Strategies of genomic integration within insect-bacterial mutualisms

Biological Bulletin

Volumn 223, Issue 1, 2012, Pages 112-122

  Wernegreen, Jennifer J ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APHID; BACTERIUM; ENDOSYMBIONT; GENOMICS; HOST-SYMBIONT INTERACTION; MUTUALISM; PHYLOGENETICS;

ANIMALIA; APHIDIDAE; BACTERIA (MICROORGANISMS); HEXAPODA;

EID: 84866403135     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.1086/BBLv223n1p112     Document Type: Article

References (81)

1. Abbot, P., and N. A. Moran. 2002. Extremely low levels of genetic polymorphism in endosymbionts (Buchnera) of aphids (Pemphigus). Mol. Ecol. 11: 2649-2660.
2. Akman-Gündü z, E., and A. Douglas. 2009. Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proc. Biol. Sci. 276: 987-991.
3. Andersson, S. G., and C. G. Kurland. 1998. Reductive evolution of resident genomes. Trends Microbiol. 6: 263-268.
4. Baumann, P., N. Moran, and L. Baumann. 2000. Bacteriocyte-associated endosymbionts of insects. Pp. 403-438 in The Prokaryotes, A Handbook on the Biology of Bacteria; Ecophysiology, Isolation, Identification, Applications, M. Dworkin, ed. Springer-Verlag, New York.
5. Bonasio, R., G. Zhang, C. Ye, N. S. Mutti, X. Fang, N. Qin, G. Donahue, P. Yang, Q. Li, C. Li et al. 2010. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329: 1068-1071.
6. Buchner, P. 1965. Endosymbiosis of Animals with Plant Microorganisms. Interscience Publishers, New York.
7. Burke, G. R., and N. A. Moran. 2011. Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol. Evol. 3: 195-208.
8. Burke, G. R., B. B. Normark, C. Favret, and N. A. Moran. 2009. Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae. Appl. Environ. Microbiol. 75: 5328-5335.
9. Cracraft, J. 2004. A new AIBS for the age of biology Bioscience 54: 979.
10. Currie, C. R. 2001. A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu. Rev. Microbiol. 55: 357-380.
11. Degnan, P. H., Y. Yu, N. Sisneros, R. A. Wing, and N. A. Moran. 2009. Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc. Natl. Acad. Sci. USA 106: 9063-9068.
12. Degnan, P. H., T. E. Leonardo, B. N. Cass, B. Hurwitz, D. Stern, R. A. Gibbs, S. Richards, and N. A. Moran. 2010. Dynamics of genome evolution in facultative symbionts of aphids. Environ. Microbiol. 12: 2060-2069.
13. Douglas, A.E. 1989. Mycetocyte symbiosis in insects. Biol. Rev. Camb. Philos. Soc. 64: 409-434.
14. Douglas, A. E. 2011. Lessons from studying insect symbioses. Cell Host Microbe 10: 359-367.
15. Douglas, A. E., S. Bouvaine, and R. R. Russell. 2011. How the insect immune system interacts with an obligate symbiotic bacterium. Proc. Biol. Sci. 278: 333-338.
16. Dunning Hotopp, J. C. 2011. Horizontal gene transfer between bacteria and animals. Trends Genet. 27: 157-163.
17. Dunning Hotopp, J. C., M. E. Clark, D. C. Oliveira, J. M. Foster, P. Fischer, M. C. Munoz Torres, J. D. Giebel, N. Kumar, N. Ishmael, S. Wang et al. 2007. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317: 1753-1756.
18. Feldhaar, H. 2011. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol. Entomol. 36: 533-543.
19. Feldhaar, H., J. Straka, M. Krischke, K. Berthold, S. Stoll, M. J. Mueller, and R. Gross. 2007. Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol. 5: 48.
20. Fischman, B. J., S. H. Woodard, and G. E. Robinson. 2011. Molecular evolutionary analyses of insect societies. Proc. Natl. Acad. Sci. USA 108(Suppl. 2): 10847-10854.
21. Funk, D. J., J. J. Wernegreen, and N. A. Moran. 2001. Intraspecific variation in symbiont genomes: bottlenecks and the aphid-buchnera association. Genetics 157: 477-489.
22. Gadagkar, R. 2011. The birth of ant genomics. Proc. Natl. Acad. Sci. USA 108: 5477-5478.
23. Gadau, J., M. Helmkampf, S. Nygaard, J. Roux, D. F. Simola, C. R. Smith, G. Suen, Y. Wurm, and C. D. Smith. 2012. The genomic impact of 100 million years of social evolution in seven ant species. Trends Genet. 28: 14-21.
24. Gerardo, N. M., B. Altincicek, C. Anselme, H. Atamian, S. M. Barribeau, M. de Vos, E. J. Duncan, J. D. Evans, T. Gabaldon, M. Ghanim et al. 2010. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 11: R21.
25. Gil, R., F. J. Silva, E. Zientz, F. Delmotte, F. González-Candelas, A. Latorre, C. Rausell, J. Kamerbeek, J. Gadau, B. Hölldobler et al. 2003. The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc. Natl. Acad. Sci. USA 100: 9388-9393.
26. Gil, R., F. J. Silva, J. Pereto, and A. Moya. 2004. Determination of the core of a minimal bacterial gene set. Microbiol. Mol. Biol. Rev. 68: 518-537.
27. Gomez-Valero, L., M. Soriano-Navarro, V. Perez-Brocal, A. Heddi, A. Moya, J. M. Garcia-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.
28. Gosalbes, M. J., A. Lamelas, A. Moya, and A. Latorre. 2008. The striking case of tryptophan provision in the cedar aphid Cinara cedri. J. Bacteriol. 190: 6026-6029.
29. Gross, R., F. Vavre, A. Heddi, G. D. Hurst, E. Zchori-Fein, and K. Bourtzis. 2009. Immunity and symbiosis. Mol. Microbiol. 73: 751-759.
30. Hansen, A. K., and N. A. Moran. 2011. Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc. Natl. Acad. Sci. USA 108: 2849-2854.
31. He, H., Y. Chen, Y. Zhang, and C. Wei. 2011. Bacteria associated with gut lumen of Camponotus japonicus Mayr. Environ. Entomol. 40: 1405-1409.
32. Heddi, A., H. Charles, C. Khatchadourian, G. Bonnot, and P. Nardon. 1998. Molecular characterization of the principal symbiotic bacteria of the weevil Sitophilus oryzae: a peculiar GC content of an endocytobiotic DNA. J. Mol. Evol. 47: 52-61.
33. Hershberg, R., and D. A. Petrov. 2010. Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet. 6: e1001115.
34. Husnik, F., T. Chrudimsky, and V. Hypsa. 2011. Multiple origins of endosymbiosis within the Enterobacteriaceae (gamma-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biol. 9: 87.
35. Ishikawa, H. 1984. Alteration with age of symbiosis of gene expression in aphid endosymbionts. Biosystems 17: 127-134.
36. Keeling, P. J. 2011. Endosymbiosis: bacteria sharing the load. Curr. Biol. 21: R623-624.
37. Kerney, R., E. Kim, R. P. Hangarter, A. A. Heiss, C. D. Bishop, and B. K. Hall. 2011. Intracellular invasion of green algae in a salamander host. Proc. Natl. Acad. Sci. USA 108: 6497-6502.
38. Kirkness, E. F., B. J. Haas, W. Sun, H. R. Braig, M. A. Perotti, J. M. Clark, S. H. Lee, H. M. Robertson, R. C. Kennedy, E. Elhaik et al. 2010. Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc. Natl. Acad. Sci. USA 107: 12168-12173.
39. 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.
40. Lamelas, A., V. Perez-Brocal, L. Gomez-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.
41. Lamelas, A., M. J. Gosalbes, A. Manzano-Marin, J. Pereto, A. Moya, and A. Latorre. 2011. Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet. 7: e1002357.
42. Lefevre, C., H. Charles, A. Vallier, B. Delobel, B. Farrell, and A. Heddi. 2004. Endosymbiont phylogenesis in the dryophthoridae weevils: evidence for bacterial replacement. Mol. Biol. Evol. 21: 965-973.
43. Login, F. H., S. Balmand, A. Vallier, C. Vincent-Monegat, A. Vigneron, M. Weiss-Gayet, D. Rochat, and A. Heddi. 2011. Antimicrobial peptides keep insect endosymbionts under control. Science 334: 362-365.
44. McCutcheon, J. P., and N. A. Moran. 2007. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc. Natl. Acad. Sci. USA 104: 19392-19397.
45. McCutcheon, J. P., and N. A. Moran. 2010. Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol. Evol. 2: 708-718.
46. McCutcheon, J. P., and N. A. Moran. 2012. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10: 13-26.
47. McCutcheon, J. P., and C. D. von Dohlen. 2011. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr. Biol. 21: 1366-1372.
48. McCutcheon, J. P., B. R. McDonald, and N. A. Moran. 2009. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl. Acad. Sci. USA 106: 15394-15399.
49. Mendonca, A. G., R. J. Alves, and J. B. Pereira-Leal. 2011. Loss of genetic redundancy in reductive genome evolution. PLoS Comput. Biol. 7: e1001082.
50. Mira, A., and N. A. Moran. 2002. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44: 137-143.
51. Mira, A., H. Ochman, and N. A. Moran. 2001. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17: 589-596.
52. Mira, A., L. Klasson, and S. G. Andersson. 2002. Microbial genome evolution: sources of variability. Curr. Opin. Microbiol. 5: 506-512.
53. Moran, N. A. 1996. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93: 2873-2878.
54. Moran, N. A., and G. R. Plague. 2004. Genomic changes following host restriction in bacteria. Curr. Opin. Genet. Dev. 14: 627-633.
55. Moran, N. A., H. E. Dunbar, and J. L. Wilcox. 2005a. Regulation of transcription in a reduced bacterial genome: nutrient-provisioning genes of the obligate symbiont Buchnera aphidicola. J. Bacteriol. 187: 4229-4237.
56. Moran, N. A., J. A. Russell, R. Koga, and T. Fukatsu. 2005b. Evolutionary relationships of three new species of enterobacteriaceae living as symbionts of aphids and other insects. Appl. Environ. Microbiol. 71: 3302-3310.
57. Moran, N. A., J. P. McCutcheon, and A. Nakabachi. 2008. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42: 165-190.
58. Moya, A., J. Pereto, R. Gil, and A. Latorre. 2008. Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat. Rev. Genet. 9: 218-229.
59. Newton, I. L., and S. R. Bordenstein. 2011. Correlations between bacterial ecology and mobile DNA. Curr. Microbiol. 62: 198-208.
60. Nikoh, N., J. P. McCutcheon, T. Kudo, S. Y. Miyagishima, N. A. Moran, and A. Nakabachi. 2010. Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet. 6: e1000827.
61. Nygaard, S., G. Zhang, M. Schiott, C. Li, Y. Wurm, H. Hu, J. Zhou, L. Ji, F. Qiu, M. Rasmussen et al. 2011. The genome of the leafcutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome Res. 21: 1339-1348.
62. Oliver, K. M., P. H. Degnan, G. R. Burke, and N. A. Moran. 2010. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 55: 247-266.
63. Pal, C., B. Papp, M. J. Lercher, P. Csermely, S. G. Oliver, and L. D. Hurst. 2006. Chance and necessity in the evolution of minimal metabolic networks. Nature 440: 667-670.
64. Perez-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.
65. Poliakov, A., C. W. Russell, L. Ponnala, H. J. Hoops, Q. Sun, A. E. Douglas, and K. J. van Wijk. 2011. Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis. Mol. Cell. Proteomics 10: M110 007039.
66. Ratzka, C., C. Liang, T. Dandekar, R. Gross, and H. Feldhaar. 2011. Immune response of the ant Camponotus floridanus against pathogens and its obligate mutualistic endosymbiont. Insect Biochem. Mol. Biol. 41: 529-536.
67. Sabree, Z. L., S. Kambhampati, and N. A. Moran. 2009. Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc. Natl. Acad. Sci. USA 106: 19521-19526.
68. Shigenobu, S., and A. C. Wilson. 2011. Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont. Cell. Mol. Life Sci. 68: 1297-1309.
69. 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.
70. Sirvio, A., and P. Pamilo. 2010. Multiple endosymbionts in populations of the ant Formica cinerea. BMC Evol. Biol. 10: 335.
71. Smillie, C. S., M. B. Smith, J. Friedman, O. X. Cordero, L. A. David, and E. J. Alm. 2011. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480: 241-244.
72. Stoll, S., H. Feldhaar, and R. Gross. 2009. Transcriptional profiling of the endosymbiont Blochmannia floridanus during different developmental stages of its holometabolous ant host. Environ. Microbiol. 11: 877-888.
73. Suen, G., C. Teiling, L. Li, C. Holt, E. Abouheif, E. Bornberg-Bauer, P. Bouffard, E. J. Caldera, E. Cash, A. Cavanaugh et al. 2011. The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genet. 7: e1002007.
74. Tamas, I., L. Klasson, B. Canback, A. K. Naslund, A. S. Eriksson, J. J. Wernegreen, J. P. Sandstrom, N. A. Moran, and S. G. Andersson. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376-2379.
75. Toh, H., B. L. Weiss, S. A. Perkin, A. Yamashita, K. Oshima, M. Hattori, and S. Aksoy. 2006. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res. 16: 149-156.
76. Toju, H., T. Hosokawa, R. Koga, N. Nikoh, X. Y. Meng, N. Kimura, and T. Fukatsu. 2010. "Candidatus Curculioniphilus buchneri, " a novel clade of bacterial endocellular symbionts from weevils of the genus Curculio. Appl. Environ. Microbiol. 76: 275-282.
77. Van Ham, R. C., J. Kamerbeek, C. Palacios, C. Rausell, F. Abascal, U. Bastolla, J. M. Fernandez, L. Jimenez, M. Postigo, F. J. Silva et al. 2003. Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. USA 100: 581-586.
78. von Dohlen, C. D., S. Kohler, S. T. Alsop, and W. R. McManus. 2001. Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412: 433-436.
79. Wernegreen, J. J., S. N. Kauppinen, S. G. Brady, and P. S. Ward. 2009. One nutritional symbiosis begat another: phylogenetic evidence that the ant tribe Camponotini acquired Blochmannia by tending sap-feeding insects. BMC Evol. Biol. 9: 292.
80. Wilcox, J. L., H. E. Dunbar, R. D. Wolfinger, and N. A. Moran. 2003. Consequences of reductive evolution for gene expression in an obligate endosymbiont. Mol. Microbiol. 48: 1491-1500.
81. Williams, L. E., and J. J. Wernegreen. 2010. Unprecedented loss of ammonia assimilation capability in a urease-encoding bacterial mutualist. BMC Genomics 11: 287.