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Characterization of Bacillus spharicus binary proteins for biological control of Culex quinquefasciatus mosquitoes: a review

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Review Paper 01/03/2012
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Characterization of Bacillus spharicus binary proteins for biological control of Culex quinquefasciatus mosquitoes: a review

Md. Ataur Rahman, Shakil Ahmed Khan, Md. Tipu Sultan, Md. Rokibul Islam
Int. J. Biosci.2( 3), 1-13, March 2012.
Certificate: IJB 2012 [Generate Certificate]
Key: Bacillus sphaericusBinary proteinBiopesticideCulex quinquefasciatusMosquitocidal

Abstract

The larvicidal action of the entomopathogen Bacillus sphaericus towards Culex quinquefasciatus is due to the binary (Bin) toxin protein present in crystals, which are produced during bacterial sporulation. However, the molecular basis for binary and receptor recognition is not well understood. In this review we attempted to discuss the general biology of this species and concentrate on the genetics and physiology of toxin production and it’s processing for the production of biopesticides. In addition, larvicide of B. sphaericus is unique in that it consists of two proteins of 42 (BinA) and 51(BinB) kDa, both of which are required for toxicity to mosquito larvae midgut and these binary proteins are cleaved by proteases, yielding peptides of 39 kDa and 43 kDa, respectively that form the active toxin. These associate bind to the receptor, a α-glucosidase on the midgut microvilli, and cause lysis of midgut cells after internalization. Besides, Bin toxin can increase the toxicity of other mosquitocidal proteins and may be useful for both increasing the activity of commercial bacterial larvicides. Recently, recombinant DNA techniques have been used to improve bacterial insecticide efficacy by markedly increasing the synthesis of mosquitocidal proteins and by enabling new endotoxin combinations from different bacteria to be produced within single strains. Finally, the availability of Bin toxins of B. sphaericus and newly discovered mosquitocidal protein offers the potential for constructing recombinant bacterial insecticides for more effective biopesticides for the biological control of mosquito vectors.

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Abdullah MAF. 2002. Characterization of toxicity determinants in Bacillus thuringiensis mosquitocidal delta-endotoxins. PhD thesis, Ohio State University, USA.

Adams TT. Eiteman MA. Hanel BM. 2002. Solid state fermentation of broiler litter for production of biocontrol agents. Bioresource Technol 82, 33–41.

Ampofo JA. 1995. Use of local row materials for the production of Bacillus sphaericus insecticide in Ghana. Biocontrol Sci. Technol 5, 417–423.

Baumann P. Baumann L. 1991. Effects of components of the Bacillus sphaericus toxin on mosquito larvae and mosquitocidal-derived tissue culture grown cells. Curr. Microbiol 23, 51–57.

Baumann L. Broadwell AH. Baumann P. 1988. Sequence analysis of the mosquitocidal toxin genes encoding 51.4- and 41.9-kilodalton proteins from Bacillus sphaericus 2362 and 2297. J Bacteriol 170, 2045–2050.

 Baumann P. Clark MA. Baumann L. Broadwell AH. 1991. Bacillus sphaericus as a  mosquito pathogen: Properties of the organism and its toxins. Microbiol. Rev 55, 425–436.

Baumann P. Unterman BM. Baumann L. Broadwell AH. Abbene SJ. Bowditch RD. 1985. Purification of the larvicidal toxin of Bacillus sphaericus and evidence for high-molecular-weight precursors. J Bacteriol 163, 738–747.

Becker N. 2000. Bacterial control of vector-mosquitoes and blackflies. In Entomopathogenic Bacteria: From Laboratory to Field Application. Charles JF. Delécluse A. Nielson-LeRoux C. (eds). Dordrecht, the Netherlands: Kluwer, pp. 383–398.

Berry C. Jackson-Yap J. Oei C. Hindley J. 1989. Nucleotide sequence of two toxin genes from Bacillus  phaericus IAB59: sequence comparisons between five highly toxinogenic strains. Nucleic Acids Res 17, 7516.

Broadwell AH. Baumann P. 1986. Sporulation-associated activation of Bacillus sphaericus larvicide. Appl Environ Microbiol 52, 758–764.

Broadwell AH. Clark MA. Baumann L. Baumann P. 1990. Construction by sitedirected mutagenesis of a 39-kilodalton mosquitocidal protein similar to the larva processed toxin of Bacillus sphaericus 2362. J Bacteriol 172, 4032–4036.

Charles JF. Nielsen-LeRoux C. Delécluse A. 1996. Bacillus sphaericus toxins: molecular biology and mode of action. Annu. Rev. Entomol 41, 451–472.

Charles JF. Silva-Filha MH. Nielsen-LeRoux C. Humphreys MJ. Berry C. 1997. Binding of the 51-and 42-kDa individual components from the Bacillus sphaericus crystal toxin to mosquito larval midgut membranes from Culex and Anopheles sp. (Diptera: Culicidae). FEMS Microbiol Lett 156, 153–159.

Charles JF. Kalfon A. Bourgouin C. de Barjac H. 1988. Bacillus sphaericus asporogenous mutants: morphology, protein pattern and larvicidal activity. Ann Inst Pasteur Microbiol 139, 243–259.

Charles JF. 1987. Ulrastructural midgut events in Culicidae larvae fed with Bacillus sphaericus 2297 spores/crystal complex. Ann. Inst. Past. Microbiol 138, 471–484.

Cheongw C. Yaph H. 1985. Bioassays of Bacillus sphaericus (strain 1593) against mosquitoes of public health importance in Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 16, 54–58.

Claus D. Berkeley RCW. 1986. Genus Bacillus, In Sneath PHA. Mair NS. Sharpe ME. Holt JG. Bergey’s manual of systematic bacteriology, vol. 2. The Williams & Wilkins Co., Baltimore. 31. Dadd RH. 1971. Effects of size and concentration p. 1105–1139.

Darboux I. Nielsen-LeRoux C. Charles JF. Pauchet Y. Pauron D. 2001. The receptor of Bacillus sphaericus binary toxin in C. pipiens (Diptera: Culicidae) midgut: molecular cloning and expression. Insect Biochem. Mol. Biol 31, 981–990.

Davidson E W. 1983. Alkaline extraction of toxin from spores of the mosquito pathogen, Bacillus sphaericus strain 1593. Can J Microbiol 29, 271–275.

Davidson EW. 1988. Binding of the Bacillus sphaericus (Eubacteriales: Bacillaceae) toxin to midgut cells of mosquito (Diptera: Culicidae) larvae: relationship to host range. J. Med. Entomol 25, 151–157.

Davidson EW. 1995. Biochemistry and mode of action of the Bacillus sphaericus toxins. Mem. Inst. Oswaldo Cruz 90, 81–86.

Davidson EW. Urbina M. Payne J. Mulla MS. Darwazeh H. Dulmage HT. Correa A. 1984. Fate of Bacillus sphaericus 1593 and 2362 spores used as larvicides in the aquatic environment. Appl Environ Microbiol 47, 125–129.

Delécluse A. Juarez-Perez V. Berry C. 2000. Vector-active toxins: structure and diversity. In Entomopathogenic Bacteria: from Laboratory to Field Application (ed. J.-F. Charles A. Delécluse C. Nielsen-LaRoux. Dordrecht. The Netherlands: Kluwer.pp. 101–125.

de Barjac H. Thiery I. Cosmao-Dumanoir V. Frachon E. Laurent P. Charles JF. Hamon S. Ofori J. 1988. Another Bacillus sphaericus serotype harbouring strains very toxic to mosquito larvae: serotype H6. Ann Inst Pasteur Microbiol 139, 363–377.

 De Barjac H. 1990. Classification of Bacillus sphaericus strains and comparative toxicity to mosquito larvae. In: Bacterial Control of Mosquitoes and Black Flies (De Barjac H. Southerland D. eds.), pp. 228–236. Rutgers University Press, New Jeresy.

de   Melo   JV.  Vasconcelos    RH.   Furtado  AF. Peixoto CA. Silva-Filha MH. 2008. Ultrastructural analysis of midgut cells from Culex quinquefasciatus (Diptera: Culicidae) larvae resistant to Bacillus sphaericus. Micron 39, 1342–1350.

Federici BA. Park HW. Sakano Y. 2006. Insecticidal protein crystals of Bacillus thuringiensis. In: Shively, J.M. (Ed.), Inclusions in Prokaryotes. Springer-Verlag, Berlin, Heidelberg, Germany, pp. 195–236.

Federici BA. Park HW. Bideshi DK. Wirth MC. Johnson JJ. Sakano Y. Tang M. 2007. Developing recombinant bacteria for control of mosquito larvae. J Am Mosquito Contr 23, 164–175.

Fillinger U. Lindsay SW. 2006. Suppression of exposure to malaria vectors by an order of magnitude using microbial larvicides in rural Kenya. Trop Med Int Health 11, 1629–1642.

Fitz-James PC. Gillespie JB. Loewy D. 1984. A surface net on parasporal inclusions of Bacillus thuringiensis. J. Invertebr. Pathol 43, 47–58.

Foda MS. Ismail IMK. Moharam ME Sadek KHA. 2002. A novel approach for production of Bacillus thuringiensis by solid state fermentation. Egypt. Microbiol 37, 135–156.

Foda MS. El-Bendary MA. Moharam ME. 2003. Salient parameters involved in mosquitocidal toxins production from Bacillus sphaericus by semi-solid substrate fermentation. Egypt. Microbiol 38, 229– 246.

Glare TR. O’Callaghan M. 2000. Bacillus Thruingiensis: Biology, Ecology, and Safety. New York, NY, USA: John Wiley and Sons.

Gordon RE. Haynes WC. Pang CHN. 1973. The genus Bacillus. In: Agricultural Handbook No. 427. Washington, DC: United states Department of Agriculture.

Gunasekaran K. Padmanaban V. Balaraman K. 2000. Development of Wuchereria bancrofti in Culex quinquefasciatus that survived the exposure of sub-lethal dose of Bacillus sphaericus as larvae. Acta Trop 1, 43–49.

Hire RS. Hadapad AB. Dongre TK . Kumar V. Purification and characterization of mosquitocidal Bacillus sphaericus BinA protein. J Invertebr Pathol 101, 106–111.

Hougard JM. Mbentengam R. Lochouarn L. Escaffre H. Darriet F. Barbazan P. Quillevere D. 1993. Campaign against Culex quinquefasciatus using Bacillus sphaericus: results of a pilot project in a large urban area of equatorial Africa. Bull World Health Organ 71, 367–375.

Humphreys MJ. Berry C. 1998. Variants of the Bacillus sphaericus binary toxins: implications for differential toxicity of strains. J. Invert. Pathol 71, 184–185.

Kalfon A. Charles JF. Bourgouin C. de Barjac H. 1984. Sporulation of Bacillus sphaericus 2297: an electron microscope study of crystal-like inclusion biogenesis and toxicity to mosquito larvae.J Gen Microbiol 130, 893–900.

Kramer VL. 1990. Efficacy and persistence of Bacillus sphaericus, Bacillus thuringiensis var. israelensis, and methoprene against Culiseta incidens (Diptera: Culicidae) in tires. J Econ Entomol 83, 1280–1285.

Knowles BH. Eller DJ. 1987. Colloid-osmotic lysis as a general feature of the mechanism of action of Bacillus thuringiensis δ-endotoxin. Biochimica et Biophysica Acta 924, 509–578.

Kotze AC. O’Grady J. Gough JM. Pearson R. Bagnall NH. Kemp DH.      Akhurst RJ. 2005. Toxicity of Bacillus thuringiensis to parasitic and free-living life stages of nematodes parasites of livestock. Int J Parasitol 35, 1013–1022

Kovendan K. Murugan K. Vincent S. Barnard DR. 2011. Studies on larvicidal and pupicidal activity of Leucas aspera Willd. (Lamiaceae) and bacterial insecticide, Bacillus sphaericus, against malarial vector, Anopheles stephensi Liston. (Diptera: Culicidae). Parasitol Res.

Kumar    A.     Sharma     VP.     Thavaselvam     D. Sumodan PK. Kamat RH. Audi SS. Surve BN. 1996. Control of Culex quinquefasciatus with Bacillus sphaericus in Vasco City, Goa. J Am Mosq Control Assoc 12, 409–413.

Krych  VK.  Johnson JL.       Yousten AA. 1980. Deoxyribonucleic acid homologies among strains of Bacillus sphaericus. Int. J. Syst. Bacteriol 30, 476-484.

Lacey LA. Undeen AH. 1986. Microbial control of black flies and mosquitoes. Annu Rev Entomol 31, 265–296.

Lacey LA. 2007. Bacillus thuringiensis serovariety israelensis and Bacillus sphaericus for mosquito control. J. Am. Mosq. Control Assoc 23, 133–163.

Lee YW. Zairi J. 2005. Laboratory evaluation of Bacillus thuringiensis H-14 against Aedes aegypti. Trop Biomed 22, 5–10.

Lee HL. Seleena P. 1991. Fermentation of a Malaysian Bacillus thuringiensis serotype H-14 isolate, a mosquito microbial control agent utilizing local wastes. Southeast Asian J. Trop. Med. Public Health 22, 108–112.

Liu BL. Tzeng YM. 1998. Optimization of growth medium for the production of spores from Bacillus thuringiensis using response surface methodology. Bioprocess Engineering 18, 413–418.

Manceva SD. Pusztai-carey M. Peter. Butko. 2004. Effect of pH and ionic strength on the cytolytic toxin Cyt1A: a fluorescence spectroscopy study. Biochem. Bioph. Acta 1699, 123–130.

Medeiros FP. Santos MA. Regis L. Rios EM. Rolim Neto PJ. 2005. Development of a Bacillus sphaericus tablet formulation and its evaluation as a larvicide in the biological control of Culex quinquefasciatus. Mem Inst Oswaldo Cruz 100, 431– 434

Mittal PK. 2003. Biolarvicides in vector control: challenges and prospects. J. Vect. Borne. Dis 40, 20– 32.

Mulla MS. Federici BA. Darwazeh HA. Ede L. 1982. Field  evaluation  of  the  microbial  insecticide Bacillus thuringiensis serotype H-14 against floodwater mosquitoes. Appl Environ Microbiol 43, 1288–1293.

Mulla MS. Thavara U. Tawatsin A. Chomposri J. Su TY. 2003. Emergence of resistance and resistance management in field populations of tropical Culex quinquefasciatus to the microbial insecticide agent Bacillus sphaericus. J Am Mosq Control Assoc 19, 39–46.

Mulligan FS. Schaefer CH. Wilder WH. 1980. Efficacy and persistence of Bacillus sphaericus and B. thuringiensis H.14 against mosquitoes under laboratory and field conditions. J Econ Entomol 73, 684–688

Mummigatti     SG.     Raghunathan      N.     1990. Influence of media composition on the production of δ-endotoxin by Bacillus thuringiensis var. thuringiensis. J. Invert. Pathol 55, 147–151.

Mwangangi JM. Kahindi SC. Kibe LW. Nzovu JG. Luethy P. Githure JI. Mbogo CM. 2011. Wide-scale application of Bti/Bs biolarvicide in different aquatic habitat types in urban and peri-urban Malindi, Kenya. Parasitol Res 108, 1355–1363

Myers  P.  Yousten  AA.  Davidson  EW.  1979. Comparative studies of the mosquito-larval toxin of Bacillus sphaericus SSII-1 and 1593. Can J Microbiol 25, 1227–1231.

Nicolas L. Dossou-Yovo J. Hougard JM. 1987. Persistence and recycling of Bacillus sphaericus 2362 spores in Culex quinquefasciatus breeding sites in West Africa. Appl Microbiol Biotechnol 25, 341–590.

Obeta JAN. Okafor N. 1983. Production of Bacillus sphaericus 1593 primary powder on media made from locally obtainable Nigerian agriculture products. Can J. Microbiol 29, 704–709.

Oei C. Hindley J. Berry C. 1992. Binding of purified Bacillus sphaericus binary toxin and its deletion derivatives to Culex quinquefasciatus gut: elucidation of functional binding domains. J. Gen. Microbiol 138, 1515–1526.

Paily KP. Agiesh Kumar B. Balaraman K. 2007. Transferrin in the mosquito, Culex quinquefasciatus Say (Diptera: Culicidae), up-regulated upon infection and development of the filarial parasite,Wuchereria bancrofti (Cobbold) (Spirurida: Onchocercidae). Parasitol Res 101, 325–330.

Park HW. Federici BA. 2009. Genetic engineering of bacteria to improve efficacy using the insecticidal proteins of Bacillus species. In: Stock, S.P. (Ed.), Insect Pathogens: Molecular Approaches and Techniques. CABI International, pp. 275–305.

Park HW. Bideshi DK. Wirth MC. Johnson JJ. Walton WE. Federici BA. 2005. Recombinant larvicidal bacteria with markedly improved efficacy against Culex vectors of West Nile virus. Am J Trop Med Hyg 72, 732–738.

Park HW. Bideshi DK. Federici BA. 2010. Properties and applied use of the mosquitocidal bacterium, Bacillus sphaericus. J. Asia– Pac. Entomol 13, 159–168.

Porter   AG.    Davidson    EW.    Liu    JW.   1993. Mosquitocidal toxins of bacilli and their genetic manipulation for effective biological control of mosquitoes. Microbiol Rev 57, 838–861

Priest FG. 1992. Biological control of mosquitoes and other biting flies by Bacillus sphaericus and Bacillus thuringiensis. J. Appl. Bacteriol 72, 357–369.

Raghavendra K. Barik TK. Niranjan Reddy BP. Sharma P. Dash AP. 2011. Malaria vector control: from past to future. Parasitol Res 108, 757–779.

Regis L. Oliveira CM. Silva-Filha MH. Silva SB. Maciel A. Furtado AF. 2000. Efficacy of Bacillus sphaericus in control of the filariasis vector Culex quinquefasciatus in an urban area of Olinda Brazil. Trans R Soc Trop Med Hyg 94, 488–492.

Regis L. Silva-Filha MH. Nielsen-Leroux C. Charles JF. 2001. Bacteriological larvicides of dipteran disease vectors. Trends in Paracitol 17, 377– 380.

Romão TP. de Melo Chalegre. KD. Key S. Ayres CF. Fontes de Oliveira. CM. de-Melo-Neto OP. Silva-Filha MH. 2006. A second independent resistance mechanism to Bacillus sphaericus binary toxin targets its alpha-glucosidase receptor in Culex quinquefasciatus. FEBS J 273, 1556-1568.

Sachdeva V. Tyagi RD. Valero JR. 1999. Factors affecting the production of Bacillus thuringiensis bioinsecticides. Rec. Res. Dev. Microbiol 3, 363–375.

Salama HS. Foda MS. Selim MH. El-Sharaby A. 1983. Utilization of fodder yeast and agro-industrial by-products in production of spores and biologically active endotoxins from Bacillus thuringiensis. Zbl. Mikrobiol 138, 553–563.

Schwartz  JL. Potvin  L.  Coux F.  Charles  JF. Berry C. Humphreys MJ. Jones AF. Bernhart I. Dalla Serra M. Menestrina G. 2001. Permeabilization of model lipid membranes by Bacillus sphaericus mosquitocidal binary toxin and its individual components. J. Membr. Biol 184, 171-183.

Siegel JP. 2001. The mammalian safety of Bacillus thuringiensis based insecticides. J. Invert. Pathol 77, 13–21.

Silva-Filha MH. Oliveira CM. Regis L. Yuan Z. Rico CM. Nielsen-LeRoux C. 2004. Two Bacillus sphaericus binary toxins share the midgut receptor binding site: implications for resistance of Culex pipiens complex (Diptera: Culicidae) larvae. FEMS Microbiol. Lett 241, 185-191.

Singh GJP. Gill SS.1988. An electron microscope study of the toxic action of Bacillus sphaericus in Culex quinquifasciatus larvae. J. Invert. Pathol 52, 237–247.

Singh G. Prakash S. 2009. Efficacy of Bacillus sphaericus against larvae of malaria and filarial vectors: an analysis of early resistance detection. Parasitol Res 104,763–766.

Smith AW. Camara-Artigas A. Brune DC. Allen JP. 2005. Implications of highmolecular-weight oligomers of the binary toxin from Bacillus sphaericus. J. Invert. Pathol 88, 27-33.

Vidyarthi AS. Tyagi RD. Valero JR. Surampalli RY. 2002. Studies on the production of Bacillus thuringiensis based bioinsecticides using wastewater sludge as a raw material. Wat. Res 36, 4850–4860.

WHO. 1985. Informal consultation on the development of Bacillus sphaericus as a microbial larvicide. Special Programme for Research and Training in tropical Diseases. TDR⁄ BCV ⁄ SPHAERICUS ⁄ 85.3.

WHO. 1999. Microbial pest control agent Bacillus thuringiensis. Report of UNEP/ILO/WHO (EHC, 217). WHO, Geneva.

Yousten AA. 1984. Bacillus  sphaericus: microbiological  factors  related  to  its  potential  as  a mosquito larvicide. Adv Biotechnol Processes 3, 315-343.

Yousten AA. Davidson EW. 1982. Ultrastructural Analysis of Spores and Parasporal Crystals Formed by Bacillus sphaericus 2297. Appl Environ Microbiol 44, 1449–1455.

Yuan Z. Zhang Y. Cia Y. Liu EY. 2000. High-level field resistance to Bacillus sphaericus C3-41 in Culex quinquefasciatus from southern China. Biocontrol Sci Technol 10, 41–49.

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