Bacterial symbionts affect host susceptibility to fenitrothion and imidacloprid within the obligate hematophagous mattress bug, Cimex hemipterus

0
149
Bacterial symbionts influence host susceptibility to fenitrothion and imidacloprid in the obligate hematophagous bed bug, Cimex hemipterus

  • Brownlie, J. C. & Johnson, K. N. Symbiont-mediated protection in insect hosts. Trends Microbiol. 17, 348–354 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Oliver, K. M., Moran, N. A. & Hunter, M. S. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl. Acad. Sci. U.S.A. 102, 12795–12800 (2005).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X. Y. & Fukatsu, T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc. Natl. Acad. Sci. 107, 769–774 (2010).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Hosokawa, T. & Fukatsu, T. Relevance of microbial symbiosis to insect behavior. Curr. Opin. Insect Sci. 39, 91–100 (2020).

    Article 
    PubMed 

    Google Scholar 

  • McCutcheon, J. P., Boyd, B. M. & Dale, C. The life of an insect endosymbiont from the cradle to the grave. Curr. Biol. 29, 485–495 (2019).

    Article 

    Google Scholar 

  • Teoh, M. C., Furusawa, G. & Veera Singham, G. Multifaceted interactions between the pseudomonads and insects: Mechanisms and prospects. Arch. Microbiol. 203, 1891–1915 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lehane, M. J. & Lehane, M. The Biology of Blood-Sucking in Insects (Cambridge University Press, 2005).

    Book 

    Google Scholar 

  • Rio, R. V., Attardo, G. M. & Weiss, B. L. Grandeur alliances: Symbiont metabolic integration and obligate arthropod hematophagy. Trends Parasitol. 32, 739–749 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Douglas, A. E. The B vitamin nutrition of insects: The contributions of diet, microbiome and horizontally acquired genes. Curr. Opin. Insect Sci. 23, 65–69 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Husnik, F. Host-symbiont-pathogen interactions in blood-feeding parasites: Nutrition, immune cross-talk and gene exchange. Parasitology 145, 1294–1303 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Michalkova, V., Benoit, J. B., Weiss, B. L., Attardo, G. M. & Aksoy, S. Vitamin B6 generated by obligate symbionts is critical for maintaining proline homeostasis and fecundity in tsetse flies. Appl. Environ. Microbiol. 80, 5844–5853 (2014).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Puchta, O. Experimentelle untersuchungen uber die bedeutung der symbiose der kleiderlaus Pediculus vestimenti Burm. Z. Parasitenkd. 17, 1 (1955).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Perotti, M. A., Kirkness, E. F., Reed, D. L. & Braig, H. R. Endosymbionts of lice. In Insect Symbiosis (eds Bourtzis, K. & Miller, T. A.) 205–219 (CRC Press, 2009).

    Google Scholar 

  • Kirkness, E. F. et al. Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc. Natl. Acad. Sci. U. S. A. 107, 12168–12173 (2010).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nikoh, N. et al. Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc. Natl. Acad. Sci. U. S. A. 111, 10257–10262 (2014).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Duron, O. et al. Tick-bacteria mutualism depends on B vitamin synthesis pathways. Curr. Biol. 28, 1896–1902 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Usinger, R. L. Monograph of Cimicidae (Hemiptera, Heteroptera) (Thomas Say Foundation, College Park, 1966).

    Google Scholar 

  • Doggett, S. L., Miller, D. M. & Lee, C. Y. Introduction. In Advances in the Biology and Management of Modern Bed Bugs (eds Doggett, S. L. et al.) 1–7 (Wiley-Blackwell, 2018).

    Chapter 

    Google Scholar 

  • Doggett, S. L., Dwyer, D. E., Peñas, P. F. & Russell, R. C. Bed bugs: Clinical relevance and control options. Clin. Microbiol. Rev. 25, 164–192 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hwang, S. J. E., Doggett, S. L. & Fernandez-Penas, P. Dermatology and immunology. In Advances in the Biology and Management of Modern Bed Bugs (eds Doggett, S. L. et al.) 109–116 (Wiley-Blackwell, 2018).

    Google Scholar 

  • Lee, C. Y., Miller, D. M. & Doggett, S. L. Chemical control. In Advances in the Biology and Management of Modern Bed Bugs (eds Doggett, S. L. et al.) 285–310 (Wiley-Blackwell, 2018).

    Chapter 

    Google Scholar 

  • Dang, K., Doggett, S. L., Singham, G. V. & Lee, C. Y. Insecticide resistance and resistance mechanisms in bed bugs, Cimex spp. (Hemiptera: Cimicidae). Parasit. Vectors 10, 318 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Romero, A. Insecticide resistance. In Advances in the Biology and Management of Modern Bed Bugs (eds Doggett, S. L. et al.) 273–280 (Wiley-Blackwell, 2018).

    Chapter 

    Google Scholar 

  • Leong, X. Y. et al. Performance of commercial insecticide formulations against different developmental stages of insecticide-resistant tropical bed bugs (Hemiptera: Cimicidae). J. Econ. Entomol. 113, 353–366 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Punchihewa, R., de Silva, W. P. P., Weeraratne, T. C. & Karunaratne, S. P. Insecticide resistance mechanisms with novel ‘kdr’ type gene mutations in the tropical bed bug Cimex hemipterus. Parasit. Vectors 12, 310 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhao, Y., Feng, X., Li, M. & Qiu, X. The double-mutation (M918I+ L1014F) kdr allele is fixed in Cimex hemipterus populations in Guangxi, China. Bull. Entomol. Res. 110, 506–511 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Zhu, F. et al. Bed bugs evolved unique adaptive strategy to resist pyrethroid insecticides. Sci. Rep. 3, 1–8 (2013).

    Google Scholar 

  • Kilpinen, O., Kristensen, M. & Jensen, K. M. V. Resistance differences between chlorpyrifos and synthetic pyrethroids in Cimex lectularius population from Denmark. Parasitol. Res. 109, 1461–1464 (2011).

    Article 
    PubMed 

    Google Scholar 

  • Karunaratne, S., Damayanthi, B., Fareena, M., Imbuldeniya, V. & Hemingway, J. Insecticide resistance in the tropical bedbug Cimex hemipterus. Pestic. Biochem. Physiol. 88, 102–107 (2007).

    Article 
    CAS 

    Google Scholar 

  • Leong, X. Y., Singham, G. V., Shu-Chien, A. C., Doggett, S. L. & Lee, C. Y. Influences of exposure time and mortality assessment interval on bioassay results of insecticide-resistant tropical bed bugs (Hemiptera: Cimicidae). Insects 11, 640 (2020).

    Article 
    PubMed Central 

    Google Scholar 

  • Tawatsin, A. et al. Insecticide resistance in bedbugs in Thailand and laboratory evaluation of insecticides for the control of Cimex hemipterus and Cimex lectularius (Hemiptera: Cimicidae). J. Med. Entomol. 48, 1023–1030 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Romero, A. & Anderson, T. D. High levels of resistance in the common bed bug, Cimex lectularius (Hemiptera: Cimicidae), to neonicotinoid insecticides. J. Med. Entomol. 53, 727–731 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Busvine, J. R. Insecticide-resistance in bed-bugs. Bull. World Health Organ. 19, 1041 (1958).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dang, K., Doggett, S. L., Leong, X. Y., Veera Singham, G. & Lee, C. Y. Multiple mechanisms conferring broad-spectrum insecticide resistance in the tropical bed bug (Hemiptera: Cimicidae). J. Econ. Entomol. 114, 2473–2484 (2021).

    Article 
    PubMed 

    Google Scholar 

  • González-Morales, et al. Resistance to fipronil in the common bed bug (Hemiptera: Cimicidae). J. Med. Entomol. 58, 1798–1807 (2021).

    Article 
    PubMed 

    Google Scholar 

  • Lilly, D. G., Latham, S. L., Webb, C. E. & Doggett, S. L. Cuticle thickening in a pyrethroid-resistant strain of the common bed bug, Cimex lectularius L.(Hemiptera: Cimicidae). PLoS ONE 11, e0153302 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dang, K. et al. Identification of putative kdr mutations in the tropical bed bug, Cimex hemipterus (Hemiptera: Cimicidae). Pest Manag. Sci. 71, 1015–1020 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Gressel, J. Microbiome facilitated pest resistance: Potential problems and uses. Pest Mang. Sci. 74, 511–515 (2018).

    Article 
    CAS 

    Google Scholar 

  • Kikuchi, Y. et al. Symbiont-mediated insecticide resistance. Proc. Natl. Acad. Sci. 109, 8618–8622 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Blanton, A. G. & Peterson, B. F. Symbiont-mediated insecticide detoxification as an emerging problem in insect pests. Fron. Microbiol. 11, 547108 (2020).

    Article 

    Google Scholar 

  • Langille, M. G. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Soh, L. S. & Singham, G. V. Cuticle thickening associated with fenitrothion and imidacloprid resistance and influence of voltage-gated sodium channel mutations on pyrethroid resistance in the tropical bed bug Cimex hemipterus. Pest Manag. Sci. 77, 5202–5212 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Williamson, M. S., Martinez-Torres, D., Hick, C. A. & Devonshire, A. L. Identification of mutations in the housefly para-type sodium channel gene associated with knockdown resistance (kdr) to pyrethroid insecticides. Mol. Gen. Genet. 252, 51–60 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Sonoda, S. et al. Frequencies of the M918I mutation in the sodium channel of the diamondback moth in China, Thailand and Japan and its association with pyrethroid resistance. Pestic. Biochem. Physiol. 102, 142–145 (2012).

    Article 
    CAS 

    Google Scholar 

  • Boush, M. G. & Matsumura, F. Insecticidal degradation by Pseudomonas melophthora, the bacterial symbiote of the apple maggot. J. Econ. Entomol. 60, 918–920 (1967).

    Article 
    CAS 

    Google Scholar 

  • Cheng, D. F. et al. Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5, 13 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Xie, X., Sun, B. & Gurr, G. Gut microbiota mediate insecticide resistance in the diamondback moth, Plutella xylostella (L.). Front. Microbiol. 9, 25 (2018).

    Article 
    CAS 

    Google Scholar 

  • Pang, R. et al. A distinct strain of Arsenophonus symbiont decreases insecticide resistance in its insect host. PLoS Genet. 14, e1007725 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Akami, M. et al. Gut bacteria of the cowpea beetle mediate its resistance to dichlorvos and susceptibility to Lippia adoensis essential oil. Sci. Rep. 9, 6435 (2019).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pietri, J. E., Tiffany, C. & Liang, D. Disruption of the microbiota affects physiological and evolutionary aspects of insecticide resistance in the German cockroach, an important urban pest. PLoS ONE 13, e0207985 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Li, Y., Liu, X. & Guo, H. Variations in endosymbiont infection between buprofezin-resistant and susceptible strains of Laodelphax striatellus (Fallén). Curr. Microbiol. 75, 709–715 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Li, Y. et al. Background-dependent Wolbachia-mediated insecticide resistance in Laodelphax striatellus. Environ. Microbiol. 22, 2653–2663 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Ghanim, M. & Kontsedalov, S. Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Mang. Sci. 65, 939–942 (2009).

    Article 
    CAS 

    Google Scholar 

  • Shemshadian, A., Vatandoost, H., Oshaghi, M. A., Abai, M. R. & Djadid, N. D. Relationship between Wolbachia infection in Culex quinquefasciatus and its resistance to insecticide. Heliyon 7, e06749 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Berticat, C., Rousset, F., Raymond, M., Berthomieu, A. & Weill, M. High Wolbachia density in insecticide-resistant mosquitoes. Proc. Royal Soc. Lond. B Biol. Sci. 269, 1413–1416 (2002).

    Article 

    Google Scholar 

  • Campbell, E. A. et al. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104, 901–912 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wehrli, W., Knüsel, F. & Staehelin, M. Action of rifamycin on RNA-polymerase from sensitive and resistant bacteria. Biochem. Biophys. Res. Comm. 32, 284–288 (1968).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Duan, X. Z. et al. Recent infection by Wolbachia alters microbial communities in wild Laodelphax striatellus populations. Microbiome 8, 104 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Audsley, M. D. et al. Wolbachia infection alters the relative abundance of resident bacteria in adult Aedes aegypti mosquitoes, but not larvae. Mol Ecol. 27, 297–309 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Simhadri, R. K. et al. The gut commensal microbiome of Drosophila melanogaster is modified by the endosymbiont Wolbachia. mSphere 2, e00287 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Puinean, A. M. et al. Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid myzus persicae. PLoS Genet. 6, e1000999 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tang, T. et al. Antibiotics increased host insecticide susceptibility via collapsed bacterial symbionts reducing detoxification metabolism in the brown planthopper Nilaparvata lugens. J. Pest Sci. 94, 757–767 (2021).

    Article 

    Google Scholar 

  • Parte, S. G., Mohekar, A. D. & Kharat, A. S. Microbial degradation of pesticide: A review. Afr. J. Microbiol. Res. 11, 992–1012 (2017).

    Article 
    CAS 

    Google Scholar 

  • Chen, B. et al. Gut bacteria of the silkworm Bombyx mori facilitate host resistance against the toxic effects of organophosphate insecticides. Environ. Int. 143, 105886 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Dang, K., Singham, G. V., Doggett, S. L., Lilly, D. G. & Lee, C. Y. Effects of different surfaces and insecticide carriers on residual insecticide bioassays against bed bugs, Cimex spp. (Hemiptera: Cimicidae). J. Econ. Entomol. 110, 558–566 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Khalid, M. F., Lee, C. Y., Doggett, S. L. & Singham, G. V. Circadian rhythms in insecticide susceptibility, metabolic enzyme activity, and gene expression in Cimex lectularius (Hemiptera: Cimicidae). PLoS ONE 14, e0218343 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Son-un, P. et al. Effect of relaxation of deltamethrin pressure on metabolic resistance in a pyrethroid-resistant Aedes aegypti (Diptera: Culicidae) strain harboring fixed P989P and G1016G kdr alleles. J. Med. Entomol. 55, 975–981 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lacey, L. & Brooks, W. Initial handling and diagnosis of diseased insects. In Manual of Techniques in Insect Pathology (ed. Lacey, L. L.) 1–15 (Academic Press, 1997).

    Google Scholar 

  • Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • de Santis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072 (2006).

    Article 
    ADS 

    Google Scholar 

  • Hall, M. & Beiko, R. G. 16S rRNA gene analysis with QIIME2. In Microbiome Analysis 113–129 (Humana Press, 2018).

    Chapter 

    Google Scholar 

  • Oliveros, J.C. Venny. An interactive tool for comparing lists with Venn’s diagrams. https://bioinfogp.cnb.csic.es/tools/venny/index.html (2015).

  • Parks, D. H., Tyson, G. W., Hugenholtz, P. & Beiko, R. G. STAMP: Statistical analysis of taxonomic and functional profiles. Bioinformatics 30, 3123–3124 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol 57, 289–300 (1995).

    MathSciNet 
    MATH 

    Google Scholar