Determination of shear stress thresholds in toxic dinoflagellates cultured in shaken flasks. Implications in bioprocess engineering

Process Biochemistry

Volumn 42, Issue 11, 2007, Pages 1506-1515

  Garcia Camacho F ^a   Gallardo Rodriguez J J ^a   Sanchez Miron A ^a   Ceron Garcia M C ^a   Belarbi, E H ^a   Molina Grima, E ^a  

^a UNIVERSITY OF ALMERÍA   (Spain)

Author keywords

Damage; Dinoflagellate; Microalgae; Pluronic; Protoceratium reticulatum; Shear stress

Indexed keywords

ALGAE; BIOMEDICAL ENGINEERING; BIOTECHNOLOGY; HYDRODYNAMICS; MARINE BIOLOGY; SHEAR STRESS; TOXICITY;

HYDRODYNAMIC SHEAR STRESS; MICROALGAE; PROTOCERATIUM RETICULATUM; TOXIC DINOFLAGELLATES;

PROTOZOA;

DINOPHYCEAE; PROTOCERATIUM RETICULATUM;

EID: 35148833634     PISSN: 13595113     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.procbio.2007.08.001     Document Type: Article

References (51)

1. Backer L.C., Fleming L.E., Rowan A.D., and Baden D.G. Epidemiology, public health and human diseases associated with harmful marine algae. In: Hallegraef G.M., Anderson D.M., and Cembella A.D. (Eds). Manual on harmful marine microalgae (2004), Unesco Publishing, Paris 723-749
2. Camacho F.G., Rodríguez J.G., Mirón A.S., García M.C., Belarbi E.H., and Chisti Y. Grima EM biotechnological significance of toxic marine dinoflagellates. Biotechnol Adv 25 2 (2007) 176-194
3. Pollingher U., and Zemel E. In situ and experimental evidence of the influence of turbulence on cell division processes of Peridinium cinctum forma westii (lemm.) Lefèvre. Br Phycol J 16 (1981) 281-287
4. Gibson C.H., and Thomas W.H. Effects of turbulence intermittency on growth inhibition of a red tide dionflagellate Gonyalaux polyedra Stein. J Phycol 30 (1995) 50-59
5. Juhl A.R., and Latz M. Mechanisms of fluid shear-induced inhibition of population growth in a red-tide dinoflagelate. J Phycol 38 (2002) 683-694
6. Sullivan J.M., and Swift E. Effects of small-scale turbulence on net growth rate and size of ten species of marine dinoflagellates. J Phycol 39 (2003) 83-94
7. García Camacho F., Molina Grima E., Sánchez Mirón A., González Pascual V., and Chisti Y. Carboxymethyl cellulose protects algal cells against hydrodynamic stress. Enzyme Microb Technol 29 (2001) 602-610
8. Sánchez Mirón A., Cerón García M.C., Contreras Gómez A., García Camacho F., Molina Grima E., and Chisti Y. Shear stress tolerance and biochemical characterization of Phaeodactylum tricornutum in quasi steady-state continuous culture in outdoor photobioreactors. Biochem Eng J 16 (2003) 287-297
9. Mazzuca Sobczuk T., Garcia Camacho F., Molina Grima E., and Chisti Y. Effects of agitation on the microalgae Phaeodactylum tricornutum and Porphyridium cruentum. Bioproc Biosyst Eng 28 (2006) 243-250
10. Lin Y., Zang Z., and Thibault J. Aureobasidium pullulans batch cultivations based on a factorial design for improving the production and molecular weight of exopolysaccharides. Process Biochem 42 (2007) 820-827
11. Rocha-Valadez J., Estrada M., Galindo E., and Serrano-Carreón L. From shake flasks to stirred fermentors: Scale-up of an extractive fermentation process for 6-pentyl-a-pyrone production by Trichoderma harzianum using volumetric power input. Process Biochem 41 (2006) 1347-1352
12. Kawaguti H.Y., Ferrari M., Castilho D., Tiemi G., and Harumi H. Effect of the additives polyethylenimine and glutaraldehyde on the immobilization of Erwinia sp. D12 cells in calcium alginate for isomaltulose production. Process Biochem 41 (2006) 2035-2040
13. Velagapudi V., Wittmann C., Lengauer T., Talwar P., and Heinzle E. Metabolic screening of Saccharomyces cerevisiae single knockout strains reveals unexpected mobilization of metabolic potential. Process Biochem 41 (2006) 2170-2179
14. Cerón M.C., Sánchez A., Fernández J.M., Molina E., and García F. Mixotrophic growth of the microalga Phaeodactylum tricornutum: influence of different nitrogen and organic carbon sources on productivity and biomass composition. Process Biochem 40 (2005) 297-305
15. Büchs J., Maier U., Milbradt C., and Zoels B. Power consumption in shaking flasks on rotary shaking machines. II. Nondimensional description of specific power consumption and flow regimes in unbaffled flasks at elevated liquid viscosity. Biotechnol Bioeng 68 6 (2000) 594-601
16. Peter C.P., Suzuki Y., and Büchs J. Hydromechanical stress in shake flasks: correlation for the maximum local energy dissipation rate. Biotechnol Bioeng 93 (2006) 1164-1176
17. Palomares L.A., González M., and Ramíi{dotless}rez O.T. Evidence of pluronic F-68 direct interaction with insect cells: impact on shear protection, recombinant protein, and baculovirus production. Enzyme Microb Technol 26 (2000) 324-331
18. King A.T., Davey M.R., Mulligan B.J., and Lowe K.C. Effects of pluronic F-68 on plant cells in suspension culture. Biotechnol Lett 1 (1990) 29-32
19. García Camacho F., Belarbi E.H., Cerón García M.C., Sánchez Mirón A., Chile T., Chisti Y., et al. Shear effects on suspended marine sponge cells. Biochem Eng J 26 (2005) 115-121
20. Rodriguez J.G., Garcia M.C., Camacho F.G., Miron A.S., Belarbi E.H., and Grima E.M. New culture approaches for yessotoxin production from the dinoflagellate Protoceratium reticulatum. Biotechnol Prog 23 2 (2007) 339-350
21. Paz B., Vázquez J.A., Riobó P., and Franco J.M. Study of the effect of temperature, irradiance and salinity on growth and yessotoxin production by the dinoflagellate Protoceratium reticulatum in culture by using a kinetic and factorial approach. Mar Environ Res 62 (2006) 286-300
22. Guillard R., and Hargraves P. Stichochysis immovilis is a diatom, not a chysophyte. Phycologia 32 (1993) 234-236
23. Ormerod M. Flow cytometry: a practical approach (2000), Oxford University Press, Oxford p. 296
24. Henzler H.J. Particle stress in bioreactors. Adv Biochem Eng Biotechnol 67 (2000) 35-82
25. Zhang H., Williams-Dalson W., Keshavarz-Moore E., and Shamlou P.A. Computational-fluid-dynamics (CFD) analysis of mixing and gas-liquid mass transfer in shake flasks. Biotechnol Appl Biochem 41 (2005) 1-8
26. Standard methods for the examination of water and wastewater. 19th ed. (1995), American Public Health Association. American Water Works Association. Federation of Sewage & Industrial Wastes Associations, New York
27. Moya MJ. Haematococcus lacustris. Cinética de crecimiento y producción de astaxantina. Ph.D. thesis. Spain: Universidad Ramón Llull; 1996.
28. Lazt M.I., Case J.F., and Gran R.L. Excitation of luminescence by laminar fluid shear associated with simple Couette flow. Limnol Oceanogr 39 (1994) 1424-1439
29. Juhl A.R., Velázquez V., and Latz M.I. Effect of growth conditions on flow-induced inhibition of population growth of a red-tide dinoflagellate. Limnol Oceanogr 45 (2000) 905-915
30. Chisti Y. Animal-cell damage in sparged bioreactors. Trends Biotechnol 18 (2000) 420-432
31. Kieran P.M., Malone D.M., and MacLoughlin P.K. Effects of hydrodynamic and interfacial forces on plant cell suspension systems. Adv Biochem Eng Biotechnol 67 (2000) 139-177
32. Berdalet E., and Estrada M. Effects of turbulence on several dinoflagellate species. In: Smayda T.J., and Shimizu Y. (Eds). Effects phytoplankton blooms in the sea (1993), Elsevier Science, Amsterdam 737-740
33. García Camacho F., Contreras Gómez A., Mazzuca Sobezuk T., and Molina Grima E. Effects of mechanical and hydrodynamic stress in agitated, sparged cultures of Porphyridium cruentum. Process Biochem 35 (2000) 1045-1050
34. Yeung P.K.K., and Wong J.T.Y. Inhibition of cell proliferation by mechanical agitation involves transient cell cycle arrest at G1 phase in dinoflagellates. Protoplasma 220 (2003) 173-178
35. Mollet M., Ma N., Zhao Y., Brodkey R., Taticek R., and Chalmers J.J. Bioprocess equipment: characterization of energy dissipation rate and its potential to damage cells. Biotechnol Prog 20 (2004) 1437-1446
36. Wichterle K., Sobolík V., Lutz M., and Denk V. Shear rate on centrifugal pump impeller. Chem Eng Sci 5 (1996) 5227-5228
37. Brindley Alías C., García-Malea López M.C., Acién Fernández F.G., Fernández Sevilla J.M., García Sánchez J.L., and Molina Grima E. Influence of power supply in the feasibility of Phaeodactylum tricornutum cultures. Biotechnol Bioeng 87 (2004) 723-733
38. Sánchez Mirón A., García Camacho F., Contreras Gómez A., Molina Grima E., and Chisti Y. Bubble column and airlift photobioreactors for algal culture. AIChE J 46 (2000) 1872-1887
39. Contreras A., García F., Molina E., and Merchuk J.C. Influence of sparger on energy dissipation, shear rate, and mass transfer to sea water in a concentric-tube airlift bioreactor. Enzyme Microb Technol 25 (1999) 820-830
40. Sánchez Mirón A., Cerón García M.C., Belarbi E.H., García Camacho F., Molina Grima E., and Chisti Y. Mixing in bubble column and airlift reactors. Chem Eng Res Des 82 (2004) 1367-1374
41. Barbosa M.J., Hadiyanto, and Wijffels R.H. Overcoming Shear Stress of Microalgae Cultures in Sparged Photobioreactors. Biotechnol Bioeng 85 (2003) 78-85
42. Cetta C.M., and Anderson D.M. Cell cycle studies of the dinoflagellate Gonyaulax polyedra Stein and Gyrodinium uncatenum Hulburt during asexual and sexual reproduction. J Exp Mar Biol Ecol 135 (1990) 69-84
43. Zhang Z., Al-Rubeai M., and Thomas C.R. The effect of pluronic F-68 on mechanical properties of mammalian cells. Enzyme Microb Technol 14 (1992) 980-983
44. Sowana D.D., Williams D.R.G., O'Neill B.K., and Dunlop E.H. Studies of the shear protective effects of Pluronic F-68 on wild carrot cell cultures. Biochem Eng J 12 (2002) 165-173
45. Kumar V., Laouar L., Davey M.R., Mulligan B.J., and Lowe K.C. Pluronic F-68 stimulates growth of Solanum dulcamara in culture. J Exp Bot 43 (1992) 487-493
46. Goldblum S., Bae Y.K., Hink W.F., and Chalmers J. Protective effect of methylcellulose and other polymers on insect cells subjected to laminar shear stress. Biotechnol Prog 6 (1990) 383-390
47. Mallipattu S.K., Haidekker M.A., Latz M.I., and Frangos J.A. Evidence for shar-induced increase in membrane fluidity in the dinoflagellate Lingulodinium polyedrum. J Comp Physiol A 188 (2002) 409-416
48. Papoutsakis E.T. Fluid-mechanical damage of animal cells in bioreactors. Trends Biotechnol 9 (1991) 427-437
49. Chisti Y. Shear sensivity. In: Flickinger M.C., and Drew S. (Eds). Encyclopedia of bioprocess technology-fermentation, biocatalysis, and bioseparation vols. 1-5. (2000), John Wiley & Sons, NY 2379-2406
50. Abu-Reesh I., and Kargi F. Biological responses of hybridoma cells to hydrodynamic shear in an agitated bioreactor. Enzyme Microb Technol 13 (1991) 913-919
51. Mercille S., Johnson M., Lanthier S., Kamen A.A., and Massie B. Understanding factors that limit the productivity of suspension-based perfusion cultures operated at high medium renewal rates. Biotechnol Bioeng 67 (2000) 435-450