Intracellular symbionts drive sex ratio in the whitefly by facilitating fertilization and provisioning of B vitamins

McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA. 2013;110:3229–36.

CAS  PubMed  Google Scholar 

Moran NA, Bennett GM. The tiniest tiny genomes. Annu Rev Microbiol. 2014;68:195–215.

CAS  PubMed  Google Scholar 

Douglas AE. Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol. 2015;60:17–34.

CAS  PubMed  Google Scholar 

Engelstädter J, Hurst GDD. The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst. 2009;40:127–49.

Google Scholar 

Ma WJ, Schwander T. Patterns and mechanisms in instances of endosymbiont-induced parthenogenesis. J Evol Biol. 2017;30:868–88.

PubMed  Google Scholar 

Bondy EC, Hunter MS. Sex ratios in the haplodiploid herbivores, aleyrodidae and thysanoptera: a review and tools for study. Adv Insect Physiol. 2019;56:251–81.

Google Scholar 

Hunter MS, Perlman SJ, Kelly SE. A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc Natl Acad Sci USA. 2003;270:2185–90.

Google Scholar 

Beckmann JF, Ronau JA, Hochstrasser MA. Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat Microbiol 2017;2:17007.

PubMed  PubMed Central  Google Scholar 

Harumoto T, Lemaitre B. Male-killing toxin in a bacterial symbiont of Drosophila. Nature 2018;557:252–5.

CAS  PubMed  PubMed Central  Google Scholar 

Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci USA. 2010;107:769–74.

CAS  PubMed  Google Scholar 

Michalkova V, Benoit JB, Weiss BL, Attardo GM, Aksoy S. Vitamin B6 generated by obligate symbionts is critical for maintaining proline homeostasis and fecundity in tsetse flies. Appl Environ Microbiol. 2014;80:5844–53.

PubMed  PubMed Central  Google Scholar 

Moriyama M, Nikoh N, Hosokawa T, Fukatsu T. Riboflavin provisioning underlies Wolbachia’s fitness contribution to its insect host. mBio . 2015;6:e01732–15.

CAS  PubMed  PubMed Central  Google Scholar 

Snyder AK, Rio RVM. ‘Wigglesworthia morsitans’ folate (vitamin B9) biosynthesis contributes to tsetse host fitness. Appl Environ Microbiol. 2015;81:5375–86.

CAS  PubMed  PubMed Central  Google Scholar 

Ju JF, Bing XL, Zhao DS, Guo Y, Xi Z, Hoffmann AA, et al. Wolbachia supplement biotin and riboflavin to enhance reproduction in planthoppers. ISME J. 2019;14:676–87.

PubMed  Google Scholar 

Tsuchida T, Koga R, Shibao H, Matsumoto T, Fukatsu T. Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol Ecol. 2002;11:2123–35.

CAS  PubMed  Google Scholar 

Baumann P. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol. 2005;59:155–89.

CAS  PubMed  PubMed Central  Google Scholar 

Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, Fleury F, et al. Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J. 2008;22:2591–9.

CAS  PubMed  Google Scholar 

Sloan DB, Moran NA. Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Mol Biol Evol. 2012;29:3781–92.

CAS  PubMed  PubMed Central  Google Scholar 

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

PubMed  PubMed Central  Google Scholar 

McCutcheon JP, Von Dohlen CD. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol. 2011;21:1366–72.

CAS  PubMed  PubMed Central  Google Scholar 

Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, et al. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell. 2013;153:1567–78.

CAS  PubMed  Google Scholar 

Koga R, Meng XY, Tsuchida T, Fukatsu T. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proc Natl Acad Sci USA. 2012;109:E1230–E1237.

CAS  PubMed  Google Scholar 

Fukatsu T, Nikoh N. Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl Environ Microbiol. 1998;64:3599–606.

CAS  PubMed  PubMed Central  Google Scholar 

Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci USA. 2009;106:9063–8.

CAS  PubMed  Google Scholar 

Rao Q, Wang S, Su YL, Bing XL, Liu SS, Wang XW. Draft genome sequence of ‘Candidatus Hamiltonella defensa’ an endosymbiont of the whitefly Bemisia tabaci. J Bacteriol. 2012;194:3558.

CAS  PubMed  PubMed Central  Google Scholar 

Xue J, Zhou X, Zhang CX, Yu LL, Fan HW, Wang Z, et al. Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. Genome Biol. 2014;15:521.

PubMed  PubMed Central  Google Scholar 

Santos-Garcia D, Juravel K, Freilich S, Zchori-Fein E, Latorre A, Moya A, et al. To B or not to B: comparative genomics suggests Arsenophonus as a source of B vitamins in whiteflies. Front Microbiol. 2018;9:2254–70.

PubMed  PubMed Central  Google Scholar 

Ouvrard D, Martin JH. The whiteflies: taxonomic checklist of the world’s whiteflies (Insecta: Hemiptera: Aleyrodidae). 2019. http://www.hemiptera-databases.org/whiteflies/.

Yang P. The greenhouse whiteflies and plant quarantine. Chin Bull Entomol. 1981;18:69–71.

Google Scholar 

Liu SS, De Barro PJ, Xu J, Luan JB, Zang LS, Ruan YM, et al. Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science . 2007;318:1769–72.

CAS  PubMed  Google Scholar 

Zchori-Fein E, Lahav T, Freilich S. Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Front Microbiol. 2014;5:310.

PubMed  PubMed Central  Google Scholar 

Luan JB, Shan HW, Isermann P, Huang JH. Cellular and molecular remodelling of a host cell for vertical transmission of bacterial symbionts. Proc R Soc B. 2016;283:20160580.

PubMed  Google Scholar 

Luan JB, Sun XP, Fei ZJ, Douglas AE. Maternal inheritance of a single somatic animal cell displayed by the bacteriocyte in the whitefly Bemisia tabaci. Curr Biol. 2018;28:459–65.

CAS  PubMed  PubMed Central  Google Scholar 

Shan HW, Luan JB, Liu YQ, Douglas AE, Liu SS. The inherited bacterial symbiont Hamiltonella influences the sex ratio of an insect host. Proc R Soc B. 2019;286:20191677.

CAS  PubMed  Google Scholar 

Rao Q, Rollat-Farnier PA, Zhu DT, Santos-Garcia D, Silva FJ, Moya A, et al. Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci. BMC Genom. 2015;16:226.

Google Scholar 

Scott IAW, Workman PJ, Drayton GM, Burnip GM. First record of Bemisia tabaci biotype Q in New Zealand. N Z Plant Prot. 2007;60:264–70.

CAS  Google Scholar 

Qin L, Pan LL, Liu SS. Further insight into reproductive incompatibility between putative cryptic species of the Bemisia tabaci whitefly complex. Insect Sci. 2016;23:215–24.

CAS  PubMed  Google Scholar 

Xu XR, Li NN, Bao XY, Douglas AE, Luan JB. Patterns of host cell inheritance in the bacterial symbiosis of whiteflies. Insect Sci. 2019; https://doi.org/10.1111/1744-7917.12708.

Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008;3:1101–8.

CAS  PubMed  Google Scholar 

Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, et al. Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl Environ Microbiol. 2006;72:3646–52.

CAS  PubMed  PubMed Central  Google Scholar 

Hadjistylli M, Schwartz SA, Brown JK, Roderick GK. Isolation and characterization of nine microsatellite loci from Bemisia tabaci (Hemiptera: Aleyrodidae) biotype B. J Insect Sci. 2014;14:148.

CAS  PubMed  PubMed Central  Google Scholar 

Bondy EC, Hunter MS. Determining the egg fertilization rate of Bemisia tabaci using a cytogenetic technique. J Vis Exp. 2019;https://doi.org/10.3791/59213.

Ankrah NYD, Luan JB, Douglasa AE. Cooperative metabolism in a three-partner insect-bacterial symbiosis revealed by metabolic modeling. J Bacteriol 2017;199:e00872–16.

CAS  PubMed  PubMed Central  Google Scholar 

Ren FR, Bai B, Hong JS, Huang YZ, Luan JB. A microbiological assay for biotin determination in insects. Insect Sci. 2020; https://doi.org/10.1111/1744-7917.12827.

Salem H, Bauer E, Strauss AS, Vogel H, Marz M, Kaltenpoth M. Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host. Proc R Soc B. 2014;281:1838.

Google Scholar 

Duron O, Morel O, Noël V, Buysse M, Binetruy F, Lancelot R, et al. Tick-bacteria mutualism depends on B vitamin synthesis pathways. Curr Biol. 2018;28:1896–902.

CAS  PubMed  Google Scholar 

Pant NC, Fraenkel G. The function of the symbiotic yeasts of two insect species, Lasioderma serricorne F. and Stegobium (Sitodrepa) paniceum L. Science. 1950;112:498–500.

CAS  PubMed  Google Scholar 

Byrne DN, Bellows TS Jr. Whitefly biology. Annu Rev Entomol. 1991;36:431–57.

Google Scholar 

Giorgini M, Monti MM, Caprio E, Stouthamer R, Hunter MS. Feminization and the collapse of haplodiploidy in an asexual parasitoid wasp harboring the bacterial symbiont Cardinium. Heredity. 2009;102:365–71.

CAS  PubMed  Google Scholar 

Ma WJ, Pannebakker BA, van de Zande L, Schwander T, Wertheim B, Beukeboom LW. Diploid males support a two-step mechanism of endosymbiont-induced thelytoky in a parasitoid wasp. BMC Evol Biol. 2015;15:84.

PubMed  PubMed Central  Google Scholar 

Sloan DB, Moran NA. The evolution of genomic instability in the obligate endosymbionts of whiteflies. Genome Biol Evol. 2013;5:783–93.

PubMed  PubMed Central  Google Scholar 

Chen W, Hasegawa DK, Kaur N, Kliot A, Pinheiro PV, Luan JB, et al. The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance. BMC Biol. 2016;14:110.

PubMed  PubMed Central  Google Scholar 

Luan JB, Chen W, Hasegawa DK, Simmons A, Wintermantel WM, Ling KS, et al. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome Biol Evol. 2015;7:2635–47.

CAS  PubMed  PubMed Central  Google Scholar 

Russell JA, Latorre A, Sabater-Muñoz B, Moya A, Moran NA. Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol. 2003;12:1061–75.

CAS  PubMed  Google Scholar 

Manzano-Marı́n A, Coeur d’acier A, Clamens AL, Orvain C, Cruaud C, Barbe V, et al. Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems. ISME J. 2020;14:259–73.

Google Scholar 

Ayoubi A, Talebi AA, Fathipour Y, Mehrabadi M. Coinfection of the secondary symbionts, Hamiltonella defensa and Arsenophonus sp. contribute to the performance of the major aphid pest, Aphis gossypii (Hemiptera: Aphididae). Insect Sci. 2020;27:86–98.

PubMed  Google Scholar 

Thao MLL, Baumann P. Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Curr Microbiol. 2004;48:140–4.

CAS  PubMed  Google Scholar 

Nováková E, Hypša V, Moran NA. Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol. 2009;9:143.

PubMed  PubMed Central  Google Scholar 

Nováková E, Husník F, Šochová E, Hypša V. Arsenophonus and Sodalis symbionts in louse flies: an analogy to the Wigglesworthia and Sodalis system in tsetse flies. Appl Environ Microbiol. 2015;81:6189–99.

PubMed  PubMed Central  Google Scholar 

Nikoh N, Hosokawa T, Moriyama M, Oshima K, Hattori M, Fukatsu T. Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc Natl Acad Sci USA. 2014;111:10257–62.

CAS  PubMed  Google Scholar 

Wu D, Daugherty SC, Van Aken SE, Pai GH, Watkins KL, Khouri H, et al. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 2006;4:e188.

PubMed  PubMed Central  Google Scholar 

McCutcheon JP, Moran NA. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA. 2007;104:19392–7.

CAS  PubMed  Google Scholar 

McCutcheon JP, McDonald BR, Moran NA. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci USA. 2009;106:15394–9.

CAS  PubMed  Google Scholar 

Matsuura Y, Moriyama M, Łukasik P, Vanderpool D, Tanahashi M, Meng XY, et al. Recurrent symbiont recruitment from fungal parasites in cicadas. Proc Natl Acad Sci USA. 2018;115:E5970–E5979.

CAS  PubMed  Google Scholar 

Kapantaidaki DE, Ovcarenko I, Fytrou N, Knott KE, Bourtzis K, Tsagkarakou A. Low levels of mitochondrial DNA and symbiont diversity in the worldwide agricultural pest, the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). J Hered. 2014;106:80–92.

PubMed  Google Scholar 

Douglas AE. The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally acquired genes. Curr Opin Insect Sci. 2017;23:65–69.

PubMed  Google Scholar 

Smykal V, Raikhel AS. Nutritional control of insect reproduction. Curr Opin Insect Sci. 2015;11:31–38.

PubMed  PubMed Central  Google Scholar 

Wheeler D. The role of nourishment in oogenesis. Ann Rev Entomol. 1996;41:407–31.

CAS  Google Scholar 

Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, et al. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science. 2011;332:254–6.

CAS  PubMed  Google Scholar