An interdependent metabolic patchwork in the nested symbiosis of mealybugs

Current Biology

Volumn 21, Issue 16, 2011, Pages 1366-1372

  McCutcheon, John P ^a,b   Von Dohlen, Carol D ^c  

^a University of Arizona   (United States)

^b UNIVERSITY OF MONTANA   (United States)

^c UTAH STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; BACTERIAL GENOME; BETAPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GENE EXPRESSION; GENETICS; HEMIPTERA; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; SYMBIOSIS;

ANIMALS; BETAPROTEOBACTERIA; GAMMAPROTEOBACTERIA; GENE EXPRESSION; GENOME, BACTERIAL; HEMIPTERA; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; SYMBIOSIS;

BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; CANDIDATUS TREMBLAYA; CANDIDATUS TREMBLAYA PRINCEPS; GAMMAPROTEOBACTERIA; HEMIPTERA; HEXAPODA; PLANOCOCCUS CITRI; PSEUDOCOCCIDAE;

EID: 80051978497     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2011.06.051     Document Type: Article

References (45)

1. J.P. McCutcheon, B.R. McDonald, and N.A. Moran Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont PLoS Genet. 5 2009 e1000565
2. A. Nakabachi, A. Yamashita, H. Toh, H. Ishikawa, H.E. Dunbar, N.A. Moran, and M. Hattori The 160-kilobase genome of the bacterial endosymbiont Carsonella Science 314 2006 267 (Pubitemid 44571965)
3. J.P. McCutcheon, and N.A. Moran Parallel genomic evolution and metabolic interdependence in an ancient symbiosis Proc. Natl. Acad. Sci. USA 104 2007 19392 19397
4. J.P. McCutcheon, and N.A. Moran Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution Genome Biol. Evol. 2 2010 708 718
5. V. Pérez-Brocal, R. Gil, S. Ramos, A. Lamelas, M. Postigo, J.M. Michelena, F.J. Silva, A. Moya, and A. Latorre A small microbial genome: The end of a long symbiotic relationship? Science 314 2006 312 313 (Pubitemid 44571978)
6. D. Wu, S.C. Daugherty, S.E. Van Aken, G.H. Pai, K.L. Watkins, H. Khouri, L.J. Tallon, J.M. Zaborsky, H.E. Dunbar, and P.L. Tran Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters PLoS Biol. 4 2006 e188
7. J.P. McCutcheon, B.R. McDonald, and N.A. Moran Convergent evolution of metabolic roles in bacterial co-symbionts of insects Proc. Natl. Acad. Sci. USA 106 2009 15394 15399
8. C.D. von Dohlen, S. Kohler, S.T. Alsop, and W.R. McManus Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts Nature 412 2001 433 436 (Pubitemid 32702705)
9. I. Tamas, L. Klasson, B. Canbäck, A.K. Näslund, A.S. Eriksson, J.J. Wernegreen, J.P. Sandström, N.A. Moran, and S.G. Andersson 50 million years of genomic stasis in endosymbiotic bacteria Science 296 2002 2376 2379 (Pubitemid 34734208)
10. P.H. Degnan, A.B. Lazarus, and J.J. Wernegreen Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects Genome Res. 15 2005 1023 1033 (Pubitemid 41126858)
11. L. Baumann, M.L. Thao, J.M. Hess, M.W. Johnson, and P. Baumann The genetic properties of the primary endosymbionts of mealybugs differ from those of other endosymbionts of plant sap-sucking insects Appl. Environ. Microbiol. 68 2002 3198 3205 (Pubitemid 34734012)
12. J.P. McCutcheon The bacterial essence of tiny symbiont genomes Curr. Opin. Microbiol. 13 2010 73 78
13. P. Shen, and H.V. Huang Homologous recombination in Escherichia coli: Dependence on substrate length and homology Genetics 112 1986 441 457
14. A.E. Douglas Mycetocyte symbiosis in insects Biol. Rev. Camb. Philos. Soc. 64 1989 409 434
15. N.A. Moran, G.R. Plague, J.P. Sandström, and J.L. Wilcox A genomic perspective on nutrient provisioning by bacterial symbionts of insects Proc. Natl. Acad. Sci. USA 100 Suppl 2 2003 14543 14548 (Pubitemid 37499279)
16. S. Shigenobu, H. Watanabe, M. Hattori, Y. Sakaki, and H. Ishikawa Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS Nature 407 2000 81 86
17. R.C. van Ham, J. Kamerbeek, C. Palacios, C. Rausell, F. Abascal, U. Bastolla, J.M. Fernández, L. Jiménez, M. Postigo, and F.J. Silva Reductive genome evolution in Buchnera aphidicola Proc. Natl. Acad. Sci. USA 100 2003 581 586 (Pubitemid 36126095)
18. P. Baumann Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects Annu. Rev. Microbiol. 59 2005 155 189 (Pubitemid 41507428)
19. O. Weinstock, C. Sella, D.M. Chipman, and Z. Barak Properties of subcloned subunits of bacterial acetohydroxy acid synthases J. Bacteriol. 174 1992 5560 5566
20. A.C. Wilson, P.D. Ashton, F. Calevro, H. Charles, S. Colella, G. Febvay, G. Jander, P.F. Kushlan, S.J. Macdonald, and J.F. Schwartz Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola Insect Mol. Biol. 19 Suppl 2 2010 249 258
21. A.K. Hansen, and N.A. Moran Aphid genome expression reveals host-symbiont cooperation in the production of amino acids Proc. Natl. Acad. Sci. USA 108 2011 2849 2854
22. A. Poliakov, C.W. Russell, L. Ponnala, H.J. Hoops, Q. Sun, A.E. Douglas, and K.J. van Wijk Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis Mol. Cell. Proteomics 10 2011 M110, 007039
23. N.B. Hardy, P.J. Gullan, and C.J. Hodgson A subfamily-level classification of mealybugs (Hemiptera: Pseudococcidae) based on integrated molecular and morphological data Syst. Entomol. 33 2008 51 71
24. S.H. Payne, and W.F. Loomis Retention and loss of amino acid biosynthetic pathways based on analysis of whole-genome sequences Eukaryot. Cell 5 2006 272 276 (Pubitemid 43262014)
25. J. Sandstrom, and J. Pettersson Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance J. Insect Physiol. 40 1994 947 955 (Pubitemid 2161542)
26. M.J. Gosalbes, A. Lamelas, A. Moya, and A. Latorre The striking case of tryptophan provision in the cedar aphid Cinara cedri J. Bacteriol. 190 2008 6026 6029
27. T. Woyke, H. Teeling, N.N. Ivanova, M. Huntemann, M. Richter, F.O. Gloeckner, D. Boffelli, I.J. Anderson, K.W. Barry, and H.J. Shapiro Symbiosis insights through metagenomic analysis of a microbial consortium Nature 443 2006 950 955 (Pubitemid 44646166)
28. Y. Inagaki, and W. Ford Doolittle Evolution of the eukaryotic translation termination system: Origins of release factors Mol. Biol. Evol. 17 2000 882 889 (Pubitemid 30346547)
29. J.N. Timmis, M.A. Ayliffe, C.Y. Huang, and W. Martin Endosymbiotic gene transfer: Organelle genomes forge eukaryotic chromosomes Nat. Rev. Genet. 5 2004 123 135 (Pubitemid 38160279)
30. N. Nikoh, J.P. McCutcheon, T. Kudo, S.Y. Miyagishima, N.A. Moran, and A. Nakabachi Bacterial genes in the aphid genome: Absence of functional gene transfer from Buchnera to its host PLoS Genet. 6 2010 e1000827
31. E.F. Kirkness, B.J. Haas, W. Sun, H.R. Braig, M.A. Perotti, J.M. Clark, S.H. Lee, H.M. Robertson, R.C. Kennedy, and E. Elhaik Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle Proc. Natl. Acad. Sci. USA 107 2010 12168 12173
32. F.J. Silva, A. Latorre, and A. Moya Why are the genomes of endosymbiotic bacteria so stable? Trends Genet. 19 2003 176 180 (Pubitemid 36398416)
33. S.R. Bordenstein, and W.S. Reznikoff Mobile DNA in obligate intracellular bacteria Nat. Rev. Microbiol. 3 2005 688 699 (Pubitemid 41199586)
34. I.L.G. Newton, and S.R. Bordenstein Correlations between bacterial ecology and mobile DNA Curr. Microbiol. 62 2011 198 208
35. S.G. Andersson, and C.G. Kurland Reductive evolution of resident genomes Trends Microbiol. 6 1998 263 268 (Pubitemid 28343306)
36. N.A. Moran, and J.J. Wernegreen Lifestyle evolution in symbiotic bacteria: Insights from genomics Trends Ecol. Evol. (Amst.) 15 2000 321 326 (Pubitemid 30484256)
37. P. Buchner Endosymbiosis of Animals with Plant Microorganisms 1965 Interscience New York
38. M. Kono, R. Koga, M. Shimada, and T. Fukatsu Infection dynamics of coexisting beta- and gammaproteobacteria in the nested endosymbiotic system of mealybugs Appl. Environ. Microbiol. 74 2008 4175 4184 (Pubitemid 351962443)
39. J. Tamames, R. Gil, A. Latorre, J. Peretó, F.J. Silva, and A. Moya The frontier between cell and organelle: Genome analysis of Candidatus Carsonella ruddii BMC Evol. Biol. 7 2007 181
40. N. Kondo, N. Nikoh, N. Ijichi, M. Shimada, and T. Fukatsu Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect Proc. Natl. Acad. Sci. USA 99 2002 14280 14285 (Pubitemid 35257663)
41. J.C. Dunning Hotopp, M.E. Clark, D.C. Oliveira, J.M. Foster, P. Fischer, M.C. Muñoz Torres, J.D. Giebel, N. Kumar, N. Ishmael, and S. Wang Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes Science 317 2007 1753 1756 (Pubitemid 47461840)
42. H. Ochman, and L.M. Davalos The nature and dynamics of bacterial genomes Science 311 2006 1730 1733
43. J.O. Andersson, and S.G. Andersson Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes Mol. Biol. Evol. 18 2001 829 839 (Pubitemid 32372952)
44. A. Mira, H. Ochman, and N.A. Moran Deletional bias and the evolution of bacterial genomes Trends Genet. 17 2001 589 596 (Pubitemid 32918301)
45. M.L. Thao, P.J. Gullan, and P. Baumann Secondary (gamma-proteobacteria) endosymbionts infect the primary (beta-proteobacteria) endosymbionts of mealybugs multiple times and coevolve with their hosts Appl. Environ. Microbiol. 68 2002 3190 3197 (Pubitemid 34734011)