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Genetic diversity and host relationships of endosymbiotic bacteria in the Asian cryptic species of Bemisia tabaci from Bangladesh

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Abstract

Endosymbiotic bacteria are common in many herbivorous insects. Bemisia tabaci is a phloem-sapping pest of various crop plants and is known to harbor at least five endosymbionts. This species is a complex of at least 40 genetically distinct but morphologically indistinguishable cryptic species worldwide. Endosymbiont composition has been studied in invasive cryptic species such as MEAM1 and MED, but little information exists regarding the indigenous genetic groups in Asia. Here, we determined the endosymbiont profiles of four indigenous Asian cryptic species (Asia I, Asia II 1, Asia II 5 and Asia II 10) of B. tabaci identified in Bangladesh. Overall, the infection rates of Arsenophonus, Cardinium, Hamiltonella, Rickettsia, and Wolbachia were 93%, 86%, 0%, 31%, and 88%, respectively. Phylogenetic analysis revealed two subgroups in Arsenophonus (A1, A2) and Rickettsia (R1, R2), but only one subgroup in Cardinium (C2) and Wolbachia (W1). Each endosymbiont showed varying rates of infection in the four cryptic species and most were co-infected with various combinations. The results of this study provide important information on the relationships between the endosymbionts and cryptic species of B. tabaci indigenous to Asia.

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References

  • Ahmed MZ, Barro PJ, Greeff JM, Ren SX, Naveed M, Qiu BL (2011) Genetic identity of the Bemisia tabaci species complex and association with high cotton leaf curl disease (CLCuD) incidence in Pakistan. Pest Manag Sci 67:307–317

    Article  CAS  PubMed  Google Scholar 

  • Ansari PG, Singh RK, Kaushik S, Krishna A, Wada T, Noda H (2017) Detection of symbionts and virus in the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae), a vector of the Mungbean yellow mosaic India virus in Central India. Appl Entomol Zool 52:567–579

    Article  CAS  Google Scholar 

  • Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microb 59:155–189

    Article  CAS  Google Scholar 

  • Bing XL, Ruan YM, Rao Q, Wang XW, Liu SS (2013a) Diversity of secondary endosymbionts among different putative species of the whitefly Bemisia tabaci. Insect Sci 20:194–206

    Article  CAS  PubMed  Google Scholar 

  • Bing XL, Yang J, Zchori-Fein E, Wang XW, Liu SS (2013b) Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl Environ Microbiol 79:569–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bing XL, Xia WQ, Gui JD, Yan GH, Wang XW, Liu SS (2014) Diversity and evolution of the Wolbachia endosymbionts of Bemisia tabaci (Hemiptera: Aleyrodidae) whiteflies. Ecol Evol 4:2714–2737

    Article  PubMed  PubMed Central  Google Scholar 

  • Cahill M, Denholm I, Bryne FJ, Al D (1996) Insecticide resistance in Bemisia tabaci- current status and implications for management. In: Proceedings of Brighton crop protection conference: Pest and diseases, vol 1, pp 75–80

    Google Scholar 

  • Chiel E, Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Katzir N, Inbar M, Ghanim M (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bull Entomol Res 97:407–413

    Article  CAS  PubMed  Google Scholar 

  • Chiel E, Inbar M, Mozes-Daube N, White JA, Hunter M, Zchori-Fein E (2009) Assessments of fitness effects by the facultative symbiont Rickettsia in the sweetpotato whitefly (Hemiptera: Aleyrodidae). Ann Entomol Soc Am 102:413–418

    Article  Google Scholar 

  • Chu D, Gao CS, De Barro P, Zhang YJ, Wan FH, Khan IA (2011) Further insights into the strange role of bacterial endosymbionts in whitefly, Bemisia tabaci: comparison of secondary symbionts from biotypes B and Q in China. Bull Entomol Res 101:477–486

    Article  CAS  PubMed  Google Scholar 

  • Correa CC, Ballard J (2016) Wolbachia associations with insects: winning or losing against a master manipulator. Front Ecol Evol 3:153

    Article  Google Scholar 

  • Czosnek H, Ghanim M (2011) Bemisia tabaci – tomato yellow leaf curl virus Interaction Causing Worldwide Epidemics. In: Thompson W (ed) The whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) interaction with Geminivirus-infected host plants. Springer, Dordrecht

    Google Scholar 

  • Dalton R (2006) Whitefly infestations: the Christmas invasion. Nature. 443:898–900

    Article  CAS  PubMed  Google Scholar 

  • De Barro PJ, Liu S, Boykin LM, Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19

    Article  CAS  PubMed  Google Scholar 

  • Dinsdale A, Cook L, Riginos C, Buckley YM, Barro PD (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc Am 103:196–208

    Article  Google Scholar 

  • Ellango R, Singh ST, Rana VS, Priya NG, Raina H, Chaubey R, Naveen NC, Mahmood R, Ramamurthy VV, Asokan R (2015) Distribution of Bemisia tabaci genetic groups in India. Environ Entomol 44:1258–1264

    Article  CAS  PubMed  Google Scholar 

  • Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Firdaus S, Vosman B, Hidayati N, Supena ED, Visser RG, Heusden AW (2013) The Bemisia tabaci species complex: additions from different parts of the world. Insect Sci 20:723–733

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Bouvaine S, Maruthi M (2015) Prevalence and genetic diversity of endosymbiotic bacteria infecting cassava whiteflies in Africa. BMC Microbiol 15:93

    Article  PubMed  PubMed Central  Google Scholar 

  • Gnankine O, Mouton L, Henri H, Terraz G, Houndate T, Martin T, Vavre F, Fleury F (2013) Distribution of Bemisia tabaci (Homoptera: Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa. Insect Conserv Divers 6:411–421

    Article  Google Scholar 

  • Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N (2006) Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl Environ Microbiol 72:3646–3652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, Fleury F, Zchori-Fein E (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J 22:2591–2599

    Article  CAS  PubMed  Google Scholar 

  • Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M, Brumin M, Sobol I, Czosnek H, Vavre F, Fleury F, Ghanim M (2010) The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. J Virol 84:9310–9317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Götz M, Winter S (2016) Diversity of Bemisia tabaci in Thailand and Vietnam and indications of species replacement. J Asia Pac Entomol 19:537–543

    Article  Google Scholar 

  • Gueguen G, Vavre F, Gnankine O, Peterschmitt M, Charif D, Chiel E, Gottlieb Y, Ghanim M, Zchori-Fein E, Fleury F (2010) Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol Ecol 19:4365–4376

    Article  PubMed  Google Scholar 

  • Hameed S, Hameed S, Sadia M, Malik SA (2012) Genetic diversity analysis of Bemisia tabaci populations in Pakistan using RAPD markers. Electron J Biotechnol 15

  • Hashmi TR, Devi SR, Meshram NM, Prasad R (2018) Assessment of bacterial endosymbiont and the host Bemisia tabaci (Hemiptera: Aleyrodidae), using rRNA and mitochondrial cytochrome oxidase I gene sequences. Commun Integr Biol 11:e1433442

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 332:254–256

    Article  CAS  PubMed  Google Scholar 

  • Horowitz AR, Kontsedalov S, Khasdan V, Ishaaya I (2005) Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Arch Insect Biochem Physiol 58:216–225

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Chen YD, Jiang ZL, Nardi F, Yang TY, Jin J, Zhang ZK (2015) Global haplotype analysis of the whitefly Bemisia tabaci cryptic species Asia I in Asia. Mito DNA 26:232–241

    Article  CAS  Google Scholar 

  • Hu J, Zhang X, Jiang Z, Zhang F, Liu Y, Li Z, Zhang Z (2017) New putative cryptic species detection and genetic network analysis of Bemisia tabaci (Hemiptera: Aleyrodidae) in China based on mitochondrial COI sequences. Mito DNA Part A 29:474–484

    Article  CAS  Google Scholar 

  • Hunter MS, Perlman SJ, Kelly SE (2003) A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc Biol Sci 270:2185–2190

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiu M, Hu J, Wang LJ, Dong JF, Song YQ, Sun HZ (2017) Cryptic species identification and composition of Bemisia tabaci (Hemiptera: Aleyrodidae) complex in Henan Province, China. J Insect Sci 17:1–7

    Article  Google Scholar 

  • Jones DR (2003) Plant viruses transmitted by whiteflies. Eur J Plant Pathol 109:195–219

    Article  Google Scholar 

  • Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners are mediated by bacterial symbionts. Proc Biol Sci 277:2311–2319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khatun MF, Jahan SMH, Lee S, Lee KY (2018) Genetic diversity and geographic distribution of the Bemisia tabaci species complex in Bangladesh. Acta Trop 187:28–36

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kontsedalov S, Zchori-Fein E, Chiel E, Gottlieb Y, Inbar M, Ghanim M (2008) The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Manag Sci 64:789–792

    Article  CAS  PubMed  Google Scholar 

  • Kumar NR, Chang JC, Narayanan MB, Ramasamy S (2016) Phylogeographical structure in mitochondrial DNA of whitefly, Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) in southern India and Southeast Asia. Mito DNA Part A 28:621–631

    Article  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinfo 25:1451–1452

    Article  CAS  Google Scholar 

  • Liu SS, De Barro PJ, Xu J, Luan JB, Zang LS, Ruan YM, Wan FH (2007) Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318:1769–1772

    Article  CAS  PubMed  Google Scholar 

  • Marubayashi JM, Kliot A, Yuki VA, Rezende JAM, Krause-Sakate R, Pavan MA, Ghanim M (2014) Diversity and localization of bacterial endosymbionts from whitefly species collected in Brazil. PLoS One 9:e108363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195

    Article  Google Scholar 

  • Nirgianaki A, Banks GK, Frohlich DR, Veneti Z, Braig HR, Miller TA, Bedford ID, Markham PG, Savakis C, Bourtzis K (2003) Wolbachia infections of the whitefly Bemisia tabaci. Curr Microbiol 47:93–101

    Article  CAS  PubMed  Google Scholar 

  • Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci U S A 100:1803–1807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan H, Li X, Ge D, Wang S, Wu Q, Xie W, Jiao X, Chu D, Liu B, Xu B, Zhang Y (2012) Factors affecting population dynamics of maternally transmitted endosymbionts in Bemisia tabaci. PLoS One 7:e30760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park J, Jahan SMH, Song WG, Lee H, Lee YS, Choi HS, Lee KS, Kim CS, Lee S, Lee KY (2012) Identification of biotypes and secondary endosymbionts of Bemisia tabaci in Korea and relationships with the occurrence of TYLCV disease. J Asia Pac Entomol 15:186–191

    Article  CAS  Google Scholar 

  • Pascual S, Callejas C (2004) Intra and interspecific competition between biotypes B and Q of Bemisia tabaci (Hemiptera: Aleyrodidae) from Spain. Bull Entomol Res 94:369–375

    Article  CAS  PubMed  Google Scholar 

  • Prasanna HC, Kanakala S, Archana K, Jyothsna P, Varma RK, Malathi VG (2015) Cryptic species composition and genetic diversity within Bemisia tabaci complex in soybean in India revealed by mtCOI DNA sequence. J Integr Agr 14:1786–1795

    Article  CAS  Google Scholar 

  • Rao Q, Wang S, Su YL, Bing XL, Liu SS, Wang XW (2012) Draft genome sequence of “candidatus Hamiltonella defensa,” an endosymbiont of the whitefly Bemisia tabaci. J Bacteriol 194:3558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosell RC, Blackmer JL, Czosnek H, Inbar M (2010) In: Stansly PA, Naranjos SE (eds) Bemisia: Bionomics and Management of a Global PestMutualistic and dependent relationships with other organisms. Springer, Netherlands, pp 161–183

    Google Scholar 

  • Schaffer AA, Aravind L, Madden TL, Shavirin S, Spouge JL, Wolf YI, Koonin EV, Altschul SF (2001) Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements. Nucleic Acids Res 29:2994–3005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shah SHJ, Malik AH, Qazi J (2013) Identification of new genetic variant of Bemisia tabaci from Pakistan. Int J Entomol Res 1:16–24

    Google Scholar 

  • Singh ST, Priya NG, Kumar J, Rana VS, Ellango R, Joshi A, Priyadarshini G, Asokan R, Rajagopal R (2012) Diversity and phylogenetic analysis of endosymbiotic bacteria from field caught Bemisia tabaci from different locations of North India based on 16S r DNA library screening. Infect Genet Evol 12:411–419

    Article  PubMed  Google Scholar 

  • Sintupachee S, Milne JR, Poonchaisri S, Baimai V, Kittayapong P (2006) Closely related Wolbachia strains within the pumpkin arthropod community and the potential for horizontal transmission via the plant. Microb Ecol 51:294–301

    Article  CAS  PubMed  Google Scholar 

  • Skaljac M, Zanic K, Ban SG, Kontsedalov S, Ghanim M (2010) Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiol 10:142

    Article  PubMed  PubMed Central  Google Scholar 

  • Skaljac M, Zanic K, Hrncic S, Radonjic S, Perovic T, Ghanim M (2013) Diversity and localization of bacterial symbionts in three whitefly species (Hemiptera: Aleyrodidae) from the east coast of the Adriatic Sea. Bull Entomol Res 103:48–59

    Article  CAS  PubMed  Google Scholar 

  • Skaljac M, Kanakala S, Zanic K, Puizina J, Pleic IL, Ghanim M (2017) Diversity and phylogenetic analyses of bacterial symbionts in three whitefly species from Southeast Europe. Insects 8:113

    Article  PubMed Central  Google Scholar 

  • Tajima F (1989) A statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang XT, Cai L, Shen Y, Du YZ (2018) Diversity and evolution of the endosymbionts of Bemisia tabaci in China. PeerJ 6:e5516

    Article  PubMed  PubMed Central  Google Scholar 

  • Thao ML, Baumann P (2004) Evidence for multiple acquisitions of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Curr Microbiol 48:140–144

    Article  CAS  PubMed  Google Scholar 

  • Thierry M, Becker N, Hajri A, Lett JM, Reynaud B, Delatte H (2011) Symbiont diversity and non-random hybridization among indigenous (Ms) and invasive (B) biotypes of Bemisia tabaci. Mol Ecol 20:2172–2187

    Article  CAS  PubMed  Google Scholar 

  • Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989

    Article  CAS  PubMed  Google Scholar 

  • Weeks AR, Velten R, Stouthamer R (2003) Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc Biol Sci 270:1857–1865

  • Zchori-Fein E, Brown JK (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera; Aleyrodidae). Ann Entomol Soc Am 95:711–718

  • Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:2009–2016

    Article  CAS  PubMed  Google Scholar 

  • Zchori-Fein E, Gottlieb Y, Kelly SE, Brown JK, Wilson JM, Karr TL, Hunter MS (2001) A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc Natl Acad Sci U S A 98:12555–12560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zchori-Fein E, Lahav T, Freilich S (2014) Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Front Microbiol 5:1–8

    Article  Google Scholar 

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Acknowledgments

We thank Hwal-Su Hwang at Kyungpook National University in the Republic of Korea for his help with sequencing and molecular analysis. This work was supported by the Research Program for Exportation Support of Agricultural Products, Animal and Plant Quarantine Agency, in the Republic of Korea under Grant (#Z-1543086-2017-21-01).

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  1. Division of Applied Biosciences, College of Agriculture and Life Sciences, Kyungpook National University, Daegu, 41566, Republic of Korea

    Mst. Fatema Khatun, Jae-Kyoung Shim & Kyeong-Yeoll Lee

  2. Department of Entomology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Dhaka, Bangladesh

    Mst. Fatema Khatun

  3. Institute of Agricultural Science and Technology, Kyungpook National University, Daegu, Republic of Korea

    Jae-Kyoung Shim & Kyeong-Yeoll Lee

  4. Institute of Plant Medicine, Kyungpook National University, Daegu, Republic of Korea

    Kyeong-Yeoll Lee

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Khatun, M.F., Shim, JK. & Lee, KY. Genetic diversity and host relationships of endosymbiotic bacteria in the Asian cryptic species of Bemisia tabaci from Bangladesh. Symbiosis 79, 75–87 (2019). https://doi.org/10.1007/s13199-019-00622-6

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