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Efficacy of Lysinibacillus sphaericus against mixed-cultures of field-collected and laboratory larvae of Aedes aegypti and Culex quinquefasciatus

Published online by Cambridge University Press:  22 May 2018

J.C. Santana-Martinez
Affiliation:
Departamento de Ciencias Biológicas, Centro de Investigaciones Microbiológicas (CIMIC), Universidad de los Andes, Bogotá, Colombia
J.J. Silva
Affiliation:
Departamento de Ciencias Biológicas, Centro de Investigaciones Microbiológicas (CIMIC), Universidad de los Andes, Bogotá, Colombia Department of Entomology, University of Cornell, Ithaca, New York, USA
J. Dussan*
Affiliation:
Departamento de Ciencias Biológicas, Centro de Investigaciones Microbiológicas (CIMIC), Universidad de los Andes, Bogotá, Colombia
*
*Author for correspondence Phone: +57-1-3394949 (ext. 3644) E-mail: jdussan@uniandes.edu.co

Abstract

Lysinibacillus sphaericus (Bacillales: Planococcaceae) is a spore-forming bacillus used for the biological control of mosquitoes (Diptera: Culicidae) due to its larvicidal activity determined by various toxins and S-layer protein produced either during sporulation or by the vegetative cell. Aedes aegypti and Culex quinquefasciatus are the vectors of arboviruses that cause tropical diseases representing a current public health problem. Both species may coexist in the same larval development sites and are susceptible to the larvicidal activity of L. sphaericus. In this study, we compared the larvicidal effects of L. sphaericus 2362 (WHO Reference strain) and native strains III(3)7 and OT4b.25 against Cx. quinquefasciatus and Ae. aegypti in single-species and mixed-culture bioassays. Findings showed that L. sphaericus spores, vegetative cells and a combination thereof possessed high larvicidal activity against Cx. quinquefasciatus larvae, whereas only the formulation of L. sphaericus vegetative cells was effective against Ae. aegypti larvae. Similar results were obtained for field-collected larvae. We propose that a formulation of vegetative cells of L. sphaericus 2362 or III(3)7 could be a good alternative to chemical insecticides for the in situ control of mixed populations of Ae. aegypti and Cx. quinquefasciatus.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2018 

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References

Ali, M.Y.S., Ravikumar, S. & Beula, J.M. (2013) Mosquito larvicidal activity of seaweeds extracts against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus. Asian Pacific Journal of Tropical Disease 3, 196201.Google Scholar
Barrera, R., Amador, M., Diaz, A., Smith, J., Muñoz-Jordan, J.L. & Rosario, Y. (2008) Unusual productivity of Aedes aegypti in septic tanks and its implications for dengue control. Medical and Veterinary Entomology 22, 6269.Google Scholar
Baumann, P., Clark, M.A., Baumann, L. & Broadwell, A.H. (1991) Bacillus sphaericus as a mosquito pathogen: properties of the organism and its toxins. Microbiological Reviews 55, 425436.Google Scholar
Berry, C. (2012). The bacterium, Lysinibacillus sphaericus, as an insect pathogen. Journal of Invertebrate Pathology 109, 110.Google Scholar
Bhatt, S., Gething, P.W., Brady, O.J., Messina, J.P., Farlow, A.W., Moyes, C.L., Drake, J.M., Brownstein, J.S., Hoen, A.G., Sankoh, O., Myers, M.F., George, D.B., Jaenisch, T., Wint, G.R.W., Simmons, C.P., Scott, T.W., Farrar, J.J. & Hay, S.I. (2013) The global distribution and burden of dengue. Nature 496, 504507.Google Scholar
Bhattacharya, S. & Basu, P. (2016) The southern house mosquito, Culex quinquefasciatus: profile of a smart vector. Journal of Entomology and Zoology Studies 4, 7381.Google Scholar
Bisset, J.A., Magdalena, M.R., Fernandez, D. & Perez, O. (2004) Status of resistance to insecticides and resistance mechanisms in larvae from Playa municipality collected during the intensive campaign against Aedes aegypti in Havana City, 2001–2002. Revista Cubana de Medicina Tropical 56, 6166.Google Scholar
Boeuf, P., Drummer, H.E., Richards, J.S., Scoullar, M.J. & Beeson, J.G. (2016) The global threat of Zika virus to pregnancy: epidemiology, clinical perspectives, mechanisms, and impact. BMC Medicine 14, 112.Google Scholar
Burke, R., Barrera, R., Lewis, M., Kluchinsky, T. & Claborn, D. (2010) Septic tanks as larval habitats for the mosquitoes Aedes aegypti and Culex quinquefasciatus in Playa-Playita, Puerto Rico. Medical and Veterinary Entomology 24, 117123.Google Scholar
Campbell, G.L., Hills, S.L., Fischer, M., Jacobson, J.A., Hoke, C.H., Hombach, J.M., Marfin, A.A., Solomon, T., Tsai, T.F., Tsu, V.D. & Ginsburg, A.S. (2011) Estimated global incidence of Japanese encephalitis: a systematic review. Bulletin of the World Health Organization 89, 766774.Google Scholar
Chalegre, K.D., Romão, T.P., Tavares, D.A., Santos, E.M., Ferreira, L.M., Oliveira, C.M., de-Melo-Neto, O.P. & Silva-Filha, M.H. (2012) Novel mutations associated with resistance to Bacillus sphaericus in a polymorphic region of the Culex quinquefasciatus cqm1 gene. Applied and Environmental Microbiology 78, 63216326.Google Scholar
Chancey, C., Grinev, A., Volkova, E. & Rios, M. (2015) The global ecology and epidemiology of West Nile virus. BioMed Research International 2015, 120.Google Scholar
Charles, J.F., Nielson-LeRoux, C. & Delécluse, A. (1996) Bacillus sphaericus toxins: molecular biology and mode of action. Annual Review of Entomology 41, 451472.Google Scholar
Correa, M. & Yousten, A.A. (1995) Bacillus sphaericus spore germination and recycling in mosquito larval cadavers. Journal of Invertebrate Pathology 66, 7681.Google Scholar
Darboux, I., Nielsen-LeRoux, C., Charles, J.F. & Pauron, D. (2001) The receptor of Bacillus sphaericus binary toxin in Culex pipiens (Diptera: Culicidae) midgut: molecular cloning and expression. Insect Biochemistry and Molecular Biology 31, 981990.Google Scholar
Davidson, E.W. (1988) Binding of the Bacillus sphaericus (Eubacteriales: Bacillaceae) toxin to midgut cells of mosquito (Diptera: Culicidae) larvae: relationship to host range. Journal of Medical Entomology 25, 151157.Google Scholar
Davidson, E.W. (1989) Variation in binding of Bacillus sphaericus toxin and wheat germ agglutinin to larval midgut cells of six species of mosquitoes. Journal of Invertebrate Pathology 53, 251259.Google Scholar
Diaz, L.A., Quaglia, A.I., Konigheim, B.S., Boris, A.S., Aguilar, J.J., Komar, N. & Contigiani, M.S. (2016) Activity patterns of St. Louis encephalitis and West Nile viruses in free ranging birds during a human encephalitis outbreak in Argentina. PLoS ONE 11, e0161871.Google Scholar
Fonseca-González, I., Quiñones, M.L., Lenhart, A. & Brogdon, W.G. (2011) Insecticide resistance status of Aedes aegypti (L.) from Colombia. Pest Management Science 67,430437.Google Scholar
Garske, T., Van Kerkhove, M.D., Yactayo, S., Ronveaux, O., Lewis, R.F., Staples, J.E., Perea, W. & Ferguson, N.M. & Yellow Fever Expert Committee. (2014) Yellow fever in Africa: estimating the burden of disease and impact of mass vaccination from outbreak and serological data. PLoS Medicine 11, e1001638.Google Scholar
Gualdron, L.J. (2007) Manual de vigilancia entomologica de Dengue, Leishmaniasis, Chagas, Malaria y Fiebre Amarilla. Health Secretariat of Santander, ETV Program, 511.Google Scholar
Guo, Q.Y., Cai, Q.X., Yan, J.P., Hu, X.M., Zheng, D.S. & Yuan, Z.M. (2013) Single nucleotide deletion of cqm1 gene results in the development of resistance to Bacillus sphaericus in Culex quinquefasciatus. Journal of Insect Physiology 59, 967973.Google Scholar
Korkmaz, S., Goksuluk, D. & Zararsiz, G. (2014) MVN: an R package for assessing multivariate normality. The R Journal 6, 151163.Google Scholar
Leisnham, P.T., LaDeau, S.L. & Juliano, S.A. (2014) Spatial and temporal habitat segregation of mosquitoes in urban Florida. PLoS ONE 9, e91655.Google Scholar
Lekakarn, H., Promdonkoy, B. & Boonserm, P. (2015) Interaction of Lysinibacillus sphaericus binary toxin with mosquito larval gut cells: binding and internalization. Journal of Invertebrate Pathology 132, 125131.Google Scholar
Lima, J.B.P., Da-Cunha, M.P., Júnior, R.C.D.S., Galardo, A.K.R., Soares, S.D.S., Braga, I.A., Pimentel, R. & Valle, D. (2003) Resistance of Aedes aegypti to organophosphates in several municipalities in the state of Rio de Janeiro and Espirito Santo, Brazil. The American Journal of Tropical Medicine and Hygiene 68, 329333.Google Scholar
Liu, J.W., Porter, A.G., Wee, B.Y. & Thanabalu, T. (1996) New gene from nine Bacillus sphaericus strains encoding highly conserved 35.8-kilodalton mosquitocidal toxins. Applied and Environmental Microbiology 62, 21742176.Google Scholar
Lozano, L.C. & Dussán, J. (2013) Metal tolerance and larvicidal activity of Lysinibacillus sphaericus. World Journal of Microbiology & Biotechnology 29, 13831389.Google Scholar
Lozano, L.C. & Dussán, J. (2017) Synergistic activity between S-layer protein and spore–crystal preparations from Lysinibacillus sphaericus against Culex quinquefasciatus larvae. Current Microbiology 74, 371376.Google Scholar
Lozano, L.C., Ayala, J.A. & Dussán, J. (2011) Lysinibacillus sphaericus S-layer protein toxicity against Culex quinquefasciatus. Biotechnology Letters 33, 20372041.Google Scholar
Marchler-Bauer, A., Lu, S., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., De Weese-Scott, C., Fong, J.H., Geer, L.Y., Geer, R.C., Gonzales, N.R., Gwadz, M., Hurwitz, D.I., Jackson, J.D., Ke, Z., Lanczycki, C.J., Lu, F., Marchler, G.H., Mullokandov, M., Omelchenko, M.V., Robertson, C.L., Song, J.S., Thanki, N., Yamashita, R.A., Zhang, D., Zhang, N., Zheng, C. & Bryant, S.H. (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Research 39, D225D229.Google Scholar
Nielsen-Leroux, C. & Charles, J.F. (1992) Binding of Bacillus sphaericus binary toxin to a specific receptor on midgut brush-border membranes from mosquito larvae. European Journal of Biochemistry 210, 585590.Google Scholar
Nielsen-Leroux, C., Charles, J.F., Thiery, I. & Georghiou, G.P. (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. European Journal of Biochemistry 228, 206210.Google Scholar
Obándo, R.G., Gamboa, F., Perafán, O., Suárez, M.F. & Lerma, J.M. (2007). Experiencia de un análisis entomológico de criaderos de Aedes aegypti y Culex quinquefasciatus en Cali, Colombia/Experience of an entomological analysis of the breeding sites of Aedes aegypti and Culex quinquefasciatus in Cali, Colombia. Revista Colombiana de Entomología 33, 148156.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. Microbiology 138, 15151526.Google Scholar
Peña, G., Miranda-Rios, J., de la Riva, G., Pardo-López, L., Soberón, M. & Bravo, A. (2006) A Bacillus thuringiensis S-layer protein involved in toxicity against Epilachna varivestis (Coleoptera: Coccinellidae). Applied Environmental Microbiology 72, 353360.Google Scholar
Petersen, L.R. & Roehrig, J.T. (2001) West Nile virus: a reemerging global pathogen. Emerging Infectious Diseases 7, 611614.Google Scholar
Promdonkoy, B., Promdonkoy, P., Tanapongpipat, S., Luxananil, P., Chewawiwat, N., Audtho, M. & Panyim, S. (2004) Cloning and characterization of a mosquito larvicidal toxin produced during vegetative stage of Bacillus sphaericus 2297. Current Microbiology 49, 8488.Google Scholar
R Core Team (2012) R: A Language and Environment for Statistical Computing [online]. Vienna, Austria, R Foundation for Statistical Computing. ISBN 3-900051-07-0. Available online at http://www.Rproject.org/ (accessed 5 July 2016).Google Scholar
Reisen, W.K. (2003) Epidemiology of St. Louis encephalitis virus. Advances in Virus Research 61, 139184.Google Scholar
Rios, A.A., Machado-Allison, C.E., Rabinovich, J.E. & Rodriguez, D.J. (1978) Competencia intra e interespecífica en Aedes aegypti (L.) y Culex fatigans (Wiedemann) (Diptera: Culicidae) en condiciones de laboratorio. Acta Cientifica Venezolana 29, 467472.Google Scholar
Rocco, I.M., Santos, C.L., Bisordi, I., Petrella, S.M., Pereira, L.E., Souza, R.P., Marti, A.T., Barbosa, V.M., Cerroni, M.P., Katz, G. & Suzuki, A. (2005) St. Louis encephalitis virus: first isolation from a human in São Paulo state, Brasil. Revista do Instituto de Medicina Tropical de São Paulo 47, 281285.Google Scholar
Rozendaal, J.A. (1997) Vector Control: Methods for use by Individuals and Communities. Geneva, World Health Organization.Google Scholar
Rueda, L.M., Patel, K.J., Axtell, R.C. & Stinner, R.E. (1990) Temperature-dependent development and survival rates of Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 27, 892898.Google Scholar
Rungrod, A., Tjahaja, N.K., Soonsanga, S., Audtho, M. & Promdonkoy, B. (2009) Bacillus sphaericus Mtx1 and Mtx2 toxins co-expressed in Escherichia coli are synergistic against Aedes aegypti larvae. Biotechnology Letters 31, 551555.Google Scholar
Santacoloma, L., Chaves, B. & Brochero, H.L. (2012) Estado de la susceptibilidad de poblaciones naturales del vector del dengue a insecticidas en trece localidades de Colombia. Biomédica 32, 333343.Google Scholar
Santana-Martínez, J.C., Molina, J. & Dussán, J. (2017). Asymmetrical competition between Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae) coexisting in breeding sites. Insects 8, 111.Google Scholar
Schaffner, F., Medlock, J.M. & Bortel, W.V. (2013) Public health significance of invasive mosquitoes in Europe. Clinical Microbiology and Infection 19, 685692.Google Scholar
Silva-Filha, M.H., Nielsen-LeRoux, C. & Charles, J.F. (1999) Identification of the receptor for Bacillus sphaericus crystal toxin in the brush border membrane of the mosquito Culex pipiens (Diptera: Culicidae). Insect Biochemistry and Molecular Biology 29, 711721.Google Scholar
Staples, J.E. & Fischer, M. (2014) Chikungunya virus in the Americas – what a vectorborne pathogen can do. New England Journal of Medicine 371, 887889.Google Scholar
Thanabalu, T. & Porter, A.G. (1995) Efficient expression of a 100-kilodalton mosquitocidal toxin in protease-deficient recombinant Bacillus sphaericus. Applied and Environmental Microbiology 61, 40314036.Google Scholar
Thanabalu, T. & Porter, A.G. (1996) A Bacillus sphaericus gene encoding a novel type of mosquitocidal toxin of 31.8 kDa. Gene 170, 8589.Google Scholar
Thanabalu, T., Hindley, J., Jackson-Yap, J. & Berry, C. (1991) Cloning, sequencing, and expression of a gene encoding a 100-kilodalton mosquitocidal toxin from Bacillus sphaericus SSII-1. Journal of Bacteriology 173, 27762785.Google Scholar
Thanabalu, T., Berry, C. & Hindley, J. (1993) Cytotoxicity and ADP-ribosylating activity of the mosquitocidal toxin from Bacillus sphaericus SSII-1: possible roles of the 27-and 70-kilodalton peptides. Journal of Bacteriology 175, 23142320.Google Scholar
U.S. Environmental Protection Agency. (2015) TRAP: Toxicity Relationship Analysis Program [online]. Mid-Continent Ecology Division. Available online at http://www.epa.gov/med/Prods_Pubs/trap.htm (Accessed 10 December 2015).Google Scholar
Van Driesche, R., Hoddle, M. & Center, T. (2009) Control of Pests and Weeds by Natural Enemies: An Introduction to Biological Control. Malden, MA, USA, John Wiley & Sons, Blackwell, pp. 48.Google Scholar