Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae

Applied and Environmental Microbiology

Volumn 75, Issue 16, 2009, Pages 5328-5335

  Burke, Gaelen R ^a   Normark, Benjamin B ^b   Favret, Colin ^c   Moran, Nancy A ^a  

^a The University of Arizona   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c AphidNet LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOSYMBIOTIC BACTERIUM; ENVIRONMENTAL STRESS; HIGH INCIDENCE; PHYLOGENETIC ANALYSIS; SERRATIA;

CALCIUM;

APHID; CLADISTICS; EVOLUTIONARY BIOLOGY; MORPHOLOGY; SPECIES DIVERSITY; SUBSPECIES; SYMBIONT; TAXONOMY;

APHID; ARTICLE; BIOGEOGRAPHY; BUCHNERA; CANDIDATUS SERRATIA SYMBIOTICA; CLADISTICS; ENDOSYMBIONT; EVOLUTIONARY ADAPTATION; FUNCTIONAL ANATOMY; LACHNINAE; MORPHOLOGICAL TRAIT; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRITION; PHYLOGENY; SERRATIA; THERMOREGULATION;

ANIMALS; APHIDS; BUCHNERA; DNA, BACTERIAL; DNA, RIBOSOMAL; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOTYPE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SERRATIA; SYMBIOSIS;

APHIDIDAE; CANDIDATUS SERRATIA SYMBIOTICA; CINARA; LACHNIDAE; SERRATIA;

EID: 68549132520     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00717-09     Document Type: Article

References (41)

1. Blackman, R. L., and V. F. Eastop. 1994. Aphids on the world's trees: an identification and information guide. CAB International, Wallington, United Kingdom.
2. Chen, D.-Q., C. B. Montllor, and A. H. Purcell. 2000. Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol. Exp. Appl. 95:315-323.
3. Chen, D. Q., and A. H. Purcell. 1997. Occurrence and transmission of facultative endosymbionts in aphids. Curr. Microbiol. 34:220-225.
4. Degnan, P. H., and N. A. Moran. 2008. Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol. Ecol. 17:916-929.
5. Degnan, P. H., and N. A. Moran. 2008. Diverse phage-encoded toxins in a protective insect endosymbiont. Appl. Environ. Microbiol. 74:6782-6791.
6. Favret, C., and D. J. Voegtlin. 2004. Speciation by host-switching in pinyon Cinara (Insecta: Hemiptera: Aphididae). Mol. Phylogenet. Evol. 32:139-151.
7. Fukatsu, T., and H. Ishikawa. 1998. Differential immunohistochemical visualization of the primary and secondary intracellular symbiotic bacteria of aphids. Appl. Entomol. Zool. 33:321-326.
8. Gherna, R. L., J. H. Werren, W. Weisburg, R. Cote, C. R. Woese, L. Mandelco, and D. J. Brenner. 1991. Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int. J. Syst. Bacteriol. 41:563-565.
9. Gil, R., B. Sabater-Muñoz, A. Latorre, F. J. Silva, and A. Moya. 2002. Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc. Natl. Acad. Sci. USA 99:4454-4458.
10. Gomez-Valero, L., M. Soriano-Navarro, V. Pérez-Brocal, A. Heddi, A. Moya, J. M. García-Verdugo, and A. Latorre. 2004. Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the aphid Cinara cedri. J. Bacteriol. 186:6626-6633.
11. Grimont, P. A., and F. Grimont. 1978. The genus Serratia. Annu. Rev. Microbiol. 32:221-248.
12. Grimont, P. A. D., F. Grimont, and M. P. Starr. 1979. Serratia ficaria sp. nov., a bacterial species associated with Smyrna figs and the fig wasp Blastophaga psenes. Curr. Microbiol. 2:277-282.
13. Gruwell, M. E., G. E. Morse, and B. B. Normark. 2007. Phylogenetic congruence of armored scale insects (Hemiptera: Diaspididae) and their primary endosymbionts from the phylum Bacteroidetes. Mol. Phylogenet. Evol. 44:267-280.
14. Haynes, S., A. C. Darby, T. J. Daniell, G. Webster, F. J. Van Veen, H. C. Godfray, J. I. Prosser, and A. E. Douglas. 2003. Diversity of bacteria associated with natural aphid populations. Appl. Environ. Microbiol. 69:7216-7223.
15. Koga, R., T. Tsuchida, and T. Fukatsu. 2003. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. Biol. Sci. 270:2543-2550.
16. Koga, R., T. Tsuchida, M. Sakurai, and T. Fukatsu. 2007. Selective elimination of aphid endosymbionts: effects of antibiotic dose and host genotype, and fitness consequences. FEMS Microbiol. Ecol. 60:229-239.
17. Lamelas, A., V. Pérez-Brocal, L. Gómez-Valero, M. J. Gosalbes, A. Moya, and A. Latorre. 2008. Evolution of the secondary symbiont "Candidatus Serratia symbiotica" in aphid species of the subfamily Lachninae. Appl. Environ. Microbiol. 74:4236-4240.
18. Maddison, D. R., and W. P. Maddison. 2000. MacClade 4: analysis of phylogeny and character evolution, version 4.0. Sinauer Associates, Sunderland, MA.
19. Montllor, C., A. Maxmen, and A. H. Purcell. 2002. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum, under heat stress. Ecol. Entomol. 27:189-195.
20. Moran, N. A., J. A. Russell, R. Koga, and T. Fukatsu. 2005. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl. Environ. Microbiol. 71:3302-3310.
21. Munson, M. A., P. Baumann, M. A. Clark, L. Baumann, N. A. Moran, D. J. Voegtlin, and B. C. Campbell. 1991. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J. Bacteriol. 173:6321-6324.
22. Normark, B. B. 1999. Evolution in a putatively ancient asexual aphid lineage: recombination and rapid karyotype change. Evolution 53:1458-1569.
23. Normark, B. B. 2000. Molecular systematics and evolution of the aphid family Lachnidae. Mol. Phylogenet. Evol. 14:131-140.
24. Oliver, K. M., N. A. Moran, and M. S. Hunter. 2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl. Acad. Sci. USA 102:12795-12800.
25. Oliver, K. M., N. A. Moran, and M. S. Hunter. 2006. Costs and benefits of a superinfection of facultative symbionts in aphids. Proc. Biol. Sci. 22:1273-1280.
26. Pérez-Brocal, V., R. Gil, S. Ramos, A. Lamelas, M. Postigo, J. M. Michelena, F. J. Silva, A. Moya, and A. Latorre. 2006. A small microbial genome: the end of a long symbiotic relationship? Science 314:312-313.
27. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
28. Russell, J. A., A. Latorre, B. Sabater-Muñoz, A. Moya, and N. A. Moran. 2003. Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol. Ecol. 12:1061-1075.
29. Russell, J. A., and N. A. Moran. 2006. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc. Biol. Sci. 273:603-610.
30. Sandström, J. P., J. A. Russell, J. P. White, and N. A. Moran. 2001. Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol. Ecol. 10:217-228.
31. Scarborough, C. L., J. Ferrari, and H. C. Godfray. 2005. Aphid protected from pathogen by endosymbiont. Science 310:1781.
32. Shigenobu, S., H. Watanabe, M. Hattori, Y. Sakaki, and H. Ishikawa. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81-86.
33. Simon, J. C., S. Carre, M. Boutin, N. Prunier-Leterme, B. Sabater-Munoz, A. Latorre, and R. Bournoville. 2003. Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc. Biol. Sci. 270:1703-1712.
34. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
35. Stouthamer, R., J. A. J. Breeuwer, and G. D. D. Hurst. 1999. Wolbachia pipientis: microbial manipulation of arthropod reproduction. Annu. Rev. Microbiol. 53:72-102.
36. Stucki, G., T. A. Jackson, and M. J. Noonan. 1984. Isolation and characterization of Serratia strains pathogenic for larvae of the New Zealand grass grub, Costelytra zealandica. N. Z. J. Sci. 27:255-260.
37. Swofford, D. L. 2003. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, MA.
38. Takiya, D. M., P. L. Tran, C. H. Dietrich, and N. A. Moran. 2006. Cocladogenesis spanning three phyla: leafhoppers (Insecta: Hemiptera: Cicadellidae) and their dual bacterial symbionts. Mol. Ecol. 15:4175-4191.
39. Tsuchida, T., R. Koga, H. Shibao, T. Matsumoto, and T. Fukatsu. 2002. Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 11: 2123-2135.
40. Tsuchida, T., R. Koga, M. Sakurai, and T. Fukatsu. 2006. Facultative bacterial endosymbionts of three aphid species, Aphis craccivora, Megoura crassicauda and Acyrthosiphon pisum, sympatrically found on the same host plants. Appl. Environ. Zool. 41:129-137.
41. Unterman, B. M., P. Baumann, and D. L. McLean. 1989. Pea aphid symbiont relationships established by analysis of 16S rRNAs. J. Bacteriol. 171:2970-2974.