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The influence of antibiotics on gut bacteria diversity associated with laboratory-reared Bactrocera dorsalis

Published online by Cambridge University Press:  05 November 2018

Z. Bai ,
L. Liu ,
M.S. Noman ,
L. Zeng ,
M. Luo  and
Z. Li
Z. Bai
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
L. Liu
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
M.S. Noman
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
L. Zeng
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
M. Luo
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
Z. Li*
Affiliation:
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China
*
*Author for correspondence Phone: 86-10-62733000 Fax: 86-10-62733404 E-mail: lizh@cau.edu.cn
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Abstract

The oriental fruit fly Bactrocera dorsalis (Hendel) is a destructive insect pest of a wide range of fruit crops. Commensal bacteria play a very important part in the development, reproduction, and fitness of their host fruit fly. Uncovering the function of gut bacteria has become a worldwide quest. Using antibiotics to remove gut bacteria is a common method to investigate gut bacteria function. In the present study, three types of antibiotics (tetracycline, ampicillin, and streptomycin), each with four different concentrations, were used to test their effect on the gut bacteria diversity of laboratory-reared B. dorsalis. Combined antibiotics can change bacteria diversity, including cultivable and uncultivable bacteria, for both male and female adult flies. Secondary bacteria became the dominant population in female and male adult flies with the decrease in normally predominant bacteria. However, in larvae, only the predominant bacteria decreased, the bacteria diversity did not change a lot, likely because of the short acting time of the antibiotics. The bacteria diversity did not differ among fruit fly treatments with antibiotics of different concentrations. This study showed the dynamic changes of gut bacterial diversity in antibiotics-treated flies, and provides a foundation for research on the function of gut bacteria of the oriental fruit fly.

Keywords

Bactrocera dorsalisantibioticbacteria diversitygutlaboratory
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 4 , August 2019 , pp. 500 - 509
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Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

†

These authors contributed equally to this work.

References

Andongma, A.A., Wan, L., Dong, Y.C., Li, P., Desneux, N., White, J.A. & Niu, C.Y. (2015) Pyrosequencing reveals a shift in symbiotic bacteria populations across life stages of Bactrocera dorsalis. Scientific Reports 5, 9470.Google Scholar
Augustinos, A.A., Kyritsis, G.A., Papadopoulos, N.T., Abd-Alla, A.M.M., Cáceres, C. & Bourtzis, K. (2015) Exploitation of the medfly gut microbiota for the enhancement of sterile insect technique: use of Enterobacter sp.in larval diet-based probiotic applications. PLoS ONE 10(9), e0136459.Google Scholar
Behar, A., Yuval, B. & Jurkevitch, E. (2005) Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Molecular Ecology 14, 2637–2643.Google Scholar
Behar, A., Yuval, B. & Jurkevitch, E. (2008 a) Gut bacterial communities in the Mediterranean fruit fly (Ceratitis capitata) and their impact on host longevity. Journal of Insect Physiology 54, 1377–1383.Google Scholar
Behar, A., Jurkevitch, E. & Yuval, B. (2008 b) Bringing back the fruit into fruit fly–bacteria interactions. Molecular Ecology 17, 1375–1386.Google Scholar
Ben, A.E., Yuval, B. & Jurkevitch, E. (2010) Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidiae) improves sterile male sexual performance. Journal of International Society and Microbial Ecology 4, 28–37.Google Scholar
Ben-Yosef, M., Jurkevitch, E. & Yuval, B. (2008). Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata. Physiological Entomology 33(2), 145–154.Google Scholar
Bertacco, A., Dehner, C.A., Caturegli, G., D'Amico, F., Morotti, R., Rodriguez, M.I., Mulligan, D.C., Kriegel, M.A. & Geibel, J.P. (2017) Modulation of intestinal microbiome prevents intestinal ischemic injury. Frontiers in Physiology 8, 1064.Google Scholar
Capuzzo, C., Firrao, G., Mazzon, L., Squartini, A. & Girolami, V. (2005) ‘Candidatus Erwinia dacicola’, a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). International Journal of Systematic Evolutionary Microbiology 55, 1641–1647.Google Scholar
Chao, A. (1984) Non-parametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11, 265–270.Google Scholar
Chaplinska, M., Gerritsma, S., Dini-Andreote, F., Salles, J.F. & Wertheim, B. (2016) Bacterial communities differ among Drosophila melanogaster populations and affect host resistance against parasitoids. PLoS ONE 11(12), e0167726.Google Scholar
Chen, C., Khaleel, S. S., Huang, H. & Wu, C. H. (2014) Software for pre-processing Illumina next-generation sequencing short read sequences. Source Code for Biology and Medicine 9(1), 8.Google Scholar
Cheng, D.F., Guo, Z.J., Riegler, M., Xi, Z.Y., Liang, G.W. & Xu, Y.J. (2017) Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5, 13.Google Scholar
Chinnarajan, A.M., Jayaraj, S. & Narayanan, K. (1972) Destruction of endo symbionts with oxytetracycline and sulfanilamide in the gourd fruit fly Dacus-cucurbitae trypetidae diptera. Hindustan Antibiotics Bulletin 15(1), 16–22.Google Scholar
Cicero, L., Sivinski, J. & Aluja, M. (2012) Effect of host diet and adult parasitoid diet on egg load dynamics and egg size of braconid parasitoids attacking Anastrepha ludens. Physiological Entomology 37, 177–184.Google Scholar
Clarke, A.R., Armstrong, K.F., Carmichael, A.E., Milne, J.R., Raghu, S., Roderick, G.K. & Yeates, D.K. (2005) Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annual Review of Entomology 50, 293–319.Google Scholar
Damodaram, K.J., Ayyasamy, A. & Kempraj, V. (2016) Commensal bacteria aid mate-selection in the fruit fly, Bactrocera dorsalis. Microbial ecology 72, 725–729.Google Scholar
Eben, A., Benrey, B., Sivinski, J. & Aluja, M. (2000) Host species and host plant effects on preference and performance of Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environmental Entomology 29, 87–94.Google Scholar
Edgar, R.C. (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England) 26, 2460–2461.Google Scholar
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C. & Knight, R. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics (Oxford, England) 27, 2194–2200.Google Scholar
Hadapad, A.B., Prabhakar, C.S., Chandekar, S.C., Tripathi, J. & Hire, R.S. (2016) Diversity of bacterial communities in the midgut of Bactrocera cucurbitae (Diptera: Tephritidae) populations and their potential use as attractants. Pest Management Science 72, 1222–1230.Google Scholar
Huerta-Cepas, J., Dopazo, J. & Gabaldón, T. (2010) ETE: a python environment for tree exploration. BMC Bioinformatics 11, 24.Google Scholar
Hu, J.T., Chen, B. & Li, Z.H. (2014) Thermal plasticity is related to the hardening response of heat shock protein expression in two Bactrocera fruit flies. Journal of Insect Physiology 67, 105–113.Google Scholar
Jang, E.B. & Nishijima, K.A. (1990) Identification and Atrractancy of bacteria associated with Dacus-Dorsalis (Diptera: Tephritidae). Environmental Entomology 19, 1726–1731.Google Scholar
Khaeso, K., Andongma, A.A., Akami, M., Souliyanonh, B., Zhu, J., Krutmuang, P. & Niu, C.Y. (2018) Assessing the effects of gut bacteria manipulation on the development of the oriental fruit fly, Bactrocera dorsalis (Diptera; Tephritidae). Symbiosis 74, 97–105.Google Scholar
Kounatidis, I., Crotti, E., Sapountzis, P., Sacchi, L., Rizzi, A., Chouaia, B., Bandi, C., Alma, A., Daffonchio, D., Mavragani-Tsipidou, P. & Bourtzis, K. (2009) Acetobacter tropicalis is a major symbiont of the olive fruit fly (Bactrocera oleae). Applied and Environmental Microbiology 75, 3281–3288.Google Scholar
Krainacker, J.R.C. & Vargas, R.I. (1989) Size-specific survival and fecundity for laboratory strain of two Tephritid (Diptera: Tephritidae) species: implications for mass rearing. Economical Entomology 82(1), 104–106.Google Scholar
Lauzon, C.R., Sjogren, R.E. & Prokopy, R.J. (2000) Enzymatic capabilities of bacteria associated with apple maggot flies: a postulated role in attraction. Journal of Chemical Ecology 26, 953–967.Google Scholar
Lauzon, C.R., Bussert, T.G., Sjogren, R.E. & Prokopy, R.J. (2013) Serratia marcescens as a bacterial pathogen of Rhagoletis pomonella flies (Diptera: Tephritidae). European Journal of Entomology 100(1), 87–92.Google Scholar
Lee, J.B., Park, K.E., Lee, S.A., Jang, S.H., Eo, H.J., Jang, H.A., Kim, C.H., Ohbayashi, T., Matsuura, Y., Kikuchi, Y., Futahashi, R., Fukatsu, T. & Lee, B.L. (2017) Gut symbiotic bacteria stimulate insect growth and egg production by modulating hexamerin and vitellogenin gene expression. Developmental and Comparative Immunology 69, 12–22.Google Scholar
Li, Y.L., Wu, Y., Chen, H., Wu, J.J. & Li, Z.H. (2012) Population structure and colonization of Bactrocera dorsalis (Diptera: Tephritidae) in China, inferred from mtDNA COI sequences. Journal of Applied Entomology 136, 241–251.Google Scholar
Li, J.H., Evans, J.D., Li, W.F., Zhao, Y.Z., DeGrandi-Hoffman, G., Huang, S.K., Li, Z.G., Hamilton, M. & Chen, Y.P. (2017) New evidence showing that the destruction of gut bacteria by antibiotic treatment could increase the honey bee's vulnerability to Nosema infection. PLoS ONE 12(11), e0187505.Google Scholar
Lin, X.L., Kang, Z.W., Pan, Q.J. & Liu, T.X. (2015) Evaluation of five antibiotics on larval gut bacterial diversity of Plutella xylostella (Lepidoptera: Plutellidae). Insect Science 22, 619–628.Google Scholar
Liu, L.J., Martinez-Sanudo, I., Mazzon, L., Prabhakar, C.S., Girolami, V., Deng, Y.L., Dai, Y. & Li, Z.H. (2016) Bacterial communities associated with invasive populations of Bactrocera dorsalis (Diptera: Tephritidae) in China. Bulletin of Entomological Research 106, 718–728.Google Scholar
Louradour, I., Monteiro, C.C., Inbar, E., Ghosh, K., Merkhofer, R., Lawyer, P., Paun, A., Smelkinson, M., Secundino, N., Lewis, M., Erram, D., Zurek, L. & Sacks, D. (2017) The midgut microbiota plays an essential role in sand fly vector competence for Leishmania major. Cellular Microbiology 19(10), doi: 10.1111/cmi.12755Google Scholar
Mazzon, L., Piscedda, A., Simonato, M., Martinez-Sañudo, I., Squartini, A. & Girolami, V. (2008) Presence of specific symbiotic bacteria in flies of the subfamily Tephritinae (Diptera: Tephritidae) and their phylogenetic relationships: proposal of ‘Candidatus Stammerula tephritidis’. International Journal of Systematic Evolutionary Microbiology 58, 1277–1287.Google Scholar
Mazzon, L., Martinez-Sanudo, I., Simonato, M., Squartini, A., Savio, C. & Girolami, V. (2010) Phylogenetic relationships between flies of the Tephritinae subfamily (Diptera, Tephritidae) and their symbiotic bacteria. Molecular Phylogenetics and Evolution 56, 312–326.Google Scholar
Miyazaki, S., Boush, G.M. & Baerwald, R.J. (1968) Amino acid synthesis by Pseudomonas melophthora bacterial symbiote of Rhagoletis pomonella (Diptera). Journal of Insect Physiology 14, 513–518.Google Scholar
Morrow, J.L., Frommer, M., Shearman, D.C.A. & Riegler, M. (2015) The microbiome of field-caught and laboratory adapted Australian tephritid fruit fly species with different host plant use and specialisation. Microbial Ecology 70, 498–508.Google Scholar
Myint Khaing, M., Yang, X., Zhao, M., Zhang, W., Wang, B., Wei, J. & Liang, G. (2017) Effects of antibiotics on biological activity of Cry1Ac in Bt-susceptible and Bt-resistant Helicoverpa armigera strains. Journal of Invertebrate Pathology 151, 197–200.Google Scholar
Naaz, N., Choudhary, J.S., Prabhakar, C.S. & Maurya, M.S. (2016) Identification and evaluation of cultivable gut bacteria associated with peach fruit fly, Bactrocera zonata (Diptera: Tephritidae). Phytoparasitica 44, 165–176.Google Scholar
Noyce, G.L., Fulthorpe, R., Gorgolewski, A., Hazlett, P., Honghi, T. & Basiliko, N. (2016) Soil microbial responses to wood ash addition and forest fire in managed Ontario forests. Applied Soil Ecology 107, 368–380.Google Scholar
Peterson, B.E., Stewart, H.L. & Scharf, M.E. (2015) Quantification of symbiotic contributions to lower termite lignocellulose digestion using antimicrobial treatments. Insect Biochemistry and Molecular Biology 59, 80–88.Google Scholar
Prabhakar, C., Sood, P., Kapoor, V., Kanwar, S., Mehta, P. & Sharma, P. (2009) Molecular and biochemical characterization of three bacterial symbionts of fruit fly, Bactrocera tau (Tephritidae: Diptera). Journal of General and Applied Microbiology 55, 479–487.Google Scholar
Prabhakar, C.S., Sood, P., Kanwar, S.S., Sharma, P.N., Kumar, A. & Mehta, P.K. (2013) Isolation and characterization of gut bacteria of fruit fly, Bactrocera tau (Walker). Phytoparasitica 41, 193–201.Google Scholar
Raina, H.S., Rawal, V., Singh, S., Daimei, G., Shakarad, M. & Rajagopal, R. (2015) Elimination of Arsenophonus and decrease in the bacterial symbionts diversity by antibiotic treatment leads to increase in fitness of whitefly, Bemisia tabaci. Infection Genetics and Evolution 32, 224–230.Google Scholar
Rashid, M.A., Andongma, A.A., Dong, Y.C., Ren, X.M. & Niu, C.Y. (2018) Effect of gut bacteria on fitness of the Chinese citrus fly, Bactrocera minax (Diptera: Tephritidae). Symbiosis 76(1), 63–69.Google Scholar
Robacker, D.C., Lauzon, C.R. & He, X.D. (2004) Volatiles production and attractiveness to the Mexican fruit fly of Enterobacter agglomerans isolated from apple maggot and Mexican fruit flies. Journal of Chemical Ecology 30, 1329–1347.Google Scholar
Robacker, D.C., Lauzon, C.R., Patt, J., Margara, F. & Sacchetti, P. (2009) Attraction of Mexican fruit flies (Diptera: Tephritidae) to bacteria: effects of culturing medium on odour volatiles. Journal of Applied Entomology 133, 155–163.Google Scholar
Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E. B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., Van Horn, D.J. & Weber, C.F. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75, 7537–7541.Google Scholar
Schmieder, R. & Edwards, R. (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics (Oxford, England) 27(6), 863–864.Google Scholar
Schutze, M.K., Mahmood, K., Pavasovic, A., Bo, W., Newman, J., Clarke, A.R., Krosch, M.N. & Cameron, S.L. (2015) One and the same: integrative taxonomic evidence that Bactrocera invadens (Diptera: Tephritidae) is the same species as the Oriental fruit fly Bactrocera dorsalis. Systematic Entomology 40, 472–486.Google Scholar
Shi, Z.H., Wang, L.L. & Zhang, H.Y. (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). International Journal of Molecular Sciences 13, 6266–6278.Google Scholar
Sood, P. & Prabhakar, C.S. (2009) Molecular diversity and antibiotic sensitivity of gut bacterial symbionts of fruit fly, Bactrocera tau Walker. Journal of Biological Control 23(3), 213–220.Google Scholar
Sun, X., Cui, L.W. & Li, Z.H. (2007) Diversity and phylogeny of Wolbachia infecting Bactrocera dorsalis (Diptera: Tephritidae) populations from China. Environmental Entomology 36, 1283–1289.Google Scholar
Taylor, C., Johnson, V. & Dively, G. (2016) Assessing the use of antimicrobials to sterilize brown marmorated stink bug egg masses and prevent symbiont acquisition. Journal of Pest Science 90, 1287–1294.Google Scholar
Thakur, A., Dhammi, P., Saini, H.S. & Kaur, S. (2016) Effect of antibiotic on survival and development of Spodoptera litura (Lepidoptera: Noctuidae) and its gut microbial diversity. Bulletin of Entomological Research 106, 387–394.Google Scholar
Tsugeno, Y., Koyama, H., Takamatsu, T., Nakai, M., Kunimi, Y. & Inoue, M.N. (2017) Identification of an Early Maleilling agent in the oriental Tea Tortrix, Homona magnanima. Journal of Heredity 108, 553–560.Google Scholar
Wang, H.X., Jin, L. & Zhang, H.Y. (2011) Comparison of the diversity of the bacterial communities in the intestinal tract of adult Bactrocera dorsalis from three different populations. Journal of Applied Microbiology 110, 1390–1401.Google Scholar
Wang, H.X., Jin, L., Peng, T., Zhang, H.Y., Chen, Q.L. & Hua, Y.J. (2014) Identification of cultivable bacteria in the intestinal tract of Bactrocera dorsalis from three different populations and determination of their attractive potential. Pest Management Science 70, 80–87.Google Scholar
Xu, Y., Buss, E.A. & Boucias, D.G. (2016) Impacts of antibiotic and bacteriophage treatments on the gut-symbiont-associated Blissus insularis (Hemiptera: Blissidae). Insects 7(4), pii: E61.Google Scholar
Yao, Z.C., Wang, A.L., Li, Y.S., Cai, Z.H., Lemaitre, B. & Zhang, H.Y. (2016) The dual oxidase gene BdDuox regulates the intestinal bacterial community homeostasis of Bactrocera dorsalis. The ISME Journal 10, 1037–1050.Google Scholar
Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. (2014) PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics (Oxford, England) 30(5), 614–620.Google Scholar
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