Prevalence and genetic diversity of endosymbiotic bacteria infecting cassava whiteflies in Africa

BMC Microbiology

MN Maruthi¹  Sophie Bouvaine¹  Saptarshi Ghosh¹ 

[1] Natural Resources Institute, University of Greenwich, Chatham ME4 4 TB, Kent, UK

关键词: Arsenophonus;    Rickettsia;    Wolbachia;    mtCOI;    Whitefly;    Cassava;   

Others  :  1212050
DOI  :  10.1186/s12866-015-0425-5

 received in 2014-11-24, accepted in 2015-04-15,  发布年份 2015

【 摘 要 】

Background

Cassava provides over half of the dietary requirement for more than 200 million poor in Africa. In recent years, cassava has been affected by an epidemic of a virus disease called cassava brown streak disease (CBSD) that is spreading in much of eastern and central Africa, affecting food security and the economic development of the poor. The viruses that cause CBSD are transmitted by the insect vector whitefly (Bemisia tabaci), which have increased to very high numbers in some African countries. Strains of endosymbiotic bacteria infecting whiteflies have been reported to interact specifically with different whitefly populations with varied effects on its host biology and efficiency of virus transmission. The main aim of this study was therefore to investigate the prevalence and diversity of the secondary endosymbiotic bacteria infecting cassava whiteflies with a view to better understand their role on insect population dynamics and virus disease epidemics.

Results

The genetic diversity of field-collected whitefly from Tanzania, Malawi, Uganda and Nigeria was determined by mitochondrial DNA based phylogeny and restriction fragment length polymorphism. Cassava in these countries was infected with five whitefly populations, and each one was infected with different endosymbiotic bacteria. Incidences of Arsenophonus, Rickettsia, Wolbachia and Cardinium varied amongst the populations. Wolbachia was the most predominant symbiont with infection levels varying from 21 to 97%. Infection levels of Arsenophonus varied from 17 to 64% and that of Rickettsia was 0 to 53%. Hamiltonella and Fritschea were absent in all the samples. Multiple locus sequence typing identified four different strains of Wolbachia infecting cassava whiteflies. A common strain of Wolbachia infected the whitefly population Sub-Saharan Africa 1-subgroup 1 (SSA1-SG1) and SSA1-SG2, while others were infected with different strains. Phylogeny based on 16S rDNA of Rickettsia and 23S rDNA of Arsenophonus also identified distinct strains.

Conclusions

Genetically diverse bacteria infect cassava whiteflies in Africa with varied prevalence across different host populations, which may affect their whitefly biology. Further studies are required to investigate the role of endosymbionts to better understand the whitefly population dynamics.

【 授权许可】

   
2015 Ghosh et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

Figure 10.

【 参考文献 】

• [1]Jones DR. Plant viruses transmitted by whiteflies. Eur J Plant Path. 2003;(109):195–219.
• [2]De Barro PJ, Liu SS, Boykin LM, Dinsdale AB. Bemisia tabaci: a statement of species status. Ann Rev Entomol. 2011; 56:1-19.
• [3]Dinsdale A, Cook L, Riginos C, Buckley YM, De Barro P. Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc Am. 2010; 103:196-208.
• [4]Brown JK. Phylogenetic biology of the Bemisia tabaci sibling species group. In: Bemisia: bionomics and management of a global pest. Stansley PA, Naranjo SE, editors. Springer, Dordrecht-Heidelberg-London-New York; 2010: p.31-67.
• [5]Legg JP, Fauquet CM. Cassava viruses in Africa. Plant Mol Biol. 2004; 56:585-99.
• [6]Legg JP, Sseruwagi P, Boniface S, Okao-Okuja G, Shirima R, Bigirimana S et al.. Spatio-temporal patterns of genetic change amongst populations of cassava Bemisia tabaci whiteflies driving virus pandemics in East and Central Africa. Virus Res. 2013; 186:61-75.
• [7]Legg JP, French R, Rogan D, Okao-Okuja G, Brown JK. A distinct Bemisia tabaci (Gennadius) (Hemiptera: Sternorrhyncha: Aleyrodidae) genotype cluster is associated with the epidemic of severe cassava mosaic virus disease in Uganda. Mol Ecol. 2002; 11:1219-29.
• [8]Legg JP, Owor B, Sseruwagi P, Ndunguru J. Cassava mosaic virus disease in East and Central Africa: epidemiology and management of a regional pandemic. Adv Virus Res. 2006; 67:355-418.
• [9]Simón B, Cenis JL, De La Rúa P. Distribution patterns of the Q and B biotypes of Bemisia tabaci in the mediterranean basin based on microsatellite variation. Entomol Exp Appl. 2007; 124:327-36.
• [10]McKenzie CL, Hodges G, Osborne LS, Byrne FJ, Shatters JRG. Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in Florida-investigating the Q invasion. J Econ Entomol. 2009; 102:670-6.
• [11]Pan H, Chu D, Ge D, Wang S, Wu Q, Xie W et al.. Further spread of and domination by Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q on field crops. China J Econ Entomol. 2011; 104:978-85.
• [12]Zchori-Fein E, Brown JK. Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Ann Entomol Soc Am. 2002; 95:711-8.
• [13]Ahmed MZ, Ren S, Xue X, Li XX, Jin G, Qiu BL. Prevalence of endosymbionts in Bemisia tabaci populations and their in vivo sensitivity to antibiotics. Curr Microbiol. 2010; 61:322-8.
• [14]Gueguen G, Vavre F, Gnankine O, Peterschmitt M, Charif D, Chiel E et al.. Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol Ecol. 2010; 19:4365-78.
• [15]Bing XL, Yang J, Zchori-Fein E, Wang XW, Liu SS. Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl Environ Microb. 2013; 79:569-75.
• [16]Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol. 2008; 6:741-51.
• [17]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.
• [18]Brumin M, Kontsedalov S, Ghanim M. Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci. 2011; 18:57-66.
• [19]Hendry TA, Hunter MS, Baltrus DA. The facultative symbiont Rickettsia protects an invasive whitefly against entomopathogenic Pseudomonas syringae strains. Appl Env Microb. 2014; 80:7161-8.
• [20]Kontsedalov S, Zchori‐Fein E, Chiel E, Gottlieb Y, Inbar M, Ghanim M. The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Manag Sci. 2008; 64:789-92.
• [21]Everett KDE, Thao M, Horn M, Dyszynski GE, Baumann P. Novel chlamydiae in whiteflies and scale insects: endosymbionts “Candidatus Fritschea bemisiae” strain Falk and “Candidatus Fritschea eriococci” strain Elm. Int J Syst Evol Micr. 2005; 55:1581-7.
• [22]Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M, Brumin M et al.. 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. 2010; 84:9310-7.
• [23]Rana VS, Singh ST, Priya NG, Kumar J, Rajagopal R. Arsenophonus GroEL interacts with CLCuV and is localized in midgut and salivary gland of whitefly B. tabaci. PLoS One. 2012; 7: Article ID e42168
• [24]Su Q, Pan H, Liu B, Chu D, Xie W, Wu Q et al.. Insect symbiont facilitates vector acquisition, retention, and transmission of plant virus. Sci Rep. 2013; 3:1367.
• [25]Kliot A, Cilia M, Czosnek H, Ghanim M. Infection of the whitefly Bemisia tabaci with Rickettsia spp. alters its interactions with Tomato yellow leaf curl virus. J Virol. 2014; 88:5652-60.
• [26]Maruthi MN, Colvin J, Seal S. Mating compatibility, life‐history traits, and RAPD‐PCR variation in Bemisia tabaci associated with the cassava mosaic disease pandemic in East Africa. Entomol Exp Appl. 2001; 99:13-23.
• [27]Sseruwagi P, Maruthi MN, Colvin J, Rey MEC, Brown JK, Legg JP. Colonisation of non-cassava plant species by cassava whiteflies (Bemisia tabaci) (Gennadius) (Hemiptera:Aleyrodidae) in Uganda. Entomol Exp Appl. 2006; 119:145-53.
• [28]Berry SD, Fondong V, Rey C, Rogan D, Fauquet CM, Brown JK. Molecular evidence for five distinct Bemisia tabaci (Homoptera:Aleyrodidae) geographic haplotypes associated with cassava in sub-Saharan Africa. Ann Entomol Soc Am. 2004; 97:852-9.
• [29]Tajebe LS, Boni SB, Guastella D, Cavalieri V, Lund OS, Rugumamu CP, et al. Abundance, diversity and geographic distribution of cassava mosaic disease pandemic‐associated Bemisia tabaci in Tanzania. J Appl Entomol. 2014. (on-line version) doi:10.1111/jen.12197.
• [30]Bing X, Ruan Y, Rao Q, Wang X, Liu S. Diversity of secondary endosymbionts among different putative species of the whitefly Bemisia tabaci. Insect Sci. 2013; 20:194-206.
• [31]Singh ST, Priya NG, Kumar J, Rana VS, Ellango R, Joshi A et al.. Diversity and phylogenetic analysis of endosymbiotic bacteria from field caught Bemisia tabaci from different locations of North India based on 16S rDNA library screening. Infect Genet Evol. 2012; 12:411-9.
• [32]Tajebe LS, Guastella D, Cavalieri V, Kelly SE, Hunter MS, Lund OS, Legg JP, Rapisarda C. Diversity of symbiotic bacteria associated with Bemisia tabaci (Homoptera: Aleyrodidae) in cassava mosaic disease pandemic areas of Tanzania. Ann Appl Biol. 2014; 166:297-310.
• [33]Augustinos AA, Santos-Garcia D, Dionyssopoulou E, Moreira M, Papapanagiotou A, Scarvelakis M et al.. Detection and characterization of Wolbachia infections in natural populations of aphids: is the hidden diversity fully unravelled? PLoS One. 2011; 6: Article ID e28695
• [34]Bing XL, Xia WQ, Gui JD, Yan GH, Wang XW, Liu SS. Diversity and evolution of the Wolbachia endosymbionts of Bemisia (Hemiptera: Aleyrodidae) whiteflies. Ecol Evol. 2014; 4:2714-37.
• [35]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. BioMed Central Full Text
• [36]Chiel E, Gottlieb Y, Zchori-Fein E, Mozes Daube N, Katzir N, Inbar M et al.. Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. B Entomol Res. 2007; 97:407-13.
• [37]Gnankine O, Mouton L, Henri H, Terraz G, Houndete T, Martin T et al.. Distribution of Bemisia tabaci (Homoptera: Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa. Insect Conserv Divers. 2013; 2013(6):411-21.
• [38]Vautrin E, Vavre F. Interactions between vertically transmitted symbionts: coperation or conflict? Trends Microbiol. 2009; 17:95-9.
• [39]Chiel E, Inbar M, Mozes-Daube N, White JA, Hunter MS, Zchori-Fein E. Assessments of fitness effects by the facultative symbiont Rickettsia in the sweetpotato whitefly (Hemiptera: Aleyrodidae). Ann Entomol Soc Am. 2009; 102:413-8.
• [40]Gherna RL, Werren JH, Weisburg W, Cote R, Woese CR, Mandelco L et al.. NOTES: Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int J Syst Bacteriol. 1991; 41:563-5.
• [41]Walsh PS, Metzger DA, Higuchi R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques. 1991; 10:506-13.
• [42]Baldo L, Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR et al.. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Env Microb. 2006; 72:7098-110.
• [43]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28:2731-9.
• [44]Posada D. Selecting models of evolution. In: The phylogenetic handbook. A practical approach to DNA and protein phylogeny. Cambridge University Press, Cambridge; 2003: p.256-82.
• [45]R:a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2011.