., Vol. 19, (1998), pp. 45–52. http://dx.doi.org/10.1007/s00449005048110.1007/s004490050481Search in Google Scholar

[87] M. Miyazawa, T. Torii, Y. Toshimitsu and I. Koyama: “Effect of mechanical stress imposition on co-culture of hepatic parenchimal and nonparenchimal cells: possibility of stimulating production of regenerating factor”, Transpl. Proc., Vol. 37, (2005), pp. 2398–2401. http://dx.doi.org/10.1016/j.transproceed.2005.03.10310.1016/j.transproceed.2005.03.103Search in Google Scholar

[88] E. Dreveton, F. Monot, J. Lecourtier, D. Ballerini and L. Choplin: “Influence of fermentation hydrodynamics on gellan gum physico-chemical charasteristics”, J. Ferm. Bioeng., Vol. 82, (1996), pp. 272–276. http://dx.doi.org/10.1016/0922-338X(96)88819-210.1016/0922-338X(96)88819-2Search in Google Scholar

[89] A. Converti, M. Del Borghi, G. Ferraiolo and C. Sommariva: “Mechanical mixing and biological deactivation: the role of shear stress application time”, Chem. Eng. J., Vol. 62, (1996), pp. 155–167. Search in Google Scholar

[90] D.D. Sowana, D.R.G. Williams, B.K. O’Neill and E.H. Dunlop: “Studies of the shear protective effects of Pluronic F-68 on wild carrot cell cultures”, Biochem. Eng. J., Vol. 12, (2002), pp. 165–173. http://dx.doi.org/10.1016/S1369-703X(02)00038-410.1016/S1369-703X(02)00038-4Search in Google Scholar

[91] A. Apsite, A. Berzins, M. Rikmanis, V. Steinberga, M.M. Toma and U. Viesturs: “Bioreactors for mycelial cultures and some results of their use”, In: Proc. Int. Conf. Modelling of Filamentous Fungi, Otočec, Slovenia, September 1994. Search in Google Scholar

[92] S. Bulut, W.M. Waites and J.R. Mitchell: “Effects of combined shear and thermal forces on destruction of Microbacterium lacticum”, Appl. Environm. Microbiol., Vol. 65, (1999), pp. 4464–4469. Search in Google Scholar

[93] Pak Kin Wong, Yi-Kuen Lee and Chin-Ming Ho: “Deformation of DNA molecules by hydrodynamic focusing”, J. Fluid Mech., Vol. 497, (2003), pp. 55–65. http://dx.doi.org/10.1017/S002211200300658X10.1017/S002211200300658XSearch in Google Scholar

[94] M. Diaz, A.I. Garcia and L.A. Garcia: “Mixing power, external convection and effectiveness in bioreactors”, Biotech. Bioeng., Vol. 51, (1996), pp. 131–140. http://dx.doi.org/10.1002/(SICI)1097-0290(19960720)51:2<131::AID-BIT1>3.0.CO;2-K10.1002/(SICI)1097-0290(19960720)51:2<131::AID-BIT1>3.0.CO;2-KSearch in Google Scholar

[95] J. Vanags, M. Priede, R. Are and U. Viesturs: “Effect of various mixing systems on citric acid production”, Proc. Latvian Acad. Sci. B, Vol. 539, (1992), pp. 60–64. Search in Google Scholar

[96] A. Berzins, M. Rikmanis, M. Toma, U. Viesturs and S. Gonta: “Cultivation of Zymomonas mobilis 113S at different mixing regimes and their influence on the levan formation”, Acta Biotechnol., Vol. 21, (2001), pp. 19–26. http://dx.doi.org/10.1002/1521-3846(200102)21:1<19::AID-ABIO19>3.0.CO;2-M10.1002/1521-3846(200102)21:1<19::AID-ABIO19>3.0.CO;2-MSearch in Google Scholar

[97] P.K. Namdev and E.H. Dunlop: “Shear sensitivity of plant cells in suspensions”, Appl. Biochem. Biotechnol., Vol. 54, (1995), pp. 109–131. Search in Google Scholar

[98] G. H. Altman, R.L. Horan, I. Martin, J. Farhadi, P.R.H. Stark, V. Volloch, J.C. Richmond, G. Vunjak-Novakovic and D.L. Kaplan: “Cell differentiation by mechanical stress”, The FASEB Journal, Express article doi:10.1096/fj.01-0656fje, published online December 28, (2001). www.fasebj.org/cgi/content/abstract/01-0656fjev1. Search in Google Scholar

[99] R.S. Cherry: “Animal cells in turbulent fluids: details of the physical stimulus and the biological response”, Biotech. Adv., Vol. 11, (1993), pp. 279–299. http://dx.doi.org/10.1016/0734-9750(93)90043-M10.1016/0734-9750(93)90043-MSearch in Google Scholar

Published Online: 2007-12-1
Published in Print: 2007-12-1

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