Skip to main content

Resistance of Mosquitoes to Entomopathogenic Bacterial-Based Larvicides: Current Status and Strategies for Management

  • Chapter
  • First Online:
Bacillus thuringiensis and Lysinibacillus sphaericus

Abstract

The entomopathogenic bacteria Bacillus thuringiensis serovar. israelensis (Bti) and Lysinibacillus sphaericus have successfully been used to control insects of public health relevance, including those from the genera Aedes, Anopheles, Culex, and Simulium. These bacteria display a specific mode of action that relies on unique interactions which makes them the most selective agents currently available to control Diptera larvae. They produce crystalline insecticidal proteins that act on the larval midgut through their interaction with specific receptors. L. sphaericus presents a single major larvicidal factor, the binary (Bin) protoxin, whose action relies on the binding to one class of receptors, while Bti crystals contain four main protoxins (Cry4Aa, Cry4Ba, Cry11Aa, Cyt1Aa) which display interactions with a group of distinct midgut receptor molecules. The mode of action of L. sphaericus displays a greater potential for resistance selection, compared to Bti which has no record of insect resistance to date. These major mosquitocidal toxins and their interaction with midgut target sites, as well as resistance issues related to their utilization, are summarized in this chapter.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Amorim LB, Oliveira CMF, Rios EM, Regis L, Silva-Filha MHNL (2007) Development of Culex quinquefasciatus resistance to Bacillus sphaericus strain IAB59 needs long term selection pressure. Biol Control 42:155–160

    Article  Google Scholar 

  • Amorim LB, De Barros RA, Chalegre KD, De Oliveira CM, Regis LN, Silva-Filha MH (2010) Stability of Culex quinquefasciatus resistance to Bacillus sphaericus evaluated by molecular tools. Insect Biochem Mol Biol 40:311–316

    Article  CAS  PubMed  Google Scholar 

  • Anderson JF, Ferrandino FJ, Dingman DW, Main AJ, Andreadis TG, Becnel JJ (2011) Control of mosquitoes in catch basins in Connecticut with Bacillus thuringiensis israelensis, Bacillus sphaericus, [corrected] and spinosad. J Am Mosq Control Assoc 27:45–55

    Article  PubMed  Google Scholar 

  • Anilkumar KJ, Pusztai-Carey M, Moar WJ (2008) Fitness costs associated with Cry1Ac-resistant Helicoverpa zea (Lepidoptera: Noctuidae): a factor countering selection for resistance to Bt cotton? J Econ Entomol 101:1421–1431

    Article  PubMed  Google Scholar 

  • Araujo AP, Araujo Diniz DF, Helvecio E, De Barros RA, De Oliveira CM, Ayres CF, De Melo-Santos MA, Regis LN, Silva-Filha MH (2013) The susceptibility of Aedes aegypti populations displaying temephos resistance to Bacillus thuringiensis israelensis: a basis for management. Parasit Vectors 6:297

    Article  PubMed  PubMed Central  Google Scholar 

  • Arredondo-Jimenez JI, Lopez T, Rodriguez MH, Bown DN (1990) Small scale field trials of Bacillus sphaericus (strain 2362) against anopheline and culicine mosquito larvae in southern Mexico. J Am Mosq Control Assoc 6:300–305

    CAS  PubMed  Google Scholar 

  • Bayyareddy K, Andacht TM, Abdullah MA, Adang MJ (2009) Proteomic identification of Bacillus thuringiensis subsp. israelensis toxin Cry4Ba binding proteins in midgut membranes from Aedes (Stegomyia) aegypti Linnaeus (Diptera, Culicidae) larvae. Insect Biochem Mol Biol 39:279–286

    Article  CAS  PubMed  Google Scholar 

  • Becker N, Petric D, Dahl C, Lane J, Kaiser A (2003) Integrated pest management. In: Becker N (ed) Mosquitos and their control. Kluwer Academic/Plenum Publishers, New York, pp 417–424

    Chapter  Google Scholar 

  • Beltrão BM, Silva-Filha MH (2007) Interaction of Bacillus thuringiensis svar. israelensis Cry toxins with binding sites from Aedes aegypti (Diptera: Culicidae) larvae midgut. FEMS Microbiol Lett 266:163–169

    Article  CAS  Google Scholar 

  • Berry C (2012) The bacterium, Lysinibacillus sphaericus, as an insect pathogen. J Invertebr Pathol 109:1–10

    Article  PubMed  Google Scholar 

  • Berry C, Hindley J, Ehrhardt AF, Grounds T, De Souza I, Davidson EW (1993) Genetic determinants of host ranges of Bacillus sphaericus mosquito larvicidal toxins. J Bacteriol 175:510–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berry C, O'neil S, Ben-Dov E, Jones AF, Murphy L, Quail MA, Holden MT, Harris D, Zaritsky A, Parkhill J (2002) Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol 68:5082–5095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boonserm P, Davis P, Ellar DJ, Li J (2005) Crystal structure of the mosquito-larvicidal toxin Cry4Ba and its biological implications. J Mol Biol 348:363–382

    Article  CAS  PubMed  Google Scholar 

  • Bravo A, Gómez I, Conde J, Muñoz-Garay C, Sánchez J, Miranda R, Zhuang M, Gill SS, Soberón M (2004) Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochim Biophys Acta 1667:38–46

    Article  CAS  PubMed  Google Scholar 

  • Bravo A, Gill SS, Soberón M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49:423–435

    Article  CAS  PubMed  Google Scholar 

  • Bravo A, Likitvivatanavong S, Gill SS, Soberón M (2011) Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol 41:423–431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broadwell AH, Baumann L, Baumann P (1990) Larvicidal properties of the 42 and 51 kilodalton Bacillus sphaericus proteins expressed in different bacterial hosts: evidence for a binary toxin. Curr Microbiol 21:361–366

    Article  CAS  Google Scholar 

  • Cadavid-Restrepo G, Sahaza J, Orduz S (2012) Treatment of an Aedes aegypti colony with the Cry11Aa toxin for 54 generations results in the development of resistance. Mem Inst Oswaldo Cruz 107:74–79

    Article  CAS  PubMed  Google Scholar 

  • Cancino-Rodezno A, Alexander C, Villasenor R, Pacheco S, Porta H, Pauchet Y, Soberon M, Gill SS, Bravo A (2010) The mitogen-activated protein kinase p38 is involved in insect defense against Cry toxins from Bacillus thuringiensis. Insect Biochem Mol Biol 40:58–63

    Article  CAS  PubMed  Google Scholar 

  • Cancino-Rodezno A, Lozano L, Oppert C, Castro JI, Lanz-Mendoza H, Encarnacion S, Evans AE, Gill SS, Soberon M, Jurat-Fuentes JL, Bravo A (2012) Comparative proteomic analysis of Aedes aegypti larval midgut after intoxication with Cry11Aa toxin from Bacillus thuringiensis. PLoS One 7:e37034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantón PE, Zanicthe Reyes EZ, Ruiz De Escudero I, Bravo A, Soberón M (2011) Binding of Bacillus thuringiensis subsp. israelensis Cry4Ba to Cyt1Aa has an important role in synergism. Peptides 32:595–600

    Article  PubMed  CAS  Google Scholar 

  • Cetin H, Oz E, Yanikoglu A, Cilek JE (2015) Operational evaluation of Vectomax(R) WSP (Bacillus thuringiensis subsp. israelensis+Bacillus sphaericus) against larval Culex pipiens in septic tanks. J Am Mosq Control Assoc 31:193–195

    Google Scholar 

  • Chalegre KD, Romão TP, Amorim LB, Anastacio DB, De Barros RA, De Oliveira CM, Regis L, De-Melo-Neto OP, Silva-Filha MH (2009) Detection of an allele conferring resistance to Bacillus sphaericus binary toxin in Culex quinquefasciatus populations by molecular screening. Appl Environ Microbiol 75:1044–1049

    Article  CAS  PubMed  Google Scholar 

  • Chalegre KD, Romão TP, Tavares DA, Santos EM, Ferreira LM, Oliveira CMF, De-Melo-Neto OP, Silva-Filha MHNL (2012) Novel mutations associated to Bacillus sphaericus resistance are identified in a polymorphic region of the Culex quinquefasciatus cqm1 gene. Appl Environ Microbiol 78:6321–6326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chalegre KD, Tavares DA, Romao TP, Menezes HSG, Nascimento AL, Oliveira CMF, De-Melo-Neto OP, Silva-Filha MHNL (2015) Co-selection and replacement of resistance alleles to Lysinibacillus sphaericus in a Culex quinquefasciatus colony. FEBS J 282:3592–3602

    Google Scholar 

  • Charles JF (1987) Ultrastructural midgut events in Culicidae larvae fed with Bacillus sphaericus 2297 spore/crystal complex. Ann Inst Pasteur Microbiol 138:471–484

    Article  CAS  PubMed  Google Scholar 

  • Charles JF, Nielsen-Leroux C, Delecluse A (1996) Bacillus sphaericus toxins: molecular biology and mode of action. Annu Rev Entomol 41:451–472

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Chevillon C, Bernard C, Marquine M, Pasteur N (2001) Resistance to Bacillus sphaericus in Culex pipiens (Diptera: Culicidae): interaction between recessive mutants and evolution in southern France. J Med Entomol 38:657–664

    Article  CAS  PubMed  Google Scholar 

  • Colletier JP, Sawaya MR, Gingery M, Rodriguez JA, Cascio D, Brewster AS, Michels-Clark T, Hice RH, Coquelle N, Boutet S, Williams GJ, Messerschmidt M, Deponte DP, Sierra RG, Laksmono H et al (2016) De novo phasing with X-ray laser reveals mosquito larvicide BinAB structure. Nature 539:43–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crickmore N, Bone EJ, Wiliams JA, Ellar DJ (1995) Contribution of the individual components of the delta-endotoxin crystal to the mosquitocidal activity of Bacillus thuringiensis subs. israelensis. FEMS Microbiol Lett 131:249–254

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Darboux I, Pauchet Y, Castella C, Silva-Filha MH, Nielsen-Leroux C, Charles JF, Pauron D (2002) Loss of the membrane anchor of the target receptor is a mechanism of bioinsecticide resistance. Proc Natl Acad Sci U S A 99:5830–5835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darboux I, Charles JF, Pauchet Y, Warot S, Pauron D (2007) Transposon-mediated resistance to Bacillus sphaericus in a field-evolved population of Culex pipiens (Diptera: Culicidae). Cell Microbiol 9:2022–2029

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Davidson EW (1989) Variation in binding of Bacillus sphaericus toxin and wheat germ agglutinin to larval midgut cells of six species of mosquitoes. J Invertebr Pathol 53:251–259

    Article  CAS  PubMed  Google Scholar 

  • De Barjac H (1978) A new variety of Bacillus thuringiensis very toxic to mosquitoes: B. thuringiensis var. israelensis serotype 14. C R Seances Hebdomadaires Acad Sci Ser D 286:797–800

    Google Scholar 

  • De Maagd RA, Bravo A, Berry C, Crickmore N, Schnepf HE (2003) Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Ann Rev Genet 37:409–433

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dritz DA, Lawler SP, Evkhanian C, Graham P, Baracosa V, Dula G (2011) Control of mosquito larvae in seasonal wetlands on a wildlife refuge using VectoMax CG. J Am Mosq Control Assoc 27:398–403

    Article  PubMed  Google Scholar 

  • Du Y, Nomura Y, Satar G, Hu Z, Nauen R, He SY, Zhorov BS, Dong K (2013) Molecular evidence for dual pyrethroid-receptor sites on a mosquito sodium channel. Proc Natl Acad Sci U S A 110:11785–11790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Federici BA, Park HD, Bideshi DK (2010) Overview of the basic biology of Bacillus thuringiensis with emphasis on genetic engineering of bacterial larvicides for mosquito control. Open J Toxicol 3:83–100

    Google Scholar 

  • Ferreira LM, Silva-Filha MHNL (2013) Bacterial larvicides for vector control: mode of action of toxins and implications for resistance. Biocontrol Sci Tech 23:1137–1168

    Article  Google Scholar 

  • Ferreira LM, Romão TP, De-Melo-Neto OP, Silva-Filha MH (2010) The orthologue to the Cpm1/Cqm1 receptor in Aedes aegypti is expressed as a midgut GPI-anchored alpha-glucosidase, which does not bind to the insecticidal binary toxin. Insect Biochem Mol Biol 40:604–610

    Article  CAS  PubMed  Google Scholar 

  • Ferreira LM, Romão TP, Nascimento NA, Costa MD, Rezende AM, De-Melo-Neto OP, Silva-Filha MH (2014) Non conserved residues between Cqm1 and Aam1 mosquito alpha-glucosidases are critical for the capacity of Cqm1 to bind the Binary (Bin) toxin from Lysinibacillus sphaericus. Insect Biochem Mol Biol 50:34–42

    Article  CAS  PubMed  Google Scholar 

  • Gabrisko M (2013) Evolutionary history of eukaryotic alpha-glucosidases from the alpha-amylase family. J Mol Evol 76:129–145

    Article  CAS  PubMed  Google Scholar 

  • Gahan LJ, Pauchet Y, Vogel H, Heckel DG (2010) An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet 6:e1001248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gammon K, Jones GW, Hope SJ, De Oliveira CM, Regis L, Silva Filha MH, Dancer BN, Berry C (2006) Conjugal transfer of a toxin-coding megaplasmid from Bacillus thuringiensis subsp. israelensis to mosquitocidal strains of Bacillus sphaericus. Appl Environ Microbiol 72:1766–1770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Georghiou GP, Wirth MC (1997) Influence of exposure to single versus multiple toxins of Bacillus thuringiensis subsp. israelensis on development of resistance in the mosquito Culex quinquefasciatus (Diptera: Culicidae). Appl Environ Microbiol 63:1095–1101

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giraldo-Calderon GI, Perez M, Morales CA, Ocampo CB (2008) Evaluation of the triflumuron and the mixture of Bacillus thuringiensis plus Bacillus sphaericus for control of the immature stages of Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae) in catch basins. Biomedica 28:224–233

    Article  PubMed  Google Scholar 

  • Goldberg LH, Margalit J (1978) A bacterial spore demonstrating rapid larvicidal activity against Anopheles segentii, Uranotaenia unguiculata, Culex univitatus, Aedes aegypti and Culex pipiens. Mosq News 37:355–358

    Google Scholar 

  • Guidi V, Luthy P, Tonolla M (2013) Comparison between diflubenzuron and a Bacillus thuringiensis israelensis- and Lysinibacillus sphaericus-based formulation for the control of mosquito larvae in urban catch basins in Switzerland. J Am Mosq Control Assoc 29:138–145

    Article  PubMed  Google Scholar 

  • Guillet P, Kurtak DC, Phillipon B, Meyer R (1990) Use of Bacillus thuringiensis for onchocerciasis control in West Africa. In: De Barjac H, Sutherland D (eds) Bacterial control of mosquitoes and black-flies, 1st edn. Rutgers University Press, New Brunswick, pp 187–201

    Google Scholar 

  • Guo QY, Cai QX, Yan JP, Hu XM, Zheng DS, Yuan ZM (2013) Single nucleotide deletion of cqm1 gene results in the development of resistance to Bacillus sphaericus in Culex quinquefasciatus. J Insect Physiol 59:967–973

    Article  CAS  PubMed  Google Scholar 

  • Hertlein MB, Mavrotas C, Jousseaume C, Lysandrou M, Thompson GD, Jany W, Ritchie SA (2010) A review of spinosad as a natural product for larval mosquito control. J Am Mosq Control Assoc 26:67–87

    Article  CAS  PubMed  Google Scholar 

  • Hofte H, Whiteley HR (1989) Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol Rev 53:242–255

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hurst TP, Brown MD, Kay BH, Ryan PA (2006) Evaluation of Melanotaenia duboulayi (Atheriniformes: Melanotaeniidae), Hypseleotris galli (Perciformes: Eleotridae), and larvicide VectoLex WG (Bacillus sphaericus) for integrated control of Culex annulirostris. J Am Mosq Control Assoc 22:418–425

    Article  PubMed  Google Scholar 

  • Kale A, Hire RS, Hadapad AB, D'souza SF, Kumar V (2013) Interaction between mosquito-larvicidal Lysinibacillus sphaericus binary toxin components: analysis of complex formation. Insect Biochem Mol Biol 43:1045–1054

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kamgang B, Marcombe S, Chandre F, Nchoutpouen E, Nwane P, Etang J, Corbel V, Paupy C (2011) Insecticide susceptibility of Aedes aegypti and Aedes albopictus in Central Africa. Parasit Vectors 4:79

    Article  PubMed  PubMed Central  Google Scholar 

  • Keiser J, Maltese MF, Erlanger TE, Bos R, Tanner M, Singer BH, Utzinger J (2005) Effect of irrigated rice agriculture on Japanese encephalitis, including challenges and opportunities for integrated vector management. Acta Trop 95:40–57

    Article  PubMed  Google Scholar 

  • Knowles BH, Ellar DJ (1987) Colloid-osmotic lysis is a general feature of the mechanism of action of Bacillus thuringiensis δ-endotoxins with different insect specificity. Biochim Biophys Acta 924:507–518

    Google Scholar 

  • Krasikov VV, Karelov DV, Firsov LM (2001) Alpha-glucosidases. Biochemistry (Mosc) 66:267–281

    Article  CAS  Google Scholar 

  • Lacey L (2007) Bacillus thuringiensis serovariety israelensis and Bacillus sphaericus for mosquito control. J Am Mosq Control Assoc 23:133–163

    Article  CAS  PubMed  Google Scholar 

  • Likitvivatanavong S, Chen J, Evans AM, Bravo A, Soberón M, Gill SS (2011) Multiple receptors as targets of Cry toxins in mosquitoes. J Agric Food Chem 59:2829–2838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lingenfelser A, Rydzanicz K, Kaiser A, Becker N (2010) Mosquito fauna and perspectives for integrated control of urban vector-mosquito populations in southern Benin (West Africa). Ann Agric Environ Med 17:49–57

    PubMed  Google Scholar 

  • Liu H, Cupp EW, Guo A, Liu N (2004) Insecticide resistance in Alabama and Florida mosquito strains of Aedes albopictus. J Med Entomol 41:946–952

    Article  CAS  PubMed  Google Scholar 

  • Loke SR, Andy-Tan WA, Benjamin S, Lee HL, Sofian-Azirun M (2010) Susceptibility of field-collected Aedes aegypti (L.) (Diptera: Culicidae) to Bacillus thuringiensis israelensis and temephos. Trop Biomed 27:493–503

    CAS  PubMed  Google Scholar 

  • Marcombe S, Darriet F, Agnew P, Etienne M, Yp-Tcha MM, Yebakima A, Corbel V (2011) Field efficacy of new larvicide products for control of multi-resistant Aedes aegypti populations in Martinique (French West Indies). AmJTrop Med Hyg 84:118–126

    Article  Google Scholar 

  • Marcombe S, Farajollahi A, Healy SP, Clark GG, Fonseca DM (2014) Insecticide resistance status of United States populations of Aedes albopictus and mechanisms involved. PLoS One 9:e101992

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Margalit J, Dean D (1985) The story of Bacillus thuringiensis var. israelensis (B.t.i.) J Am Mosq Control Assoc 1:1–7

    CAS  PubMed  Google Scholar 

  • Menezes HSG, Chalegre KD, Romao TP, Oliveira CMF, De-Melo-Neto OP, Silva-Filha MHNL (2016) A new allele conferring resistance to Lysinibacillus sphaericus is detected in low frequency in Culex quinquefasciatus field populations. Parasit Vectors 9:1–7

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Nicolas L, Nielsen-Leroux C, Charles JF, Delécluse A (1993) Respective role of the 42- and 51-kDa components of the Bacillus sphaericus toxin overexpressed in Bacillus thuringiensis. FEMS Microbiol Lett 106:275–280

    Article  CAS  PubMed  Google Scholar 

  • Nielsen-Leroux C, Charles JF (1992) Binding of Bacillus sphaericus binary toxin to a specific receptor on midgut brush-border membranes from mosquito larvae. Eur J Biochem 210:585–590

    Article  CAS  PubMed  Google Scholar 

  • Nielsen-Leroux C, Charles JF, Thiery I, Georghiou GP (1995) Resistance in a laboratory population of Culex quinquefasciatus (Diptera: Culicidae) to Bacillus sphaericus binary toxin is due to a change in the receptor on midgut brush-border membranes. Eur J Biochem 228:206–210

    Article  CAS  PubMed  Google Scholar 

  • Nielsen-Leroux C, Pasquier F, Charles JF, Sinegre G, Gaven B, Pasteur N (1997) Resistance to Bacillus sphaericus involves different mechanisms in Culex pipiens (Diptera: Culicidae) larvae. J Med Entomol 34:321–327

    Article  CAS  PubMed  Google Scholar 

  • Nielsen-Leroux C, Pasteur N, Pretre J, Charles JF, Sheikh HB, Chevillon C (2002) High resistance to Bacillus sphaericus binary toxin in Culex pipiens (Diptera: Culicidae): the complex situation of West Mediterranean countries. J Med Entomol 39:729–735

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Oliveira CMF, Silva-Filha MH, Nielsen-Leroux C, Pei G, Yuan Z, Regis L (2004) Inheritance and mechanism of resistance to Bacillus sphaericus in Culex quinquefasciatus (Diptera: Culicidae) from China and Brazil. J Med Entomol 41:58–64

    Article  CAS  PubMed  Google Scholar 

  • Opota O, Charles JF, Warot S, Pauron D, Darboux I (2008) Identification and characterization of the receptor for the Bacillus sphaericus binary toxin in the malaria vector mosquito, Anopheles gambiae. Comp Biochem Physiol -Part B Biochem Mol Biol 149:419–427

    Article  CAS  Google Scholar 

  • Opota O, Gauthier NC, Doye A, Berry C, Gounon P, Lemichez E, Pauron D (2011) Bacillus sphaericus binary toxin elicits host cell autophagy as a response to intoxication. PLoS One 6:e14682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paris M, Tetreau G, Laurent F, Lelu M, Després L, David JP (2011) Persistence of Bacillus thuringiensis israelensis (Bti) in the environment induces resistance to multiple Bti toxins in mosquitoes. Pest Manag Sci 67:122–128

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Pauchet Y, Luton F, Castella C, Charles JF, Romey G, Pauron D (2005) Effects of a mosquitocidal toxin on a mammalian epithelial cell line expressing its target receptor. Cell Microbiol 7:1335–1344

    Article  CAS  PubMed  Google Scholar 

  • Paul A, Harrington LC, Zhang L, Scott JG (2005) Insecticide resistance in Culex pipiens from New York. J Am Mosq Control Assoc 21:305–309

    Article  CAS  PubMed  Google Scholar 

  • Pei G, Oliveira CM, Yuan Z, Nielsen-Leroux C, Silva-Filha MH, Yan J, Regis L (2002) A strain of Bacillus sphaericus causes slower development of resistance in Culex quinquefasciatus. Appl Environ Microbiol 68:3003–3009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez C, Fernandez LE, Sun J, Folch JL, Gill SS, Soberón M, Bravo A (2005) Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proc Natl Acad Sci U S A 102:18303–18308

    Google Scholar 

  • Pérez C, Muñoz-Garay C, Portugal LC, Sánchez J, Gill SS, Soberón M, Bravo A (2007) Bacillus thuringiensis ssp. israelensis Cyt1Aa enhances activity of Cry11Aa toxin by facilitating the formation of a pre-pore oligomeric structure. Cell Microbiol 9:2931–2937

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pigott CR, Ellar DJ (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev 71:255–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pocquet N, Darriet F, Zumbo B, Milesi P, Thiria J, Bernard V, Toty C, Labbe P, Chandre F (2014) Insecticide resistance in disease vectors from Mayotte: an opportunity for integrated vector management. Parasit Vectors 7:299

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rao DR, Mani TR, Rajendran R, Joseph AS, Gajanana A, Reuben R (1995) Development of a high level of resistance to Bacillus sphaericus in a field population of Culex quinquefasciatus from Kochi. India J Am Mosq Control Assoc 11:1–5

    CAS  PubMed  Google Scholar 

  • Regis L, Silva-Filha MH, Nielsen-Leroux C, Charles JF (2001) Bacteriological larvicides of dipteran disease vectors. Trends Parasitol 17:377–380

    Article  CAS  PubMed  Google Scholar 

  • Rinkevich FD, Du Y, Dong K (2013) Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pestic Biochem Physiol 106:93–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodcharoen J, Mulla MS (1994) Resistance development in Culex quinquefasciatus to the microbial agent Bacillus sphaericus. J Econ Entomol 87:1133–1140

    Article  Google Scholar 

  • Rodcharoen J, Mulla MS, Chaney JD (1991) Microbial larvicides for the control of nuisance aquatic midges (Diptera: Chironomidae) inhabiting mesocosms and man-made lakes in California. J Am Mosq Control Assoc 7:56–62

    CAS  PubMed  Google Scholar 

  • Rodrigues IB, Tadei WP, Dias JM (1999) Larvicidal activity of Bacillus sphaericus 2362 against Anopheles nuneztovari, Anopheles darlingi and Anopheles braziliensis (Diptera, Culicidae). Rev Inst Med Trop Sao Paulo 41:101–105

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Romão TP, De-Melo-Neto OP, Silva-Filha MH (2011) The N-terminal third of the BinB subunit from the Bacillus sphaericus binary toxin is sufficient for its interaction with midgut receptors in Culex quinquefasciatus. FEMS Microbiol Lett 321:167–174

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Silva Filha MHNL, Peixoto CA (2003) Immunocytochemical localization of the Bacillus sphaericus toxin components in Culex quinquefasciatus (Diptera: Culicidae) larvae midgut. Pestic Biochem Physiol 77:138–146

    Article  CAS  Google Scholar 

  • Silva Filha MHNL, Berry C, Regis LN (2014) Lysinibacillus sphaericus: toxins and mode of action, applications for mosquito control and resistance management. In: Dhadialla TS, Gill SS (eds) Insect midgut and insecticidal proteins. Academic Press, Oxford, pp 89–176

    Chapter  Google Scholar 

  • Silva-Filha MH, Nielsen-Leroux C, Charles JF (1997) Binding kinetics of Bacillus sphaericus binary toxin to midgut brush-border membranes of Anopheles and Culex sp. mosquito larvae. Eur J Biochem 247:754–761

    Article  CAS  PubMed  Google Scholar 

  • Silva-Filha MH, Nielsen-Leroux C, Charles JF (1999) Identification of the receptor for Bacillus sphaericus crystal toxin in the brush border membrane of the mosquito Culex pipiens (Diptera: Culicidae). Insect Biochem Mol Biol 29:711–721

    Article  CAS  PubMed  Google Scholar 

  • Silva-Filha MHNL, Chalegre KD, Anastacio DB, Oliveira CMF, Silva SB, Acioli RV, Hibi S, Oliveira DC, Parodi ESM, Marques Filho CAM, Furtado AF, Regis L (2008) Culex quinquefasciatus field populations subjected to treatment with Bacillus sphaericus did not display high resistance levels. Biol Control 44:227–234

    Article  Google Scholar 

  • Sinègre G, Babinot M, Vigo G, Jullien JL (1994) First occurrence of Culex pipiens resistance to Bacillus sphaericus in Southern France. VIII European Meeting of Society of Vector Ecology 5–8 September 1994. Faculty of Biologia. University of Barcelona Spain, Barcelona

    Google Scholar 

  • Singh GJ, Gill SS (1988) An electron microscope study of the toxic action of Bacillus sphaericus in Culex quinquefasciatus larvae. J Invertebr Pathol 52:237–247

    Article  CAS  PubMed  Google Scholar 

  • Singkhamanan K, Promdonkoy B, Srikhirin T, Boonserm P (2013) Amino acid residues in the N-terminal region of the BinB subunit of Lysinibacillus sphaericus binary toxin play a critical role during receptor binding and membrane insertion. J Invertebr Pathol 114:65–70

    Article  CAS  PubMed  Google Scholar 

  • Soberón M, Fernández LE, Pérez C, Gill SS, Bravo A (2007) Mode of action of mosquitocidal Bacillus thuringiensis toxins. Toxicon 49:597–600

    Article  PubMed  CAS  Google Scholar 

  • Srisucharitpanit K, Yao M, Promdonkoy B, Chimnaronk S, Tanaka I, Boonserm P (2014) Crystal structure of BinB: a receptor binding component of the binary toxin from Lysinibacillus sphaericus. Proteins 82:2703–2712

    Article  CAS  PubMed  Google Scholar 

  • Stalinski R, Laporte F, Tetreau G, Despres L (2016) Receptors are affected by selection with each Bacillus thuringiensis israelensis Cry toxin but not with the full Bti mixture in Aedes aegypti. Infect Genet Evol 44:218–227

    Article  CAS  PubMed  Google Scholar 

  • Tangsongcharoen C, Chomanee N, Promdonkoy B, Boonserm P (2015) Lysinibacillus sphaericus binary toxin induces apoptosis in susceptible Culex quinquefasciatus larvae. J Invertebr Pathol 128:57–63

    Article  CAS  PubMed  Google Scholar 

  • Tetreau G, Bayyareddy K, Jones CM, Stalinski R, Riaz MA, Paris M, David JP, Adang MJ, Despres L (2012) Larval midgut modifications associated with Bti resistance in the yellow fever mosquito using proteomic and transcriptomic approaches. BMC Genomics 13:248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tetreau G, Stalinski R, David JP, Despres L (2013a) Increase in larval gut proteolytic activities and Bti resistance in the dengue fever mosquito. Arch Insect Biochem Physiol 82:71–83

    Article  CAS  PubMed  Google Scholar 

  • Tetreau G, Stalinski R, David JP, Despres L (2013b) Monitoring resistance to Bacillus thuringiensis subsp. israelensis in the field by performing bioassays with each Cry toxin separately. Mem Inst Oswaldo Cruz 108:894–900

    Article  PubMed  PubMed Central  Google Scholar 

  • Torres-Martinez M, Rubio-Infante N, Garcia-Hernandez AL, Nava-Acosta R, Ilhuicatzi-Alvarado D, Moreno-Fierros L (2016) Cry1Ac toxin induces macrophage activation via ERK1/2, JNK and p38 mitogen-activated protein kinases. Int J Biochem Cell Biol 78:106–115

    Article  CAS  PubMed  Google Scholar 

  • Vachon V, Laprade R, Schwartz JL (2012) Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review. J Invert Pathol 111:1–12

    Article  CAS  Google Scholar 

  • Vasquez MI, Violaris M, Hadjivassilis A, Wirth MC (2009) Susceptibility of Culex pipiens (Diptera: Culicidae) field populations in Cyprus to conventional organic insecticides, Bacillus thuringiensis subsp. israelensis, and methoprene. J Med Entomol 46:881–887

    Article  CAS  PubMed  Google Scholar 

  • Wirth MC (2010) Mosquito resistance to bacterial larvicidal proteins. Open J Toxicol 3:101–115

    CAS  Google Scholar 

  • Wirth MC, Georghiou GP, Malik JI, Abro GH (2000) Laboratory selection for resistance to Bacillus sphaericus in Culex quinquefasciatus (Diptera: Culicidae) from California. USA J Med Entomol 37:534–540

    Article  CAS  PubMed  Google Scholar 

  • Wirth MC, Ferrari JA, Georghiou GP (2001) Baseline susceptibility to bacterial insecticides in populations of Culex pipiens complex (Diptera: Culicidae) from California and from the Mediterranean Island of Cyprus. J Econ Entomol 94:920–928

    Article  CAS  PubMed  Google Scholar 

  • Yuan ZM, Zhang YM, Liu EY (2000) High-level field resistance to Bacillus sphaericus C3-41 in Culex quinquefasciatus from southern China. Biocontrol Sci Tech 10:43–51

    Article  Google Scholar 

  • Zahiri NS, Mulla MS (2003) Susceptibility profile of Culex quinquefasciatus (Diptera: Culicidae) to Bacillus sphaericus on selection with rotation and mixture of B. sphaericus and B. thuringiensis israelensis. J Med Entomol 40:672–677

    Google Scholar 

  • Zhang X, Candas M, Griko NB, Taussig R, Bulla LA Jr (2006) A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci U S A 103:9897–9902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Helena Neves Lobo Silva-Filha .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Silva-Filha, M.H.N.L. (2017). Resistance of Mosquitoes to Entomopathogenic Bacterial-Based Larvicides: Current Status and Strategies for Management. In: Fiuza, L., Polanczyk, R., Crickmore, N. (eds) Bacillus thuringiensis and Lysinibacillus sphaericus. Springer, Cham. https://doi.org/10.1007/978-3-319-56678-8_15

Download citation

Publish with us

Policies and ethics