Skip to main content
SpringerLink
Log in

Parasitic Endosymbiosis

  • Chapter
  • First Online:
Invertebrate Bacteriology

  • 798 Accesses

Abstract

Processes accounting for the insurgence of parasitism are reviewed, including evolutionary mechanisms and Red Queen Model effects. Genetic races and host-parasite coevolution involve virulence and infectivity, with a concomitant role of environmental factors. Selective processes are active within host-parasite interactions, and their effects include the selection of different mechanisms of resistance, host immune response and tolerance. Host cuticle is the first physical barrier to pathogens invasion protecting many invertebrates and integrated by other resistance mechanisms. Several bacteria, including Bacillus thuringiensis and other taxa, are reviewed for the production and properties of a wide array of toxins. Factors related to pathogenicity, virulence and specificity of diseases are discussed. A number of invertebrate diseases are described from different groups involved in primary productions, including crustaceans, molluscs, insects and nematodes.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

Notes

  1. 1.

    In “Through the Looking-Glass” the Red Queen game antagonist tells Alice to run, if she wants to maintain her position (“in this place it takes all the running you can do, to keep in the same place”).

  2. 2.

    Epigenetics : it indicates the transmission to the progeny of a trait which is not coded by genes , but is based on different conditions, like DNA methylation or presence of small, non-coding RNA molecules affecting the gene expression patterns.

  3. 3.

    The Cry toxin classes were initially indicated by roman numbers, accounting for the target insect groups (i.e. I for lepidopterans; II for lepidopterans and dipterans; III for coleopterans or IV for dipterans). This classification has been abandoned in favor of a sequence -based system, due to the increased number of variants with dual targets, the lack of toxicity shown by some proteins and the number of specificity assays required for description of any new toxin.

  4. 4.

    Operon = a cluster of genes including promoting and regulatory elements with coordinated expression , typical of prokaryotes.

  5. 5.

    Apoptosis = programmed cell death.

  6. 6.

    Pleiotropy = property of a gene that affects multiple phenotypic traits.

  7. 7.

    Latin for orally.

References

  • Abdel-Hameed, A., Lounatmaa, K., Carlberg, G., & El-Tayeb, O. M. (1990). Studies on Bacillus thuringiensis H-14 strains isolated in Egypt II. Ultrastructure studies. World Journal of Microbiology and Biotechnology, 6, 305–312.

    Article  CAS  PubMed  Google Scholar 

  • Abdoarrahem, M. M., Gammon, K., Dancer, B. N., & Berry, C. (2009). Genetic basis for alkaline activation of germination in Bacillus thuringiensis subsp. israelensis. Applied and Environmental Microbiology, 1, 75–19.

    Google Scholar 

  • Abebe, E., Abebe-Akele, F., Morrison, J., Cooper, V., & Thomas, W. K. (2011). An insect pathogenic symbiosis between a Caenorhabditis and Serratia. Virulence, 2, 158–161.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ahmed, H. K., Mitchell, W. J., & Priest, F. G. (1995). Regulation of mosquitocidal toxin synthesis in Bacillus sphaericus. Applied Environmental Microbiology, 43, 310–314.

    CAS  Google Scholar 

  • Ahmed, I., Yokota, A., Yamazoe, A., & Fujiwara, T. (2007). Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and transfer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus comb. nov. International Journal of Systematic and Evolutionary Microbiology, 57, 1117–1125. doi:10.1099/ijs.0.63867-0.

    Article  CAS  PubMed  Google Scholar 

  • Altermatt, F., & Ebert, D. (2008). Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecology Letters, 11, 918–928.

    Article  PubMed  Google Scholar 

  • Aronson, A., Beckman, W., & Dunn, P. (1976). Bacillus thuringiensis and related insect pathogens. Microbiological Reviews, 50, 1–24.

    Google Scholar 

  • Auld, S. K. J. R., Hall, S. R., & Duffy, M. A. (2012). Epidemiology of a Daphnia-multiparasite system and its implications for the Red Queen. PLoS ONE, 7, e39564.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayoade, F., Oyejide, N. E., & Fayemi, S. O. (2014). Isolation, identification, antibiogram and characterization of bacterial pathogens of the silkworm, Bombyx mori, in South-West Nigeria. Journal of Biological Sciences, 14, 425–430.

    Article  Google Scholar 

  • Baldini, R. L., Lau, G. W., & Rahme, L. G. (2002). Use of plants and insect hosts to model bacterial pathogenesis. In Bacterial pathogenesis, Part C: Identification, regulation and function of virulence factors (Methods in enzymology, 358, pp. 3–13). San Diego: Academic Press.

    Chapter  Google Scholar 

  • Barboza-Corona, J. E., Lopez-Meza, J. E., & Ibarra, J. E. (1998). Cloning and expression of the crylEa4 gene of Bacillus thuringiensis and the comparative toxicity of its gene product. World Journal of Microbiology and Biotechnology, 14, 437–441.

    Article  CAS  Google Scholar 

  • Bechtel, D. B., & Bulla, L. A., Jr. (1976). Electron microscope study of sporulation and parasporal crystal formation in Bacillus thuringiensis. Journal of Bacteriology, 127, 1472–1481.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Benoit, T. G., Newnam, K. A., & Wilson, G. R. (1995). Correlation between alkaline activation of Bacillus thuringiensis var. kurstaki spores and crystal production. Current Microbiology, 31, 301–303.

    Article  CAS  Google Scholar 

  • Bérénos, C., Wegner, K. M., & Schmid-Hempel, P. (2010). Antagonistic coevolution with parasites maintains host genetic diversity: An experimental test. Proceedings of the Royal Society B, 278, 218–224.

    Article  PubMed  PubMed Central  Google Scholar 

  • Berry, C. (2012). The bacterium, Lysinibacillus sphaericus, as an insect pathogen. Journal of Invertebrate Pathology, 109, 1–10. doi:10.1016/j.jip.2011.11.008.

    Article  PubMed  Google Scholar 

  • Berry, C., et al. (2002). Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israelensis. Applied Environmental Microbiology, 68, 5082–5095.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bishop, A. H., Gowen, S. R., Pembroke, B., & Trotter, J. R. (2007). Morphological and molecular characteristics of a new species of Pasteuria parasitic on Meloidogyne ardenensis. Journal of Invertebrate Pathology, 96, 28–33.

    Article  CAS  PubMed  Google Scholar 

  • Boehs, G., Villalba, A., Ceuta, L. O., & Luz, J. R. (2010). Parasites of three commercially exploited bivalve mollusc species of the estuarine region of the Cachoeira river (Ilhéus, Bahia, Brazil). Journal of Invertebrate Pathology, 103, 43–47.

    Article  PubMed  Google Scholar 

  • Bose, J., & Schulte, R. D. (2014). Testing G × G interactions between coinfecting microbial parasite genotypes within hosts. Frontiers in Genetics, 5, 124.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bossé, M., Masson, L., & Brousseau, R. (1990). Nucleotide sequence of a novel crystal protein gene isolated from Bacillus thuringiensis subspecies kenyae. Nucleic Acids Research, 18, 7443.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bower, S. M., McGladdery, S. E., & Price, I. M. (1994). Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annual Review of Fish Diseases, 4, 1–199.

    Article  Google Scholar 

  • Bravo, A., & Soberón, M. (2008). How to cope with resistance to Bt toxins? Trends in Biotechnology, 26, 573–579.

    Article  CAS  PubMed  Google Scholar 

  • Bravo, A., Gill, S. S., & 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, S. S., & Soberón, M. (2011). Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochemistry and Molecular Biology, 41, 423–431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brey, P. T., et al. (1993). Role of the integument in insect immunity: Epicuticular abrasion and induction of cecropin synthesis in cuticular epithelial cells. Proceedings of the National Academy of Sciences, USA, 90, 6275–6279.

    Article  CAS  Google Scholar 

  • Brizzard, B. L., & Whiteley, H. R. (1988). Nucleotide sequence of an additional crystal protein gene cloned from Bacillus thuringiensis subsp. thuringiensis. Nucleic Acids Research, 16, 2723–2724.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brockhurst, M. A., Rainey, P. B., & Buckling, A. (2004). The effect of spatial heterogeneity and parasites on the evolution of host diversity. Proceedings of the Royal Society of London B: Biological Sciences, 271, 107–111.

    Article  Google Scholar 

  • Brown, K. L., & Whiteley, H. R. (1992). Molecular characterization of two novel crystal protein genes from Bacillus thuringiensis subsp. thompsoni. Journal of Bacteriology, 174, 549–557.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown, S. E., Cao, A. T., Hines, E. R., Akhurst, R. J., & East, P. D. (2004). A novel secreted protein toxin from the insect pathogenic bacterium Xenorhabdus nematophila. The Journal of Biological Chemistry, 279, 14595–14601.

    Article  CAS  PubMed  Google Scholar 

  • Buchanan, J. S. (1978). Cytological studies on a new species of rickettsia found in association with a phage in the digestive gland of the marine mollusk, Tellina tenuis. Journal of Fish Diseases, 1, 27–43.

    Article  Google Scholar 

  • Buchon, N., Broderick, N. A., & Lemaitre, B. (2013). Gut homeostasis in a microbial world: Insights from Drosophila melanogaster. Nature Reviews Microbiology, 11, 615–626.

    Article  CAS  PubMed  Google Scholar 

  • Buckling, A., & Rainey, P. B. (2002). The role of parasites in sympatric and allopatric host diversification. Nature, 420, 496–499.

    Article  CAS  PubMed  Google Scholar 

  • Burgents, J. E., Burnett, K. G., & Burnett, L. E. (2004). Disease resistance of Pacific white shrimp, Litopenaeus vannamei, following the dietary administration of a yeast culture food supplement. Aquaculture, 231, 1–8.

    Article  Google Scholar 

  • Burnell, A. M., & Stock, P. S. (2000). Heterorhabditis, Steinernema and their bacterial symbionts—Lethal pathogens of insects. Nematology, 2, 31–42.

    Article  Google Scholar 

  • Byers, D. L. (2005). Evolution in heterogeneous environments and the potential of maintenance of genetic variation in traits of adaptive significance. Genetica, 123, 107–124.

    Article  PubMed  Google Scholar 

  • Cáceres-Martínez, J., Vásquez-Yeomans, R., & Flores-Saaib, R. D. (2011). Intracellular prokaryote Xenohaliotis californiensis in abalone Haliotis spp. from Baja California, México. Ciencia Pesquera, 19, 5–11.

    Google Scholar 

  • Chak, K. F., & Chen, J. C. (1993). Complete nucleotide sequence and identification of a putative promoter region for the expression in Escherichia coli of the cryIA(b) gene from Bacillus thuringiensis var. aizawai HD133. Proceedings of the National Science Council, Republic of China, 17, 7–14.

    CAS  Google Scholar 

  • Chambers, J. A., et al. (1991). Isolation and characterization of a novel insecticidal crystal protein gene from Bacillus thuringiensis subsp. aizawai. Journal of Bacteriology, 173, 3966–3976.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chan, S. W., Thanabalun, T., Wee, B. Y., & Porter, A. G. (1996). Unusual amino acid determinants of host range in the Mtx2 family of mosquitocidal toxins. Journal of Biological Chemistry, 271, 14183–14187.

    Article  CAS  PubMed  Google Scholar 

  • Chang, C. F., et al. (1999). Effect of dietary beta-1,3-glucan on resistance to white spot syndrome virus (WSSV) in postlarval and juvenile Penaeus monodon. Diseases of Aquatic Organisms, 36, 163–168.

    Article  CAS  Google Scholar 

  • Cheng, T., et al. (2014). Complete genome sequence of Bacillus bombysepticus, a pathogen leading to Bombyx mori Black Chest Septicemia. Genome Announcements, 2, e00312–e00314.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ciancio, A. (1995). Phenotypic adaptations in Pasteuria spp. nematode parasites. Journal of Nematology, 27, 328–338.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clark, T. B., et al. (1985). Spiroplasma melliferum, a new species from the honeybee (Apis mellifera). International Journal of Systematic Bacteriology, 35, 296–308.

    Article  CAS  Google Scholar 

  • Comps, M., & Tigé, G. (1999). Procaryotic infections in the mussel Mytilus galloprovincialis and its parasite the turbellarian Urastoma cyprinae. Diseases of Aquatic Organisms, 38, 211–217.

    Article  Google Scholar 

  • Costa Argôlo-Filho, R., & Lopes Loguercio, L. (2014). Bacillus thuringiensis is an environmental pathogen and host-specificity has developed as an adaptation to human-generated ecological niches. Insects, 5, 62–91.

    Article  Google Scholar 

  • Cremonte, F., Balseiro, P., & Figueras, A. (2005). Occurrence of Perkinsus olseni (Protozoa: Apicomplexa) and other parasites in the venerid commercial clam Pitar rostrata from Uruguay, southwestern Atlantic coast. Diseases of Aquatic Organisms, 64, 85–90.

    Article  PubMed  Google Scholar 

  • Crickmore, N., et al. (1998). Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiology and Molecular Biology Reviews, 62, 807–813.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crickmore, N., et al. (2016). Bacillus thuringiensis toxin nomenclature. http://www.btnomenclature.info/.

  • Curtis, R. H. C., Jones, J. T., Davies, K. G., Sharon, E., & Spiegel, Y. (2011). Plant nematode surface. In K. G. Davies & Y. Spiegel (Eds.), Biological control of plant-parasitic nematodes: Building coherence between microbial ecology and molecular mechanisms (pp. 115–144). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Darboux, I., et al. (2002). Loss of the membrane anchor of the target receptor is a mechanism of bioinsecticide resistance. Proceedings of the National Academy of Science, USA, 99, 5830–5835.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Davies, K. G. (2009). Understanding the interaction between an obligate hyperparasitic bacterium, Pasteuria penetrans and its obligate plant-parasitic nematode host, Meloidogyne spp. Advances in Parasitology, 68, 211–245.

    Article  PubMed  Google Scholar 

  • De Barjac, H., & Frachon, E. (1990). Classification of Bacillus thuringiensis strains. Entomophaga, 35, 233–240.

    Article  Google Scholar 

  • Debro, L., Fitz-James, P. C., & Aronson, A. (1986). Two different parasporal inclusions are produced by Bacillus thuringiensis subsp. finitimus. Journal of Bacteriology, 165, 258–268.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Decaestecker, E., Vergote, A., Ebert, D., & De Meester, L. (2003). Evidence for strong host clone-parasite species interactions in the Daphnia microparasite system. Evolution, 57, 784–792.

    Article  PubMed  Google Scholar 

  • Decaestecker, E., et al. (2007). Host–parasite ‘Red Queen’ dynamics archived in pond sediment. Nature, 450, 870–873.

    Article  CAS  PubMed  Google Scholar 

  • Delécluse, A., Rosso, M. L., & Ragni, A. (1995). Cloning and expression of a novel toxin gene from Bacillus thuringiensis subsp. jegathesan encoding a highly mosquitocidal protein. Applied Environmental Microbiology, 61, 4230–4235.

    PubMed  PubMed Central  Google Scholar 

  • Delécluse, A., Juarez-Perez, V., & Berry, C. (2000). Vector-active toxins: Structure and diversity. In J. F. Charles, A. Delécluse, & C. Nielsen-LaRoux (Eds.), Entomopathogenic bacteria: From laboratory to field application (pp. 101–125). Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Díaz Sánchez, A. A., et al. (2014). Bacterias patógenas de larvas de Bombyx mori L. en áreas de reproducción en Cuba. Revista de Protección Vegetal, 29, 216–219.

    Google Scholar 

  • Dieppois, G., Opota, O., Lalucat, J., & Lemaitre, B. (2015). Pseudomonas entomophila: A versatile bacterium with entomopathogenic properties. In J. L. Ramos et al. (Eds.), Pseudomonas (pp. 25–49). Dordrecht: Springer.

    Google Scholar 

  • Djukic, M., Poehlein, A., Thürmer, A., & Daniel, R. (2011). Genome sequence of Brevibacillus laterosporus LMG 15441, a pathogen of invertebrates. Journal of Bacteriology, 193, 5535–5536.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Djukic, M., et al. (2014). How to kill the honey bee larva: Genomic potential and virulence mechanisms of Paenibacillus larvae. PLoS ONE, 9, e90914. doi:10.1371/journal.pone.0090914.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ebert, D. (2008). Host–parasite coevolution: Insights from the Daphnia–parasite model system. Current Opinion in Microbiology, 11, 290–301.

    Article  CAS  PubMed  Google Scholar 

  • Ebert, D., Rainey, P., Embley, T. M., & Scholz, D. (1996). Development, life cycle, ultrastructure and phylogenetic position of Pasteuria ramosa Metchnikoff 1888: Rediscovery of an obligate endoparasite of Daphnia magna Straus. Philosophical Transactions of the Royal Society of London, Series B, 351, 1689–1701.

    Article  Google Scholar 

  • Escobar, M. M., Carbonell, G. V., Beriam, L. O., Siqueira, W. J., & Yano, T. (2001). Cytotoxin production in phytopathogenic and entomopathogenic Serratia marcescens. Revista Latinoamericana de Microbiología, 43, 165–170.

    CAS  PubMed  Google Scholar 

  • Esnard, J., Potter, T. L., & Zuckerman, B. M. (1995). Streptomyces costaricanus sp. nov., isolated from nematode-suppressive soil. International Journal of Systematic Bacteriology, 45, 775–779.

    Article  CAS  PubMed  Google Scholar 

  • Estruch, J. J., et al. (1996). Vip3A, a novel Bacillus thuringiensis vegetative insecticidal protein with a wide spectrum of activities against lepidopteran insects. Proceedings of the National Academy of Sciences, USA, 93, 5389–5394.

    Article  CAS  Google Scholar 

  • Farrar, R. R., Martin, P. A. W., & Ridgway, R. L. (2001). A strain of Serratia marcescens (Enterobacteriaceae) with high virulence per os to larvae of a laboratory colony of the corn earworm (Lepidoptera: Noctuidae). Journal of Entomological Sciences, 36, 380–390.

    Google Scholar 

  • Federici, B. A., Park, H. W., & Sakano, Y. (2006). Insecticidal protein crystals of Bacillus thuringiensis. In J. M. Shively (Ed.), Inclusions in prokaryotes (pp. 196–236). Berlin: Springer-Verlag.

    Google Scholar 

  • Fedhilaa, S., et al. (2010). Comparative analysis of the virulence of invertebrate and mammalian pathogenic bacteria in the oral insect infection model Galleria mellonella. Journal of Invertebrate Pathology, 103, 24–29.

    Article  Google Scholar 

  • Feitelson, J. S. (1993). The Bacillus thuringiensis family tree. In L. Kim (Ed.), Advanced engineered pesticides (pp. 63–71). New York: Marcel Dekker.

    Google Scholar 

  • Feng, K. C., Liu, B. L., Chan, H. S., & Tzeng, Y. M. (2001). Morphology of a spectrum of parasporal endotoxin crystals from cultures of Bacillus thuringiensis ssp. kurstaki isolate A3-4. World Journal of Microbiology and Biotechnology, 17, 119–123.

    Article  Google Scholar 

  • ffrench-Constant, R. H., Eleftherianos, I., & Reynolds, S. E. (2007). A nematode symbiont sheds light on invertebrate immunity. Trends in Parasitology, 23, 514–517.

    Article  CAS  PubMed  Google Scholar 

  • Flegel, T., Pasharawipas, T., Owens, L., & Oakey, H. J. (2005). Evidence for phage-induced virulence in the shrimp pathogen Vibrio harveyi. In P. Walker, R. Lester, & M. G. Bondad-Reantaso (Eds.), Diseases in Asian aquaculture V (pp. 329–337). Manila: Fish Health Section, Asian Fisheries Society.

    Google Scholar 

  • Foottit, R. G., & Adler, P. H. (2009). Insect biodiversity: Science and society (Eds.). Blackwell, UK, 632 pp.

    Google Scholar 

  • Franco-Navarro, F., & Godinez-Vidal, D. (2008). Occurrence of Pasteuria forms from a biosphere reserve in Mexico. Nematropica, 38, 187–194.

    Google Scholar 

  • Friedman, C. S., & Crosson, L. M. (2012). Putative phage hyperparasite in the rickettsial pathogen of abalone, “Candidatus Xenohaliotis californiensis”. Microbial Ecology, 64, 1064–1072.

    Article  PubMed  Google Scholar 

  • Frost, P. C., Ebert, D., & Smith, V. H. (2008). Responses of a bacterial pathogen to phosphorus limitation of its aquatic invertebrate host. Ecology, 89, 313–318.

    Article  PubMed  Google Scholar 

  • Fünfhaus, A., Poppinga, L., & Genersch, E. (2013). Identification and characterization of two novel toxins expressed by the lethal honey bee pathogen Paenibacillus larvae, the causative agent of American foulbrood. Environmental Microbiology, 15, 2951–2965.

    PubMed  Google Scholar 

  • Genersch, E. (2010). American foulbrood in honeybees and its causative agent, Paenibacillus larvae. Journal of Invertebrate Pathology, 103(Supplement 1), 10–19.

    Article  Google Scholar 

  • George, Z., & Crickmore, N. (2012). Bacillus thuringiensis applications in agriculture. In E. Sansinenea (Ed.), Bacillus thuringiensis biotechnology (pp. 19–39). New York: Springer Science+Business Media. NL.

    Chapter  Google Scholar 

  • Giblin-Davis, R. M., et al. (2011). ‘Candidatus Pasteuria aldrichii’, an obligate endoparasite of the bacterivorous nematode Bursilla. International Journal of Systematic and Evolutionary Microbiology, 61, 2073–2080.

    Article  CAS  PubMed  Google Scholar 

  • Goarant, C., et al. (2000). Toxic factors of Vibrio strains pathogenic to shrimp. Diseases of Aquatic Organisms, 40, 101–107.

    Article  CAS  PubMed  Google Scholar 

  • Green, J. (1959). Carotenoid pigment in Spirobacillus cienkowskii Metchnikoff, a pathogen of Cladocera. Nature, 183, 56–57.

    Article  CAS  PubMed  Google Scholar 

  • Grenier, A. M., Duport, G., Pagès, S., Condemine, G., & Rahbe, Y. (2006). The phytopathogen Dickeya dadantii (Erwinia chrysanthemi) is a pathogen of the pea aphid. Applied and Environmental Microbiology, 72, 1956–1965.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haider, M. Z., & Ellar, D. J. (1988). Nucleotide sequence of a Bacillus thuringiensis aizawai ICI entomocidal crystal protein gene. Nucleic Acids Research, 16, 10927.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haker, J., & Kaper, J. B. (2000). Pathogenicity islands and the evolution of microbes. Annual Reviews in Microbiology, 54, 641–679.

    Article  Google Scholar 

  • Haldane, J. B. S. (1949). Disease and evolution. La Ricerca Scientifica, 19, 68–76.

    Google Scholar 

  • Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos, 35, 282–290.

    Article  Google Scholar 

  • Han, J. E., Tang, K. F. J., Tran, L. H., & Lightner, D. V. (2015). Photorhabdus insect-related (Pir) toxin-like genes in a plasmid of Vibrio parahaemolyticus, the causative agent of acute hepatopancreatic necrosis disease (AHPND) of shrimp. Diseases of Aquatic Organisms, 113, 33–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harshbarger, J. C., Chang, S. C., & Otto, S. V. (1977). Chlamydiae (with phages), mycoplasmas, and rickettsiae in Chesapeake Bay bivalves. Science, 196, 666–668.

    Article  CAS  PubMed  Google Scholar 

  • Hasshoff, M., Bohnisch, C., Tonn, D., Hasert, B., & Schulenburg, H. (2007). The role of Caenorhabditis elegans insulin-like signaling in the behavioural avoidance of pathogenic Bacillus thuringiensis. FASEB Journal, 21, 1801–1812.

    Article  CAS  PubMed  Google Scholar 

  • Hefford, M. A., Brousseau, R., Prefontaine, G., Hanna, Z., Condie, J. A., & Lau, P. C. K. (1987). Sequence of a lepidopteran toxin gene of Bacillus thuringiensis subsp kurstaki NRD-12. Journal of Biotechnology, 6, 307–322.

    Article  CAS  Google Scholar 

  • Herrnstadt, C., Gilroy, T. E., Sobieski, D. A., Bennett, B. D., & Gaertner, F. H. (1987). Nucleotide sequence and deduced amino acid sequence of a coleopteran-active delta-endotoxin gene from Bacillus thuringiensis subsp. san diego. Gene, 57, 37–46.

    Article  CAS  PubMed  Google Scholar 

  • Hinchliffe, S. J., Hares, M. C., Dowling, A. J., & ffrench-Constant, R. H. (2010). Insecticidal toxins from the Photorhabdus and Xenorhabdus bacteria. The Open Toxinology Journal, 3, 83–100.

    Google Scholar 

  • Höfte, H., Soetaert, P., Jansens, S., & Peferoen, M. (1990). Nucleotide sequence and deduced amino acid sequence of a new Lepidoptera-specific crystal protein gene from Bacillus thuringiensis. Nucleic Acids Research, 18, 5545.

    Article  PubMed  PubMed Central  Google Scholar 

  • Howard, R. S., & Lively, C. M. (1998). The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution, 52, 604–610.

    Article  Google Scholar 

  • Huang, X. W., Niu, Q. H., Zhou, W., & Zhang, K. Q. (2005). Bacillus nematocida sp. nov., a novel bacterial strain with nematotoxic activity isolated from soil in Yunnan, China. Systematic and Applied Microbiology, 28, 323–327.

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim, M. A., Griko, N., Junker, M., & Bulla, L. A. (2010). Bacillus thuringiensis. A genomics and proteomics perspective. Bioengineered Bugs, 1, 31–50.

    Article  PubMed  PubMed Central  Google Scholar 

  • Itami, T., Takahashi, Y., Tsuchihira, E., Igusa, H., & Konda, M. (1994). Enhancement of disease resistance of kuruma prawn Penaeus japonicus and increase in phagocytic activity of prawn hemocytes after oral administration of h-1,3-glucan (Schizophyllan). In L. M. Chou et al. (Eds.), The third Asian fisheries forum (pp. 375–378). Manila: Asian Fisheries Society.

    Google Scholar 

  • Johnson, P. T. (1983). Diseases caused by viruses, rickettsiae, bacteria and fungi. In A. J. Provenzano (Ed.), The biology of crustacea: Pathobiology (pp. 2–78). New York: Academic.

    Google Scholar 

  • Johnson, K. P., Bush, S. E., & Clayton, D. H. (2005). Correlated evolution of host and parasite body size: Tests of Harrison’s rule using birds and lice. Evolution, 59, 1744–1753.

    PubMed  Google Scholar 

  • Johnstone, I. L. (1994). The cuticle of the nematode Caenorhabditis elegans: A complex collagen structure. Bioessays, 16, 171–178.

    Article  CAS  PubMed  Google Scholar 

  • Jones, G. W., et al. (2007). A new cry toxin with a unique two-component dependency from Bacillus sphaericus. FASEB Journal, 21, 4112–4120.

    Article  CAS  PubMed  Google Scholar 

  • Kellen, W. R., et al. (1965). Bacillus sphaericus Neide as a pathogen of mosquitoes. Journal of Invertebrate Pathology, 7, 442–448.

    Article  CAS  PubMed  Google Scholar 

  • Kim, H. S., et al. (2003). Cloning and characterization of two novel crystal protein genes from a Bacillus thuringiensis serovar dakota Strain. Current Microbiology, 46, 33–38.

    Article  CAS  PubMed  Google Scholar 

  • Klaphake, E. (2009). Bacterial and parasitic diseases of selected invertebrates. Veterinary Clinics: Exotic Animal Practice, 12, 639–648.

    Google Scholar 

  • Koo, B. T., et al. (1995). Cloning of a novel crystal protein gene cry1K from Bacillus thuringiensis subsp morrisoni. FEMS Microbiology Letters, 134, 159–164.

    Article  CAS  PubMed  Google Scholar 

  • Kostanjšek, R., Štrus, J., Drobne, D., & Avguštin, G. (2004). ‘Candidatus Rhabdochlamydia porcellionis’, an intracellular bacterium from the hepatopancreas of the terrestrial isopod Porcellio scaber (Crustacea: Isopoda). International Journal of Systematic and Evolutionary Microbiology, 54, 543–549.

    Article  PubMed  CAS  Google Scholar 

  • Kronstad, J. W., Schnepf, H. E., & Whiteley, H. R. (1983). Diversity of locations for Bacillus thuringiensis crystal protein genes. Journal of Bacteriology, 154, 419–428.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krska, D., Ravulapalli, R., Fieldhouse, R. J., Lugo, M. R., & Merrill, A. R. (2015). C3larvin toxin, an ADP-ribosyltransferase from Paenibacillus larvae. Journal of Biological Chemistry, 290, 1639–1653.

    Article  PubMed  CAS  Google Scholar 

  • Lazzaro, B. P., & Little, T. J. (2009). Immunity in a variable world. Philosophical Transactions of the Royal Society of London, B Biological Sciences, 364, 15–26.

    Article  PubMed  Google Scholar 

  • Le Clec’h, W., et al. (2012). High virulence of Wolbachia after host switching: When autophagy hurts. PLoS Pathogens, 8, e1002844.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lecadet, M. M., et al. (1999). Updating the H-antigen classification of Bacillus thuringiensis. Journal of Applied Microbiology, 86, 660–672.

    Article  CAS  PubMed  Google Scholar 

  • Letchumanan, V., et al. (2015). Occurrence and antibiotic resistance of Vibrio parahaemolyticus from shellfish in Selangor, Malaysia. Frontiers in Microbiology, 6, 1417.

    PubMed  PubMed Central  Google Scholar 

  • Li, J., Pandelakis, A. K., & Ellar, D. J. (1996). Structure of the mosquitocidal ä-endotoxin CytB from Bacillus thuringiensis sp. kyushuensis and implications for membrane pore formation. Journal of Molecular Biology, 257, 129–152.

    Article  CAS  PubMed  Google Scholar 

  • Li, T., Ding, M., Zhang, J., Xiang, J., & Liu, R. (1998). Studies on the pustule disease of abalone (Haliotis discus hannai Ino) on the Dalian coast. Journal of Shellfish Research, 17, 707–711.

    Google Scholar 

  • Li, H. R., et al. (2003). Transgenic plants expressiong Bacillus thuringiensis delta-endotoxins. Entomologia Sinica, 10, 155–166.

    Google Scholar 

  • Liddell, H. G., & Scott, R. (1940). A Greek-English lexicon. Oxford: Clarendon Press.

    Google Scholar 

  • Likitvivatanavong, S., Chen, J., Bravo, A., Soberón, M., & Gill, S. S. (2010). Role of cadherin, alkaline phosphatase and aminopeptidase N as receptors of Cry11Ba toxin from Bacillus thuringiensis jegathesan in Aedes aegypti. Applied and Environmental Microbiology, 77, 24–31.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Little, T., Birch, J., Vale, P., & Tseng, M. (2007). Parasite transgenerational effects on infection. Evolutionary Ecology Research, 9, 459–469.

    Google Scholar 

  • Liu, P. C., Lee, K. K., & Chen, S. N. (1996). Pathogenicity of different isolates of Vibrio harveyi in tiger shrimp, Penaeus monodon. Letters in Applied Microbiology, 22, 413–416.

    Article  Google Scholar 

  • Luijckx, P., Ben-Ami, F., Mouton, L., Du Pasquier, L., & Ebert, D. (2011). Cloning of the unculturable parasite Pasteuria ramosa and its Daphnia host reveals extreme genotype–genotype interactions. Ecology Letters, 14, 125–131.

    Article  PubMed  Google Scholar 

  • Luijckx, P., Fienberg, H., Duneau, D., & Ebert, D. (2012). Resistance to a bacterial parasite in the crustacean Daphnia magna shows Mendelian segregation with dominance. Heredity, 108, 547–551.

    Article  CAS  PubMed  Google Scholar 

  • Luijckx, P., Fienberg, H., Duneau, D., & Ebert, D. (2013). A matching-allele model explains host resistance to parasites. Current Biology, 23, 1085–1088.

    Article  CAS  PubMed  Google Scholar 

  • Margalith, Y., & Ben-Dov, E. (2000). Biological control by Bacillus thuringiensis subsp. israelensis. In J. E. Rechcigl & N. A. Rechcigl (Eds.), Insect pest management: Techniques for environmental protection (pp. 243–301). New York: Lewis Publishers.

    Google Scholar 

  • Martin, P. A. W., Gundersen-Rindal, D., Blackburn, M., & Buyer, J. (2007). Chromobacterium subtsugae sp. nov., a betaproteobacterium toxic to Colorado potato beetle and other insect pests. International Journal of Systematic and Evolutionary Microbiology, 57, 993–999. doi:10.1099/ijs.0.64611-0.

    Article  CAS  PubMed  Google Scholar 

  • Masri, L., et al. (2013). Sex differences in host defence interfere with parasite-mediated selection for outcrossing during host–parasite coevolution. Ecology Letters, 16, 461–468.

    Article  PubMed  PubMed Central  Google Scholar 

  • Masson, L., et al. (1994). Specificity domain localization of Bacillus thuringiensis insecticidal toxins is highly dependent on the bioassay system. Molecular Microbiology, 14, 851–860.

    Article  CAS  PubMed  Google Scholar 

  • Mathavan, S., Velpandi, A., & Johnson, J. C. (1987). Sub-toxic effects of Bacillus sphaericus 1593 M on feeding growth and reproduction of Laccotrephes griseus (Hemiptera: Nepidae). Experimental Biology, 46, 149–153.

    CAS  PubMed  Google Scholar 

  • McPherson, S. A., et al. (1988). Characterization of the coleopteran-specific protein gene of Bacillus thuringiensis var. tenebrionis. Bio/Technology, 6, 61–66.

    Article  CAS  Google Scholar 

  • Meiyalaghan, S., Jacobs, J. M. E., Butler, R. C., Wratten, S. D., & Conner, A. J. (2006). Transgenic potato lines expressing cry1Ba1 or cry1Ca5 Genes are resistant to potato tuber moth. Potato Research, 49, 203–216.

    Article  CAS  Google Scholar 

  • Messick, G. A., & Sindermann, C. J. (1992). Synopsis of principal diseases of the blue crab, Callinectes sapidus. NOAA Technical Memorandum NMFS-F/NEC-88. U.S. Department of Commerce, National Marine Fisheries Service, Woods Hole, Massachusetts, 25 pp.

    Google Scholar 

  • Milutinović, B., Stolpe, C., Peub, R., Armitage, S. A. O., & Kurtz, J. (2013). The red flour beetle as a model for bacterial oral infections. PLoS ONE, 8, e64638.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mitchell, S. E., & Read, A. F. (2005). Poor maternal environment enhances offspring disease resistance in an invertebrate. Proceedings of the Royal Society B, 272, 2601–2607.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitchell, S. E., Rogers, E. S., Little, T. J., & Read, A. F. (2005). Host-parasite and genotype-by-environment interactions: Temperature modifies potential for selection by a sterilizing pathogen. Evolution, 59, 70–80.

    Article  PubMed  Google Scholar 

  • Mohanta, M. K., et al. (2015). Characterization of Klebsiella granulomatis pathogenic to silkworm, Bombyx mori L. 3. Biotech, 5, 577–583.

    Google Scholar 

  • Moodley, G., Mashigo, L., Lalloo, R., & Singh, S. (2014). Application of biological agents in abalone aquaculture: A South African perspective. In M. Hernandez-Vergara (Ed.), Sustainable aquaculture techniques (pp. 207–237). InTech, Rijeka, Croatia.

    Google Scholar 

  • Moret, Y., & Moreau, J. (2012). The immune role of the arthropod exoskeleton. Invertebrate Survival Journal, 9, 200–206.

    Google Scholar 

  • Moriarty, D. J. W. (1999). Disease control in shrimp aquaculture with probiotic bacteria. In C. R. Bell, M. Brylinsky, & P. Johnson-Green (Eds.), Microbial biosystems: New frontiers. Proceedings of the 8th international symposium on microbial ecology. Atlantic Canada Society for Microbial Ecology, Halifax, Canada.

    Google Scholar 

  • Morran, L. T., Schmidt, O. G., Gelarden, I. A., Parrish, R. C., & Lively, C. M. (2011). Running with the Red Queen: Host-parasite coevolution selects for biparental sex. Science, 333, 216–218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morran, L. T., Parrish, R. C., Gelarden, I. A., & Lively, C. M. (2012). Temporal dynamics of outcrossing and host mortality rates in host-pathogen experimental coevolution. Evolution, 67, 1860–1868.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mulla, M. S., 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. Journal of the American Mosquito Control Association, 19, 39–46.

    PubMed  Google Scholar 

  • Muller, H. J. (1964). The relation of recombination to mutational advance. Mutation Research, 106, 2–9.

    Article  CAS  PubMed  Google Scholar 

  • Murray, E. E., et al. (1991). Analysis of unstable RNA transcripts of insecticidal crystal protein genes of Bacillus thuringiensis in transgenic plants and electroporated protoplasts. Plant Molecular Biology, 16, 1035–1050.

    Article  CAS  PubMed  Google Scholar 

  • Myers, P. S., & Yousten, A. A. (1980). Localization of a mosquito-larval toxin of Bacillus sphaericus 1593. Applied and Environmental Microbiology, 39, 1205–1211.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama, T., Nomura, N., & Matsumura, M. (2006). Study on the relationship of protease production and luminescence in Vibrio harveyi. Journal of Applied Microbiology, 101, 200–205.

    Article  CAS  PubMed  Google Scholar 

  • Narva, K. E., et al. (1991). Novel Bacillus thuringiensis microbes active against nematodes, and genes encoding novel nematodes-active toxin from Bacillus thuringiensis isolates. European Patent Office: EP 0462721.

    Google Scholar 

  • Nicolas, J. L., Basuyaux, O., Mazurié, J., & Thébault, A. (2002). Vibrio carchariae, a pathogen of the abalone Haliotis tuberculata. Diseases of Aquatic Organisms, 50, 35–43.

    Article  CAS  PubMed  Google Scholar 

  • Nielsen-Leroux, C., Charles, J. F., Thiéry, 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 membranes. European Journal of Biochemistry, 228, 206–210.

    Article  CAS  PubMed  Google Scholar 

  • Nishiwaki, H., Nakashima, K., Ishida, C., Kawamura, T., & Matsuda, K. (2007). Cloning, functional characterization, and mode of action of a novel insecticidal pore- forming toxin, Sphaericolysin, produced by Bacillus sphaericus. Applied and Environmental Microbiology, 73, 3404–3411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noguera, P. A., & Ibarra, J. E. (2010). Detection of new cry genes of Bacillus thuringiensis by use of a novel PCR primer system. Applied and Environmental Microbiology, 76, 6150–6155.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nollmann, F. I., et al. (2015). A Photorhabdus natural product inhibits insect juvenile hormone epoxide hydrolase. ChemBioChem, 16, 766–771.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norabadi, M. T., Sahebani, N., & Etebarian, H. R. (2014). Biological control of root-knot nematode (Meloidogyne javanica) disease by Pseudomonas fluorescens (Chao). Archives of Phytopathology and Plant Protection, 47, 615–621.

    Article  CAS  Google Scholar 

  • Norris, J. R. (1964). The classification of Bacillus thuringiensis. Journal of Applied Bacteriology, 27, 439–447.

    Article  Google Scholar 

  • Oeda, K., et al. (1987). Nucleotide sequence of the insecticidal protein gene of Bacillus thuringiensis strain aizawai IPL7 and its high-level expression in Escherichia coli. Gene, 53, 113–119.

    Article  CAS  PubMed  Google Scholar 

  • Ohba, M., Mizuki, E., & Uemori, A. (2009). Parasporin, a new anticancer protein group from Bacillus thuringiensis. Anticancer Research, 29, 427–433.

    CAS  PubMed  Google Scholar 

  • Oliveira, C. M., Filho, F. C., Beltran, J. E., Silva-Filha, M. H., & Regis, L. (2003). Biological fitness of a Culex quinquefasciatus population and its resistance to Bacillus sphaericus. Journal of the American Mosquito Control Association, 19, 125–129.

    PubMed  Google Scholar 

  • Oliveira, C. M., Silva-Filha, M. H., 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. Journal of Medical Entomology, 41, 58–64.

    Article  CAS  PubMed  Google Scholar 

  • Opota, O., et al. (2011). Monalysin, a novel ß-pore-forming toxin from the Drosophila pathogen Pseudomonas entomophila, contributes to host intestinal damage and lethality. Plos Pathogens, 7, e1002259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orlova, M. V., Smirnova, T. A., Ganushkina, L. A., Yacubovich, V. Y., & Azizbekyan, R. R. (1998). Insecticidal activity of Bacillus laterosporus. Applied and Environmental Microbiology, 64, 2723–2725.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Page, A. P., & Johnstone, I. L. (2007). The cuticle. In WormBook (Ed.), The C. elegans research community, WormBook, doi:10.1895/wormbook.1.138.1, http://www.wormbook.org.

  • Palma, L., Muñoz, D., Berry, C., Murillo, J., & Caballero, P. (2014). Bacillus thuringiensis toxins: An overview of their biocidal activity. Toxins, 6, 3296–3325.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parker, M. W., & Feil, S. C. (2005). Pore-forming protein toxins: From structure to function. Progress in Biophys & Molecular Biology, 88, 91–142.

    Article  CAS  Google Scholar 

  • Perlak, F. J. R., Fuchs, R. L., Dean, D. A., McPherson, S. L., & Fischhoff, D. A. (1991). Modification of the coding sequence enhances plant expression of insect control protein genes. Proceedings of the National Academy of Sciences, USA, 88, 3324–3328.

    Article  CAS  Google Scholar 

  • Peters, W. (1972). Occurrence of chitin in mollusca. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 41, 541–544.

    Article  CAS  Google Scholar 

  • Pettersson, B., Rippere, K. E., Yousten, A. A., & Priest, F. G. (1999). Transfer of Bacillus lentimorbus and Bacillus popilliae to the genus Paenibacillus with emended descriptions of Paenibacillus lentimorbus comb. nov. and Paenibacillus popilliae comb. nov. International Journal of Systematic Bacteriology, 49, 531–540.

    Article  PubMed  Google Scholar 

  • Pinto, L. M. N., et al. (2012). Bacillus thuringiensis monogenic strains: Screening and interactions with insecticides used against rice pests. Brazilian Journal of Microbiology, 43, 618–626.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Priest, F. G., & Dewar, S. J. (2000). Bacteria and insects. In F. Priest & M. Goodfellow (Eds.), Applied microbial systematics (pp. 165–202). Dordrecht: Springer-Science + Business Media.

    Chapter  Google Scholar 

  • Rae, R., Iatsenko, I., Witte, H., & Sommer, R. J. (2010). A subset of naturally isolated Bacillus strains show extreme virulence to the free-living nematodes Caenorhabditis elegans and Pristionchus pacificus. Environmental Microbiology, 12, 3007–3021.

    Article  CAS  PubMed  Google Scholar 

  • Rieg, S., et al. (2010). Paenibacillus larvae bacteremia in injection drug users. Emerging Infectious Diseases, 16, 487–489.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodcharoen, J., & Mulla, M. S. (1997). Biological fitness of Culex quinquefasciatus (Diptera:Culicidae) susceptible and resistant to Bacillus sphaericus. Journal of Medical Entomology, 34, 5–10.

    Article  CAS  PubMed  Google Scholar 

  • Roh, J. Y., Choi, J. Y., Li, M. S., Jin, B. R., & Je, Y. H. (2007). Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. Journal of Microbiology and Biotechnology, 17, 547–559.

    CAS  PubMed  Google Scholar 

  • Romalde, J. L., & Barja, J. L. (2010). Bacteria in molluscs: Good and bad guys. In Formatex (Ed.), Current research, technology and education topics in applied microbiology and microbial biotechnology (Vol. 1, pp. 136–147). Badajoz: Formatex Research Center.

    Google Scholar 

  • Rosso, M. L., & Delécluse, A. (1997). Contribution of the 65-kilodalton protein encoded by the cloned gene cry19A to the mosquitocidal activity of Bacillus thuringiensis subsp. jegathesan. Applied Environmental Microbiology, 63, 4449–4455.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiu, L. (2013). Brevibacillus laterosporus, a pathogen of invertebrates and a broad-spectrum antimicrobial species. Insects, 4, 476–492.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruiu, L., Satta, A., & Floris, I. (2012). Observations on house fly larvae midgut ultrastructure after Brevibacillus laterosporus ingestion. Journal of Invertebrate Pathology, 111, 211–216.

    Article  PubMed  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, 551–555.

    Article  CAS  PubMed  Google Scholar 

  • Sanchis, V., & Bourguet, D. (2008). Bacillus thuringiensis: Applications in agriculture and insect resistance management. A review. Agronomy for Sustainable Development, 28, 11–20.

    Article  Google Scholar 

  • Sanchis, V., et al. (1989). Nucleotide sequence and analysis of the N-terminal coding region of the Spodoptera-active d-endotoxin gene of Bacillus thuringiensis aizawai 7.29. Molecular Microbiology, 3, 229–238.

    Article  CAS  PubMed  Google Scholar 

  • Sato, R., et al. (1994). Cloning, heterologous expression, and localization of a novel crystal protein gene from Bacillus thuringiensis serovar japonensis strain Buibui toxic to scarabaeid insects. Current Microbiology, 28, 15–19.

    Article  CAS  PubMed  Google Scholar 

  • Schild, H. A., Fuchs, S. W., Bode, H. B., & Grünewald, B. (2014). Low-molecular-weight metabolites secreted by Paenibacillus larvae as potential virulence factors of American foulbrood. Applied and Environmental Microbiology, 80, 2484–2492.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schirmer, J., Wieden, H.-J., Rodnina, M. V., & Aktories, K. (2002). Inactivation of the elongation factor Tu by mosquitocidal toxin-catalysed mono-ADP-ribosylation. Applied and Environmental Microbiology, 68, 4894–4899.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid-Hempel, P. (1998). Parasites in social insects. Princeton, New Jersey: Princeton University Press, 413 pp.

    Google Scholar 

  • Schnepf, H. E., Wong, H. C., & Whiteley, H. R. (1985). The amino acid sequence of a crystal protein from Bacillus thuringiensis deduced from the DNA base sequence. Journal of Biological Chemistry, 260, 6264–6272.

    CAS  PubMed  Google Scholar 

  • Schulenburg, H., & Ewbank, J. J. (2007). The genetics of pathogen avoidance in Caenorhabditis elegans. Molecular Microbiology, 66, 563–570.

    Article  CAS  PubMed  Google Scholar 

  • Schulte, R. D., Makus, C., Hasert, B., Michiels, N. K., & Schulenburg, H. (2010). Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proceedings of the National Academy of Sciences, USA, 107, 7359–7364.

    Article  CAS  Google Scholar 

  • Schulte, R. D., Makus, C., Hasert, B., Michiels, N. K., & Schulenburg, H. (2011). Host-parasite local adaptation after experimental coevolution of Caenorhabditis elegans and its microparasite Bacillus thuringiensis. Proceedings of the Royal Society of London B, 278, 2832–2839.

    Article  Google Scholar 

  • Schulte, R. D., Hasert, B., Makus, C., Michiels, N. K., & Schulenburg, H. (2012). Increased responsiveness in feeding behaviour of Caenorhabditis elegans after experimental coevolution with its microparasite Bacillus thuringiensis. Biology Letters, 8, 234–236.

    Article  PubMed  Google Scholar 

  • Shapiro-Ilan, D. I., Fuxa, J. R., Lacey, L. A., Onstad, D. W., & Kaya, H. K. (2005). Definitions of pathogenicity and virulence in invertebrate pathology. Journal of Invertebrate Pathology, 88, 1–7.

    Article  PubMed  Google Scholar 

  • Sharma, V., Singh, P. K., Midha, S., Ranjan, M., Korpole, S., & Patil, P. B. (2012). Genome sequence of Brevibacillus laterosporus strain GI-9. Journal of Bacteriology, 194, 1279.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheets, J. J., et al. (2011). Insecticidal toxin complex proteins from Xenorhabdus nematophilus. Structure and pore formation. The Journal of Biological Chemistry, 286, 22742–22749.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shevelev, A. B., et al. (1993). Primary structure of cryX, the novel delta-endotoxin-related gene from Bacillus thuringiensis spp. galleriae. FEBS Letters, 336, 79–82.

    Article  CAS  PubMed  Google Scholar 

  • Shida, O., Takagi, H., Kadowaki, K., & Komagata, K. (1996). Proposal for two new genera. Brevibacillus gen. nov. and Aneurinibacillus gen. nov. International Journal of Systematic Bacteriology, 46, 939–946.

    Article  CAS  PubMed  Google Scholar 

  • Shimizu, M., et al. (1988). Cloning and expression in Escherichia coli of the 135-kDa insecticidal protein gene from Bacillus thuringiensis subsp. aizawai IPL7. Agricultural and Biological Chemistry, 52, 1565–1573.

    CAS  Google Scholar 

  • Shin, B. S., et al. (1995). Distribution of cryV-type insecticidal protein genes in Bacillus thuringiensis and coning of cryV-type genes from Bacillus thuringiensis subsp. kurstaki and Bacillus thuringiensis subsp. entomocidus. Applied and Environmental Microbiology, 61, 2402–2407.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sick, A., Gaertner, F., & Wong, A. (1990). Nucleotide sequence of a coleopteran-active toxin gene from a new isolate of Bacillus thuringiensis subsp. tolworthi. Nucleic Acids Research, 18, 1305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siddiqui, Z. A., & Mahmood, I. (1999). Role of bacteria in the management of plant parasitic nematodes. A review. Bioresource Technology, 69, 167–179.

    Article  CAS  Google Scholar 

  • Silva, C. P., et al. (2002). Bacterial infection of a model insect: Photorhabdus luminescens and Manduca sexta. Cellular Microbiology, 4, 329–339.

    Article  CAS  PubMed  Google Scholar 

  • Silva-Werneck, J. O., & Ellar, D. J. (2008). Characterization of a novel Cry9Bb δ-endotoxin from Bacillus thuringiensis. Journal of Invertebrate Pathology, 98, 320–328.

    Article  CAS  PubMed  Google Scholar 

  • Silva-Werneck, J. O., De-Souza, M. T., de S. Dias, J. M. C., & Ribeiro, B. M. (1999). Characterization of Bacillus thuringiensis subsp. kurstaki strain S93 effective against the fall armyworm (Spodoptera frugiperda). Canadian Journal of Microbiology, 45, 464–471.

    Article  CAS  Google Scholar 

  • Singer, S. (1987). Current status of the microbial larvicide Bacillus sphericus. In K. Karamorosch (Ed.), Biotechnology in invertebrate pathology and cell culture (pp. 133–156). San Diego: Academic Press.

    Google Scholar 

  • Singer, S. (1996). The utility of strains of morphological group II Bacillus. In S. L. Neidleman & A. I. Laskin (Eds.), Advances in applied microbiology (Vol. 42, pp. 219–261). San Diego: Academic Press.

    Google Scholar 

  • Smulevitch, S. V., et al. (1991). Nucleotide sequence of a novel delta-endotoxin gene cryIG of Bacillus thuringiensis ssp. galleriae. FEBS Letters, 293, 25–28.

    Article  CAS  PubMed  Google Scholar 

  • Soberón, M., Gill, S. S., & Bravo, A. (2009). Signaling versus punching hole: How do Bacillus thuringiensis toxins kill insect midgut cells? Cell and Molecular Life Sciences, 66, 1337–1349.

    Article  CAS  Google Scholar 

  • Steinhaus, E. A., & Martignoni, M. E. (1970). An abridged glossary of terms used in invertebrate pathology, 2nd edn. USDA Forest Service, PNW Forest and Range Experiment Station.

    Google Scholar 

  • Stirling, G. (2014). Biological control of plant-parasitic nematodes (Soil ecosystem management in sustainable agriculture 2nd ed.). Oxfordshire: CABI.

    Google Scholar 

  • Sturhan, D., Shutova, T. S., Akimov, V. N., & Subbotin, S. A. (2005). Occurrence, hosts, morphology, and molecular characterisation of Pasteuria bacteria parasitic in nematodes of the family Plectidae. Journal of Invertebrate Pathology, 88, 17–26.

    Article  CAS  PubMed  Google Scholar 

  • Sun, J., & Wu, X. (2004). Histology, ultrastructure, and morphogenesis of a rickettsial-like organism causing disease in the oyster Crassostrea ariakensis Gould. Journal of Invertebrate Pathology, 86, 77–86.

    Article  PubMed  Google Scholar 

  • Tabashnik, B., Brévault, T., & Carrière, Y. (2013). Insect resistance to Bt crops: Lessons from the first billion acres. Nature Biotechnology, 31, 510–521. doi:10.1038/nbt.2597.

    Article  CAS  PubMed  Google Scholar 

  • Tan, M. W. (2002). Identificatin of host and pathogen factors involved in virulence using Caenorhabditis elegans. In Bacterial pathogenesis, part C: Identification, regulation and function of virulence factors (Methods in enzymology, 358, pp. 13–29). San Diego: Academic Press.

    Chapter  Google Scholar 

  • Tanada, Y., & Fuxa, J. R. (1987). The host population. In J. R. Fuxa & Y. Tanada (Eds.), Epizootiology of insect diseases (pp. 113–157). New York: Wiley.

    Google Scholar 

  • Tao, H. P., et al. (2011). Isolation and identification of a pathogen of silkworm Bombyx mori. Current Microbiology, 62, 876–883.

    Article  CAS  PubMed  Google Scholar 

  • Thomas, M. B., & Blanford, S. (2003). Thermal biology in insect-parasite interactions. Trends in Ecology and Evolution, 18, 344–350.

    Article  Google Scholar 

  • Thomas, S. R., & Elkinton, J. S. (2004). Pathogenicity and virulence. Journal of Invertebrate Pathology, 85, 146–151.

    Article  PubMed  Google Scholar 

  • Thorne, L., et al. (1986). Structural similarity between the Lepidoptera- and Diptera-specific insecticidal endotoxin genes of Bacillus thuringiensis subsp. “kurstaki” and “israelensis”. Journal of Bacteriology, 166, 801–811.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Treiber, N., Reinert, D. J., Carpusca, I., Aktories, K., & Schulz, G. E. (2008). Structure and mode of action of a mosquitocidal holotoxin. Journal of Molecular Biology, 381, 150–159.

    Article  CAS  PubMed  Google Scholar 

  • Tyrell, D. J., Bulla, L. A., Andrews, R. E., Kramer, K. J., Davjdson, L. I., & Nordin, P. (1981). Comparative biochemistry of entomocidal parasporal crystal of selected Bacillus thuringiensis strains. Journal of Bacteriology, 145, 105–1062.

    Google Scholar 

  • Van Frankenhuyzen, K. (2009). Insecticidal activity of Bacillus thuringiensis crystal proteins. Journal of Invertebrate Pathology, 101, 1–16.

    Article  PubMed  CAS  Google Scholar 

  • Van Klinken, R. D. (2000). Host specificity testing: Why do we do it and how we can do it better. In R. Van Driesche, T. A. Heard, A. S. McClay, & R. Reardon (Eds.), Proceedings of session: Host specificity testing of exotic arthropod biological control agents – the biological basis for improvement in safety (pp. 54–68). USDA Forest Service, Publication #FHTET-99-1, Morgantown: West Virginia, USA.

    Google Scholar 

  • Van Valen, L. (1973). A new evolutionary law. Evolutionary Theory, 1, 1–30.

    Google Scholar 

  • Villalba, A., Carballal, M. J., López, C., Cabada, A., Corral, L., & Azevedo, C. (1999). Branchial rickettsia-like infection associated with clam Venerupis rhomboides mortality. Diseases of Aquatic Organisms, 36, 53–60.

    Article  Google Scholar 

  • Visser, B., Munsterman, E., Stoker, A., & Dirkse, W. G. (1990). A novel Bacillus thuringiensis gene encoding a Spodoptera exigua-specific crystal protein. Journal of Bacteriology, 172, 6783–6788.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vodovar, N., et al. (2006). Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila. Nature Biotechnology, 24, 673–679.

    Article  CAS  PubMed  Google Scholar 

  • Wang, W. (2011). Bacterial diseases of crabs: A review. Journal of Invertebrate Pathology, 106, 18–26. doi:10.1016/j.jip.2010.09.018.

    Article  CAS  PubMed  Google Scholar 

  • Waterfield, N., Hares, M., Hinchliffe, S., Wren, B., & ffrench-Constant, R. (2007). The insect toxin complex of Yersinia. In R. D. Perry & J. D. Fetherston (Eds.), The Genus Yersinia. From genomics to function (Advances in experimental medicine and biology, 603, pp. 247–257). New York: Springer.

    Chapter  Google Scholar 

  • Wen, C. M., Kou, G. H., & Chen, S. N. (1994). Rickettsiaceae-like microorganisms in the gill and digestive gland of the hard clam, Meretrix lusoria Röding. Journal of Invertebrate Pathology, 64, 138–142.

    Article  Google Scholar 

  • Wen, C., Xue, M., Liang, H., & Zhou, S. (2014). Evaluating the potential of marine Bacteriovorax sp. DA5 as a biocontrol agent against vibriosis in Litopenaeus vannamei larvae. Veterinary Microbiology, 173, 84–91.

    Article  PubMed  Google Scholar 

  • Wilson, G. R., & Benoit, T. G. (1993). Alkaline pH activates Bacillus thuringiensis spores. Journal of Invertebrate Pathology, 62, 87–89.

    Article  Google Scholar 

  • Wilson, K., Cotter, S. C., Reeson, A. F., & Pell, J. K. (2001). Melanism and disease resistance in insects. Ecology Letters, 4, 637–649.

    Article  Google Scholar 

  • Wojciechowska, J. A., Lewitin, E., Revina, L. P., Zalunin, I. A., & Chestukhina, G. G. (1999). Two novel delta-endotoxin gene families cry26 and cry28 from Bacillus thuringiensis ssp. finitimus. FEBS Letters, 453(1–2), 46–48.

    Article  CAS  PubMed  Google Scholar 

  • Wolinska, J., & King, K. C. (2009). Environment can alter selection in host–parasite interactions. Trends in Parasitology, 25, 236–244.

    Article  PubMed  Google Scholar 

  • Wolinska, J., & Spaak, P. (2009). The cost of being common: Evidence from natural Daphnia populations. Evolution, 63, 1893–1901.

    Article  PubMed  Google Scholar 

  • Xu, K., Yuan, Z., Rayner, S., & Hu, X. (2015). Genome comparison provides molecular insights into the phylogeny of the reassigned new genus Lysinibacillus. BMC Genomics, 16, 140. doi:10.1186/s12864-015-1359-x.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ye, W., et al. (2012). Mining new crystal protein genes from Bacillus thuringiensis on the basis of mixed plasmid-enriched genome sequencing and a computational pipeline. Applied and Environmental Microbiology, 78, 4795–4801.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young, J. A., Yourth, C. P., & Agrawal, A. F. (2009). The effect of pathogens on selection gainst deleterious mutations in Drosophila melanogaster. Journal of Evolutionary Biology, 22, 2125–2129.

    Article  PubMed  Google Scholar 

  • Yu, X., et al. (2012). Co-expression and synergism analysis of Vip3Aa29 and Cyt2Aa3 insecticidal proteins from Bacillus thuringiensis. Current Microbiology, 64, 326–331.

    Article  CAS  PubMed  Google Scholar 

  • Zeigler, D. (1999). Bacillus thuringiensis and Bacillus cereus. Bacillus Genetic Stock Center Catalog of Strains. 7th edn, Part 2. The Ohio State University, USA, 56 pp.

    Google Scholar 

  • Zeigler, D. (2013). The Family Paenibacillaceae. Bacillus Genetic Stock Center Catalog of Strains. Part 5. The Ohio State University, USA, 32 pp.

    Google Scholar 

  • Zhang, J., Hodgman, T. C., Krieger, L., Schnetter, W., & Schairer, H. U. (1997). Cloning and analysis of the first cry gene from Bacillus popilliae. Journal of Bacteriology, 179, 4336–4341.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, X. B., Candas, M., Griko, N. B., Taussig, R., & Bulla, L. A. (2006). A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proceedings of the National Academy of Sciences, USA, 103, 9897–9902.

    Article  CAS  Google Scholar 

  • Zhang, J., Shen, Z., Tang, X., Xu, L., & Zhu, F. (2013). Isolation and identification of a pathogen, Providencia rettgeri, in Bombyx mori. Journal of Bacteriology Research, 5, 22–28.

    Article  CAS  Google Scholar 

  • Zhong, C., et al. (2000). Characterization of a Bacillus thuringiensis δ-endotoxin which is toxic to insects in three orders. Journal of Invertebrate Pathology, 76, 131–139.

    Article  CAS  PubMed  Google Scholar 

  • Zhong, W. F., Wu, J., Cai, P. Z., & Yan, W. Z. (2004). Cloning and sequencing of Cry1Aa13 gene from Bacillus thuringiensis subsp sotto. Journal of the Sichuan University (Natural Science Edition), 41, 1050–1053.

    CAS  Google Scholar 

  • Zhu, Y., et al. (2011). Complete genome sequence of Bacillus thuringiensis serovar finitimus strain YBT-020. Journal of Bacteriology, 193, 2379–2380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zielinski, F. U., et al. (2009). Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels. Environmental Microbiology, 11, 1150–1167.

    Article  CAS  PubMed  Google Scholar 

  • Zubasheva, M. V., Ganushkina, L. A., Smirnova, T. A., & Azizbekyan, R. R. (2010). Larvicidal activity of crystal-forming strains of Brevibacillus laterosporus. Applied Biochemistry and Microbiology, 46, 755–762.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Sustainable Plant Protection Institute, National Research Council, Bari, Italy

    Aurelio Ciancio

Authors
  1. Aurelio Ciancio
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Ciancio, A. (2016). Parasitic Endosymbiosis. In: Invertebrate Bacteriology. Springer, Dordrecht. https://doi.org/10.1007/978-94-024-0884-3_4

Download citation

Publish with us

Policies and ethics

Search

Navigation