Abstract
Symbionts are associated with many insects and play several multifunctional roles in insect-microorganism mutualistic relationships. The trichlorphon-degrading symbiont Citrobacter freundii (CF-BD) of the oriental fruit fly Bactrocera dorsalis was recently discovered; however, its intraspecies transmission pathway among flies remains unknown. Here, we use fluorescence in situ hybridization (FISH), PCR detection, and a series of ingenious experiments to reveal that CF-BD was aggregated in rectal pads associated with the female ovipositor, and the CF-BD symbiont was vertically transmitted via egg surface contamination. Although CF-BD was not detected in ovaries, it was found in deposited eggs. In addition, CF-BD was readily acquired horizontally between larvae or adults via oral uptake, although it was not transferred via mating behavior. Surface sterilization of eggs had a negative effect on the insects, which exhibited a lower body weight and a sharp decrease in fecundity, suggesting important biological roles of CF-BD in the fitness of the host insects. Our findings may also help to explain the high pesticide resistance levels of B. dorsalis. Furthermore, identifying a clear transmission pathway of this organophosphorus-degrading symbiont will be useful for pesticide resistance management and future pest control technologies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbott WS (1987) A method of computing the effectiveness of an insecticide. J Am Mosq Control Assoc 3(2):302–303. https://doi.org/10.1093/jee/18.2.265a
Abe Y, Mishiro K, Takanashi M (1995) Symbiont of brown-winged green bug, Plautia stali SCOTT. Jpn J Appl Entomol Zool 39(2):109–115. https://doi.org/10.1303/jjaez.39.109
Ahmed MZ, Li SJ, Xue X, Yin XJ, Ren SX, Jiggins FM, Greeff JM, Qiu BL (2015) The intracellular bacterium Wolbachia uses parasitoid wasps as phoretic vectors for efficient horizontal transmission. PLoS Pathog 11(2):e1004672. https://doi.org/10.1371/journal.ppat.1004672
Andongma AA, Wan L, Dong YC, Li P, Desneux N, White JA, Niu CY (2015) Pyrosequencing reveals a shift in symbiotic bacteria populations across life stages of Bactrocera dorsalis. Sci Rep 5:9470. https://doi.org/10.1038/srep09470
Baumann P, Moran NA (1997) Non-cultivable microorganisms from symbiotic associations of insects and other hosts. Anton Leeuw Int J G 72(1):39–48. https://doi.org/10.1023/A:1000239108771
Behar A, Jurkevitch E, Yuval B (2008a) Bringing back the fruit into fruit fly-bacteria interactions. Mol Ecol 17(5):1375–1386. https://doi.org/10.1111/j.2008.03674.x
Behar A, Yuval B, Jurkevitch E (2008b) Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. J Insect Physiol 54(9):1377–1383. https://doi.org/10.1016/j.jinsphys.2008.07.011
Ben-Yosef M, Jurkevitch E, Yuval B (2008) Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. Physiol Entomol 33(2):145–154. https://doi.org/10.1111/j.1365-3032.2008.00617.x
Ben-Yosef M, Aharon Y, Jurkevitch E, Yuval B (2010) Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet-dependent fashion. P Roy Soc B Biol Sci 277(1687):1545–1552. https://doi.org/10.1098/rspb.2009.2102
Ben Ami E, Yuval B, Jurkevitch E (2010) Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. ISME J 4(1):28–37. https://doi.org/10.1038/ismej.2009.82
Benelli G, Daane KM, Canale A, Niu CY, Messing RH, Vargas RI (2014) Sexual communication and related behaviours in Tephritidae: current knowledge and potential applications for Integrated Pest Management. J Pest Sci 87(3):385–405. https://doi.org/10.1007/s10340-014-0577-3
Bourtzis K, Miller TA (2003) Insect symbiosis. CRC Press, Boca Raton
Capuzzo C, Firrao G, Mazzon L, Squartini A, Girolami V (2005) ‘Candidatus Erwinia dacicol’, a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). Int J Syst Evol Microbiol 55(Pt4):1641–1647. https://doi.org/10.1099/ijs.0.63653-0
Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portnoy V, Belausov E, Hunter MS, Zchori-Fein E (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. P Roy Soc B Biol Sci 279(1734):1791–1796. https://doi.org/10.1098/rspb.2011.2095
Cheng DF, Guo ZJ, Riegler M, Xi ZY, Liang GW, Xu YJ (2017) Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5(1):13. https://doi.org/10.1186/s40168-017-0236-z
Clarke AR, Armstrong KF, Carmichael AE, Milne JR, Raghu S, Roderick GK, Yeates DK (2005) Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annu Rev Entomol 50(1):293–319. https://doi.org/10.1146/annurev.ento.50.071803.130428
Clausen CP, Clancy DW, Chock QC (1965) Biological control of the oriental fruit fly (Dacus dorsalis Hendel). USDA Tech Bull 1322:102
Denholm I, Devine GJ, Williamson MS (2002) Evolutionary genetics—insecticide resistance on the move. Science 297(5590):2222–2223. https://doi.org/10.1126/science.1077266
Devonshire AL, Field LM, Foster SP, Moores GD, Williamson MS, Blackman RL (1998) The evolution of insecticide resistance in the peach-potato aphid, Myzus persicae. Philos T R Soc B 353(1376):1677–1684. https://doi.org/10.1098/rstb.1998.0318
Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43(1):17–37. https://doi.org/10.1146/annurev.ento.43.1.17
Dunbar HE, Wilson ACC, Ferguson NR, Moran NA (2007) Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol 5(5):1006–1015. https://doi.org/10.1371/journal.pbio. 0050096
Duron O, Wilkes TE, Hurst GDD (2010) Interspecific transmission of a male-killing bacterium on an ecological timescale. Ecol Lett 13(9):1139–1148. https://doi.org/10.1111/j.1461-0248.2010.01502.x
Fitt GP, O'Brien R (1985) Bacteria associated with four species of Dacus (Diptera: Tephritidae) and their role in the nutrition of the larvae. Oecologia 67(3):447–454. https://doi.org/10.1007/BF00384954
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299. https://doi.org/10.1371/journal.pone.0013102
Fukatsu T, Hosokawa T (2002) Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Appl Environ Microbiol 68(1):389–396. https://doi.org/10.1128/AEM.68.1.389-396.2002
Fukatsu T, Nikoh N (2000) Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta, Homoptera). Appl Environ Microbiol 66(2):643–650. https://doi.org/10.1128/AEM.66.2.643-650.2000
Haramoto FH, Bess HA (1970) Recent studies on the abundance of the oriental and Mediterranean fruit flies and the status of their parasites. P Hawaiian Entomol Soc 20(3):551–566
Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332(6026):254–256. https://doi.org/10.1126/science.1199410
Hosokawa T, Kikuchi Y, Meng XY, Fukatsu T (2005) The making of symbiont capsule in the plataspid stinkbug Megacopta punctatissima. FEMS Microbiol Ecol 54(3):471–477. https://doi.org/10.1016/j.femsec.2005.06.002
Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. P Natl Acad Sci USA 107(2):769–774. https://doi.org/10.1073/pnas.0911476107
Huigens ME, de Almeida RP, Boons PAH, Luck RF, Stouthamer R (2004) Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. P Roy Soc B Biol Sci 271(1538):509–515. https://doi.org/10.1098/rspb.2003.2640
Jiggins FM, Hurst GD (2011) Microbiology. Rapid insect evolution by symbiont transfer. Science 332(6026):185–186. https://doi.org/10.1126/science.1205386
Jin T, Zeng L, Lin YY, Lu YY, Liang GW (2011) Insecticide resistance of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), in mainland China. Pest Manag Sci 67(3):370–376. https://doi.org/10.1002/ps.2076
Kaiwa N, Hosokawa T, Kikuchi Y, Nikoh N, Meng XY, Kimura N, Ito M, Fukatsu T (2010) Primary gut symbiont and secondary, Sodalis-allied symbiont of the Scutellerid stinkbug Cantao ocellatus. Appl Environ Microbiol 76(11):3486–3494. https://doi.org/10.1128/AEM.00421-10
Kajiwara H, Nakamura M (2008) Hierarchical cluster analyses and heat map analyses of silkworm tissues using R-statistics. J Electrophoresis 52(1):29–38. https://doi.org/10.2198/jelectroph.52.29
Kaltenpoth M, Winter SA, Kleinhammer A (2009) Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs. FEMS Microbiol Ecol 69(3):373–383. https://doi.org/10.1111/j.1574-6941.2009.00722.x
Kikuchi Y, Hosokawa T, Fukatsu T (2007) Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol 73(13):4308–4316. https://doi.org/10.1128/Aem.00067-07
Kikuchi Y, Hosokawa T, Nikoh N, Meng XY, Kamagata Y, Fukatsu T (2009) Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol 7(1):1–22. https://doi.org/10.1186/1741-7007-7-2
Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. P Natl Acad Sci USA 109(22):8618–8622. https://doi.org/10.1073/pnas.1200231109
Kuzina LV, Peloquin JJ, Vacek DC, Miller TA (2001) Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae). Curr Microbiol 42(4):290–294. https://doi.org/10.1007/s002840010219
Lee WY, Lin TL (2003) Morphology and ultrastructure of the hindgut of the oriental fruit fly Bactrocera dorsalis (Diptera: Tephritidae). Formosan Entomol 23(2):113–128
Li SJ, Ahmed MZ, Lv N, Shi PQ, Wang XM, Huang JL, Qiu BL (2016) Plant-mediated horizontal transmission of Wolbachia between whiteflies. ISME J 11:1019–1028. https://doi.org/10.1038/ismej.2016.164
Li WC (2013) Insect physiology and biochemistry (Bilingual Textbook). Modern education press, Beijing
Liu HQ, Cupp EW, Micher KM, Guo AG, Liu NN (2004) Insecticide resistance and cross-resistance in Alabama and Florida strains of Culex quinquefaciatus. J Med Entomol 41(3):408–413. https://doi.org/10.1603/0022-2585-41.3.408
Liu LJ, Martinez-Sanudo I, Mazzon L, Prabhakar CS, Girolami V, Deng YL, Dai Y, Li ZH (2016) Bacterial communities associated with invasive populations of Bactrocera dorsalis (Diptera: Tephritidae) in China. B Entomol Res 106(6):718–728. https://doi.org/10.1017/S0007485316000390
Mccune B, Grace J (2002) Analysis of ecological communities. Mjm Soft Des Gleneden Beach 289(03):448. https://doi.org/10.1016/S0022-0981(03)00091-1
Moran NA, Dunbar HE (2006) Sexual acquisition of beneficial symbionts in aphids. P Natl Acad Sci USA 103(34):12803–12806. https://doi.org/10.1073/pnas.0605772103
Morrow JL, Frommer M, Shearman DCA, Riegler M (2015) The microbiome of field-caught and laboratory-adapted Australian Tephritid fruit fly species with different host plant use and specialisation. Microb Ecol 70(2):498–508. https://doi.org/10.1007/s00248-015-0571-1
Nardon P (2006) Oogenesis and transmission of symbiotic bacteria in the weevil Sitophilus oryzae L. (Coleoptera : Dryophthoridae). Ann Soc Entomol Fr 42(2):129–164
Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55(55):247–266. https://doi.org/10.1146/annurev-ento-112408-085305
Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. P Natl Acad Sci USA 100(4):1803–1807. https://doi.org/10.1073/pnas.0335320100
Prado SS, Rubinoff D, Almeida RPP (2006) Vertical transmission of a pentatomid caeca-associated symbiont. Ann Entomol Soc Am 99(3):577–585. https://doi.org/10.1603/0013-8746(2006)99
Robacker DC, Bartelt RJ (1997) Chemicals attractive to Mexican fruit fly from Klebsiella pneumoniae and Citrobacter freundii. Cultures sampled by solid-phase microextraction. J Chem Ecol 23(12):2897–2915. https://doi.org/10.1023/A:1022579414233
Romero A, Broce A, Zurek L (2006) Role of bacteria in the oviposition behaviour and larval development of stable flies. Med Vet Entomol 20(1):115–121. https://doi.org/10.1111/j.1365-2915.2006.00602.x
Sauer C, Dudaczek D, Holldobler B, Gross R (2002) Tissue localization of the endosymbiotic bacterium “Candidatus Blochmannia floridanus” in adults and larvae of the carpenter ant Camponotus floridanus. Appl Environ Microbiol 68(9):4187–4193. https://doi.org/10.1128/Aem.68.9.4187-4193.2002
Schloss P, Westcott S, Ryabin T, Hall J, Hartmann M, Hollister E, Lesniewski R, Oakley B, Parks D, Robinson C, Sahl J, Stres B, Thallinger G, Van Horn D, Weber D (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. https://doi.org/10.1128/AEM.01541-09
Schröder D, Deppisch H, Obermayer M, Krohne G, Stackebrandt E, Hôlldobler B, Goebel W, Gross R (1996) Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Mol Microbiol 21(3):479–489. https://doi.org/10.1111/j.1365-2958.1996.tb02557.x
Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E (2010) Commensal bacteria play a role in mating preference of Drosophila melanogaster. P Natl Acad Sci USA 107(46):20051–20056. https://doi.org/10.1073/pnas.1009906107
Shi ZH, Wang LL, Zhang HY (2012) Low diversity bacterial community and the trapping activity of metabolites from cultivable bacteria species in the female reproductive system of the oriental fruit fly, Bactrocera dorsalis Hendel (Diptera: Tephritidae). Int J Mol Sci 13(5):6266–6278. https://doi.org/10.3390/ijms13056266
Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303(5666):1989. https://doi.org/10.1126/science.1094611
Wang H, Jin L, Zhang H (2011) Comparison of the diversity of the bacterial communities in the intestinal tract of adult Bactrocera dorsalis from three different populations. J Appl Microbiol 110(6):1390–1401. https://doi.org/10.1111/j.1365-2672.2011.05001.x
Wang HX, Jin L, Peng T, Zhang HY, Chen QL, Hua YJ (2014) Identification of cultivable bacteria in the intestinal tract of Bactrocera dorsalis from three different populations and determination of their attractive potential. Pest Manag Sci 70(1):80–87. https://doi.org/10.1002/ps.3528
Zhang YP, Zeng L, Lu YY, Liang GW (2007) Monitoring of insecticide resistance of Bactrocera dorsalis adults in South China. J South China Agric Univ 28(3):20–23
Funding
This study was supported by the National Key Research and Development Project (2016YC1201200). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical statement
This article does not involve any studies with human participants performed by any of the authors.
Electronic supplementary material
ESM 1
(PDF 456 kb)
Rights and permissions
About this article
Cite this article
Guo, Z., Lu, Y., Yang, F. et al. Transmission modes of a pesticide-degrading symbiont of the oriental fruit fly Bactrocera dorsalis (Hendel). Appl Microbiol Biotechnol 101, 8543–8556 (2017). https://doi.org/10.1007/s00253-017-8551-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-017-8551-7