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Applied and Environmental Microbiology, July 2002, p. 3190-3197, Vol. 68, No. 7
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.7.3190-3197.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Secondary ({gamma}-Proteobacteria) Endosymbionts Infect the Primary (ß-Proteobacteria) Endosymbionts of Mealybugs Multiple Times and Coevolve with Their Hosts

MyLo Ly Thao,1 Penny J. Gullan,2 and Paul Baumann1*

Microbiology Section, University of California, Davis, California 95616-8665,1 Department of Entomology, University of California, Davis, California 95616-85842

Received 15 February 2002/ Accepted 19 April 2002

Mealybugs (Hemiptera, Coccoidea, Pseudococcidae) are plant sap-sucking insects that have within their body cavities specialized cells containing prokaryotic primary endosymbionts (P-endosymbionts). The P-endosymbionts have the unusual property of containing within their cytoplasm prokaryotic secondary endosymbionts (S-endosymbionts) [C. D. von Dohlen, S. Kohler, S. T. Alsop, and W. R. McManus, Nature (London) 412:433-436, 2001]. Four-kilobase fragments containing 16S-23S ribosomal DNA (rDNA) were obtained from the P-endosymbionts of 22 mealybug species and the S-endosymbionts of 12 representative species. Phylogenetic analyses of the P-endosymbionts indicated that they have a monophyletic origin and are members of the ß-subdivision of the Proteobacteria; these organisms were subdivided into five different clusters. The S-endosymbionts were members of the {gamma}-subdivision of the Proteobacteria and were grouped into clusters similar to those observed with the P-endosymbionts. The S-endosymbiont clusters were distinct from each other and from other insect-associated bacteria. The similarity of the clusters formed by the P- and S-endosymbionts suggests that the P-endosymbionts of mealybugs were infected multiple times with different precursors of the S-endosymbionts and once the association was established, the P- and S-endosymbionts were transmitted together. The lineage consisting of the P-endosymbionts of mealybugs was given the designation "Candidatus Tremblaya" gen. nov., with a single species, "Candidatus Tremblaya princeps" sp. nov. The results of phylogenetic analyses of mitochondrial DNA fragments encoding cytochrome oxidase subunits I and II from four representative mealybug species were in agreement with the results of 16S-23S rDNA analyses, suggesting that relationships among strains of "Candidatus T. princeps" are useful in inferring the phylogeny of their mealybug hosts.

* Corresponding author. Mailing address: Microbiology Section, University of California, Davis, CA 95616-8665. Phone: (530) 752-0272. Fax: (530) 752-9014. E-mail: pabaumann{at}ucdavis.edu.

Applied and Environmental Microbiology, July 2002, p. 3190-3197, Vol. 68, No. 7
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.7.3190-3197.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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