Calcium gluconate as cross-linker improves survival and shelf life of encapsulated and dried Metarhizium brunneum and Saccharomyces cerevisiae for the application as biological control agents

References

• Aristov YI, Tokarev M, Cacciola G, Restuccia G. Selective water sorbents for multiple applications, 1. CaCl2 confined in mesopores of silica gel: Sorption properties. React Kinet Catalysis Lett, 1996;59:325–33.
   Google Scholar
• Beker MJ, Rapoport AI. Conservation of yeasts by dehydration. Adv Biochem Eng Biotechnol, 1987;35:127–71.
   Google Scholar
• Bernklau EJ, Bjostad LB. Reinvestigation of host location by western corn rootworm larvae (Coleoptera: Chrysomelidae): CO2 is the only volatile attractant. J Econ Entomol, 1998;91:1331–40.
   Web of Science ®Google Scholar
• Braccini I, Perez S. Molecular basis of C(2+)-induced gelation in alginates and pectins: the egg-box model revisited. Biomacromolecules, 2001;2:1089–96.
   PubMed Web of Science ®Google Scholar
• Cadiere A, Ortiz-Julien A, Camarasa C, Dequin S. Evolutionary engineered Saccharomyces cerevisiae wine yeast strains with increased in vivo flux through the pentose phosphate pathway. Metab Eng, 2011;13:263–71.
   PubMed Web of Science ®Google Scholar
• Chan ES, Wong SL, Lee PP, Lee JS, Ti TB, Zhang ZB, Poncelet D, Ravindra P, Phan SH, Yim ZH. Effects of starch filler on the physical properties of lyophilized calcium-alginate beads and the viability of encapsulated cells. Carbohydr Polym, 2011;83:225–32.
   Web of Science ®Google Scholar
• Clegg JS, Seitz P, Seitz W, Hazlewood CF. Cellular responses to extreme water loss: the water-replacement hypothesis. Cryobiology, 1982;19:306–16.
   PubMed Web of Science ®Google Scholar
• CropLife International, 2009. Guidelines for specifying the shelf life of plant protection products. Technical Monograph n°17, 2nd edn. Brussels, Belgium: CropLife International.
   Google Scholar
• Crowe JH, Crowe LM, Oliver AE, Tsvetkova N, Wolkers W, Tablin F. The trehalose myth revisited: Introduction to a symposium on stabilization of cells in the dry state. Cryobiology, 2001;43:89–105.
   PubMed Web of Science ®Google Scholar
• Crowe JH, Hoekstra FA, Crowe LM. Anhydrobiosis. Ann Rev Physiol, 1992;54:579–99.
   PubMed Web of Science ®Google Scholar
• Crowe LM, Womersley C, Crowe JH, Reid D, Appel L, Rudolph A. Prevention of fusion and leakage in freeze-dried liposomes by carbohydrates. Biochim Biophys Acta, 1986;861:131–40.
   Web of Science ®Google Scholar
• Doane J, Lee Y, Klingler J, Westcott N. The orientation response of Ctenicera destructor and other wire worms (Coleoptera: Elateridae) to germinating grain and to carbon dioxide. Can Entomol, 1975;107:1233–52.
   Web of Science ®Google Scholar
• Eckard S, Ansari MA, Bacher S, Butt TM, Enkerli J, Grabenweger G. Virulence of in vivo and in vitro produced conidia of Metarhizium brunneum strains for control of wireworms. Crop Protect, 2014;64:137–42.
   Web of Science ®Google Scholar
• Eisenbrand G, Schreier P. 2006. Roempp-Lexikon lebensmittelchemie. Stuttgart: Thieme.
   Google Scholar
• Faria M, Hajek AE, Wraight SP. Imbibitional damage in conidia of the entomopathogenic fungi Beauveria bassiana, Metarhizium acridum, and Metarhizium anisopliae. Biol Control, 2009;51:346–54.
   Web of Science ®Google Scholar
• Fravel DR, Connick Jr, WJ, Lewis JA. 1998. Formulation of microorganisms to control plant diseases. In: Burges HD, ed. Formulation of microbial biopesticides. Dordrecht: Kluwer Academic Publishers, pp. 187–202.
   Google Scholar
• Fravel DR, Marois JJ, Lumsden RD, Connick WJ. Encapsulation of potential biocontrol agents in an alginate-clay matrix. Phytopathology, 1985;75:774–7.
   Web of Science ®Google Scholar
• Fu N, Chen XD. Towards a maximal cell survival in convective thermal drying processes. Food Res Int, 2011;44:1127–49.
   Web of Science ®Google Scholar
• Gancedo C, Delgado MA. Isolation and characterization of a mutant from Saccharomyces cerevisiae lacking fructose 1,6-bisphosphatase. Eur J Biochem, 1984;139:651–5.
   PubMedGoogle Scholar
• Goh CH, Heng PWS, Chan LW. Alginates as a useful natural polymer for microencapsulation and therapeutic applications. Carbohydr Polym, 2012;88:1–12.
   Web of Science ®Google Scholar
• Gombotz WR, Wee SF. Protein release from alginate matrices. Adv Drug Deliv Rev, 1998;31:267–85.
   PubMed Web of Science ®Google Scholar
• Grant WD. Life at low water activity. Philos Trans Royal Soc Lond B Biol Sci, 2004;359:1249–67.
   PubMed Web of Science ®Google Scholar
• Grant GT, Morris ER, Rees DA, Smith PJC, Thom D. Biological interactions between polysaccharides and divalent cations: The egg-box model. FEBS Lett, 1973;32:195–8.
   Web of Science ®Google Scholar
• Haug A, Larsen B, Smidsrod O. A study on the constitution of alginic acid by partial hydrolysis. Acta Chem Scand, 1966;20:183–90.
   Google Scholar
• Heng PWS, Chan LW, Wong TW. Formation of alginate microspheres produced using emulsification technique. J Microencapsul, 2003;20:401–13.
   PubMed Web of Science ®Google Scholar
• Horaczek A, Viernstein H. Comparison of three commonly used drying technologies with respect to activity and longevity of aerial conidia of Beauveria brongniartii and Metarhizium anisopliae. Biol Control, 2004;31:65–71.
   Web of Science ®Google Scholar
• Kabaluk JT, Lafontaine J, Borden JH. An attract and kill tactic for click beetles based on Metarhizium brunneum and a new formulation of sex pheromone. J Pest Sci, 2015;88:707–16.
   Web of Science ®Google Scholar
• Kierstan M, Bucke C. The immobilization of microbial cells, subcellular organelles, and enzymes in calcium alginate gels. Biotechnol Bioeng, 1977;19:387–97.
   PubMed Web of Science ®Google Scholar
• Leach RH, Scott WJ. The influence of rehydration on the viability of dried micro-organisms. J Gen Microbiol, 1959;21:295–307.
   PubMedGoogle Scholar
• Lee P, Rogers MA. Effect of calcium source and exposure-time on basic caviar spherification using sodium alginate. Int J Gastron Food Sci, 2012;1:96–100.
   Google Scholar
• Leland JE, Mullins DE, Vaughan LJ, Warren HL. Effects of media composition on submerged culture spores of the entomopathogenic fungus, Metarhizium anisopliae var. acridum, Part 1: Comparison of cell wall characteristics and drying stability among three spore types. Biocontrol Sci Technol, 2005;15:379–92.
   Web of Science ®Google Scholar
• Leong JY, Lam WH, Ho KW, Voo WP, Lee MFX, Lim HP, Tey BT, Poncelet D, Chan ES. Advances in fabricating spherical alginate hydrogels with controlled particle designs by ionotropic gelation as encapsulation systems. Particuology, 2016;24:44–60.
   Web of Science ®Google Scholar
• Leslie SB, Israeli E, Lighthart B, Crowe JH, Crowe LM. Trehalose and sucrose protect both membranes and proteins in intact bacteria during drying. Appl Environ Microbiol, 1995;61:3592–7.
   PubMed Web of Science ®Google Scholar
• Leslie SB, Teter SA, Crowe LM, Crowe JH. Trehalose lowers membrane phase transitions in dry yeast cells. Biochim Biophys Acta Biomembranes, 1994;1192:7–13.
   PubMed Web of Science ®Google Scholar
• Martinsen A, Skjakbraek G, Smidsrod O. Alginate as immobilization material: I. Correlation between chemical and physical properties of alginate gel beads. Biotechnol Bioeng, 1989;33:79–89.
   PubMed Web of Science ®Google Scholar
• Mater DDG, Jean-Noël B, Edmundo NSJ, Nicole T, Daniel T. Effect of gelation temperature and gel-dissolving solution on cell viability and recovery of two Pseudomonas putida strains co-immobilized within calcium alginate or κ-carrageenan gel beads. Biotechnol Tech, 1995;9:747–52.
   Google Scholar
• Moellering H, Bergmeyer HU. 1988. D-Gluconate (D-glucono-δ-lactone) and D-gluconate 6-phosphate. Cambridge UK: VCH Publishers (UK).
   Google Scholar
• Moore D, Langewald J, Obognon F. Effects of rehydration on the conidial viability of Metarhizium flavoviride mycopesticide formulations. Biocontrol Sci Technol, 1997;7:87–94.
   Web of Science ®Google Scholar
• Morgan CA, Herman N, White PA, Vesey G. Preservation of micro-organisms by drying: A review. J Microbiol Methods, 2006;66:183–93.
   PubMed Web of Science ®Google Scholar
• Mugnier J, Jung G. Survival of bacteria and fungi in relation to water activity and the solvent properties of water in biopolymer gels. Appl Environ Microbiol, 1985;50:108–14.
   PubMed Web of Science ®Google Scholar
• Ouwerx C, Velings N, Mestdagh M, Axelos M. Physico-chemical properties and rheology of alginate gel beads formed with various divalent cations. Polym Gels Netw, 1998;6:393–408.
   Google Scholar
• Parkkinen E, Oura E, Suomalainen H. Comparison of methods for the determination of cell viability in stored baker’s yeast. J Inst Brew, 1976;82:283–5.
   Web of Science ®Google Scholar
• Paul E, Fages J, Blanc P, Goma G, Pareilleux A. Survival of alginate-entrapped cells of Azospirillum lipoferum during dehydration and storage in relation to water properties. Appl Microbiol Biotechnol, 1993;40:34–9.
   Web of Science ®Google Scholar
• Poirier I, Marechal PA, Richard S, Gervais P. Saccharomyces cerevisiae viability is strongly dependant on rehydration kinetics and the temperature of dried cells. J Appl Microbiol, 1999;86:87–92.
   PubMed Web of Science ®Google Scholar
• Posthuma CC, Bader R, Engelmann R, Postma PW, Hengstenberg W, Pouwels PH. Expression of the xylulose 5-phosphate phosphoketolase gene, xpkA, from Lactobacillus pentosus MD363 is induced by sugars that are fermented via the phosphoketolase pathway and is repressed by glucose mediated by CcpA and the mannose phosphoenolpyruvate phosphotransferase system. Appl Environ Microbiol, 2002;68:831–7.
   PubMed Web of Science ®Google Scholar
• Potts M. Desiccation tolerance of prokaryotes. Microbiol Rev, 1994;58:755–805.
   PubMedGoogle Scholar
• Sanyal B, Sengupta C, Poi R, Dasgupta B, Sen C. Survival potential of Trichoderma harzianum in alginate prills. J Biol Control, 2003;17:69–73.
   Google Scholar
• Schoebitz M, Simonin H, Poncelet D. Starch filler and osmoprotectants improve the survival of rhizobacteria in dried alginate beads. J Microencapsul, 2012;29:532–8.
   PubMed Web of Science ®Google Scholar
• Schumann M, Patel A, Vemmer M, Vidal S. The role of carbon dioxide as an orientation cue for western corn rootworm larvae within the maize root system: Implications for an attract-and-kill approach. Pest Manag Sci, 2014;70:642–50.
   PubMed Web of Science ®Google Scholar
• Selmer-Olsen E, Sorhaug T, Birkeland SE, Pehrson R. Survival of Lactobacillus helveticus entrapped in Ca-alginate in relation to water content, storage and rehydration. J Ind Microbiol Biotechnol, 1999;23:79–85.
   PubMed Web of Science ®Google Scholar
• Sinha A, Maitra PK. Induction of specific enzymes of the oxidative pentose phosphate pathway by glucono-δ-lactone in Saccharomyces cerevisiae. J Gen Microbiol, 1992;138:1865–73.
   PubMedGoogle Scholar
• Skinner M, Parker B, Kim J. Role of entomopathogenic fungi in integrated pest management. In: Abrol DP, ed. Integrated pest management: Current concepts and ecological perspective. Amsterdam: Elsevier, pp. 169–191.
   Google Scholar
• Toegel S, Salar-Behzadi S, Horaczek-Clausen A, Viernstein H. Preservation of aerial conidia and biomasses from entomopathogenic fungi Beauveria brongniartii and Metarhizium anisopliae during lyophilization. J Invertebr Pathol, 2010;105:16–23.
   PubMed Web of Science ®Google Scholar
• Turker N, Hamamci H. Storage behaviour of immobilized dried micro-organisms. Food Microbiol, 1998;15:3–11.
   Web of Science ®Google Scholar
• Velings NM, Mestdagh MM. Physico-chemical properties of alginate gel beads. Polym Gels Netw, 1995;3:311–30.
   Google Scholar
• Vemmer M, Patel AV. Review of encapsulation methods suitable for microbial biological control agents. Biol Control, 2013;67:380–9.
   Web of Science ®Google Scholar
• Vemmer M, Schumann M, Beitzen‐Heineke W, French BW, Vidal S, Patel AV. Development of a CO2 releasing co‐formulation based on starch, Saccharomyces cerevisiae and Beauveria bassiana attractive towards western corn rootworm larvae. Pest Manag Sci, 2016;72:2136–45.
   PubMed Web of Science ®Google Scholar
• Walters C, Hill LM, Wheeler LJ. Dying while dry: Kinetics and mechanisms of deterioration in desiccated organisms. Integr Comp Biol, 2005;45:751–8.
   PubMed Web of Science ®Google Scholar
• Wang CS, Hu G, St Leger RJ. Differential gene expression by Metarhizium anisopliae growing in root exudate and host (Manduca sexta) cuticle or hemolymph reveals mechanisms of physiological adaptation. Fungal Genet Biol, 2005;42:704–18.
   PubMed Web of Science ®Google Scholar
• Wolfe J, Bryant G. Freezing, drying, and/or vitrification of membrane- solute-water systems. Cryobiology, 1999;39:103–29.
   PubMed Web of Science ®Google Scholar