Comparative Genomics of Insect-Symbiotic Bacteria: Influence of Host Environment on Microbial Genome Composition

Applied and Environmental Microbiology

Volumn 69, Issue 11, 2003, Pages 6825-6832

  Rio, Rita V M ^a   Lefevre, Cedric ^b   Heddi, Abdelaziz ^b   Aksoy, Serap ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UA INRA 203   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; ECOLOGY; ESCHERICHIA COLI; FATTY ACIDS; GENES; METABOLISM;

PARASITES;

BACTERIOLOGY;

ARTICLE; BACTERIUM; CLADISTICS; COLEOPTERA; ENDOSYMBIONT; ENERGY METABOLISM; ESCHERICHIA COLI; FATTY ACID METABOLISM; FATTY ACID TRANSPORT; GENOME; GENOMICS; INSECT; MICROBIAL GENETICS; NONHUMAN; SITOPHILUS ORYZAE; SITOPHILUS ORYZAE PRIMARY ENDOSYMBIONT; SODALIS GLOSSINIDIUS; STATISTICAL SIGNIFICANCE; SYMBIOSIS; TSETSE FLY;

ANIMALS; BACTERIAL PROTEINS; BEETLES; DNA, BACTERIAL; ECOSYSTEM; ESCHERICHIA COLI; GAMMAPROTEOBACTERIA; GENOME, BACTERIAL; GENOMICS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SYMBIOSIS; TSETSE FLIES;

BACTERIA (MICROORGANISMS); COLEOPTERA; DIPTERA; ESCHERICHIA COLI; GLOSSINA (PROPER); INSECTA; PROKARYOTA; SITOPHILUS ORYZAE; SODALIS; SODALIS GLOSSINIDIUS;

EID: 0242657423     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.69.11.6825-6832.2003     Document Type: Article

References (53)

1. Akman, L., and S. Aksoy. 2001. Escherichia coli gene array analysis provides insight into the biology of the obligate endosymbiont of tsetse flies, Wigglesworthia glossinidia. Proc. Natl. Acad. Sci. USA 98:7546-7551.
2. Akman, L., R. Rio, C. B. Beard, and S. Aksoy. 2001. Genome size determination and coding capacity of Sodalis glossinidius, an enteric symbiont of tsetse flies, as revealed by hybridization to Escherichia coli gene arrays. J. Bacteriol. 183:4517-4525.
3. Akman, L., A. Yamashita, H. Watanabe, K. Oshima, T. Shiba, M. Hattori, and S. Aksoy. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402-407.
4. Aksoy, S., X. Chen, and V. Hyspa. 1997. Phylogeny and potential transmission routes of midgut-associated endosymbionts of tsetse (Diptera: Glossinidae). Insect Mol. Biol. 6:183-190.
5. Andersson, J. O., and S. G. E. Andersson. 2001. Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes. Mol. Biol. Evol. 18:829-839.
6. Andersson, S. G. E., and C. G. Kurland. 1998. Reductive evolution of resident genomes. Trends Microbiol. 6:263-268.
7. Andersson, S. G. E., A. Zomorodipour, J. O. Andersson, T. Sicheritz-Ponten, U. C. M. Alsmark, R. M. Podowski, A. K. Naslund, A. Eriksson, H. H. Winkler, and C. G. Kurland. 1998. The genome sequence of Rickettsia prowazekii and the origin of the mitochondria. Nature 96:133-140.
8. Blattner, F. R., G. Plunkett, C. A. Bloch III, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
9. Braig, H. R., W. Zhou, S. L. Dobson, and S. L. O'Neill. 1998. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J. Bacteriol. 180:2373-2378.
10. Buchner, P. 1965. Endosymbiosis of animals with plant microorganisms. Interscience, New York, N.Y.
11. Charles, H., G. Condemine, C. Nardon, and P. Nardon. 1997. Genome size characterization of the principal endocellular symbiotic bacteria of the weevil Sitophilus oryzae, using pulsed field gel electrophoresis. Insect Biochem. Mol. Biol. 27:345-350.
12. Chen, D. Q., and A. H. Purcell. 1997. Occurrence and transmission of facultative endosymbionts in aphids. Curr. Microbiol. 34:220-225.
13. 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. Applic. 95:315-323.
14. Cheng, Q., and S. Aksoy. 1999. Tissue tropism, transmission, and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol. Biol. 8:125-132.
15. Dale, C., S. A. Young, D. T. Haydon, and S. C. Welburn. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. USA 98:1883-1888.
16. Dale, C., G. R. Plague, B. Wang, H. Ochman, and N. A. Moran. 2002. Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc. Natl. Acad. Sci. USA 99:12397-12402.
17. Fukatsu, T., and N. Nikoh. 1998. Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl. Environ. Microbiol. 64:3599-3606.
18. Fukatsu, T., N. Nikoh, R. Kawai, and R. Koga. 2000. The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta, Homoptera). Appl. Environ. Microbiol. 66:2748-2758.
19. Gasnier-Fauchet, F., A. Gharib, and P. Nardon. 1986. Comparison of methionine metabolism in symbiotic and aposymbiotic larvae of Sitophilus oryzae L. (Coleoptera: Curculionidae). I. Evidence for a glycine N-methyl-transferase like activity in the aposymbiotic larvae. Comp. Biochem. Physiol. 85B:245-250.
20. Goebel, W., and R. Gross. 2001. Intracellular survival strategies of mutualistic and parasitic prokaryotes. Trends Microbiol. 9:267-273.
21. Grenier, A. M., C. Nardon, and P. Nardon. 1994. The role of symbionts in flight activity of Sitophilus weevils. Entomol. Exp. Applic. 70:201-208.
22. Heddi, A., F. Lefebvre, and P. Nardon. 1991. The influence of symbiosis on the respiratory control ratio (RCR) and the ADP/O ratio in the adult weevil Sitophilus oryzae (Coleoptera: Curculionidae). Endocyt. Cell Res. 8:61-73.
23. Heddi, A., F. Lefebvre, and P. Nardon. 1993. Effect of endocytobiotic bacteria on mitochondrial enzymatic activities in the weevil Sitophilus oryzae (Coleoptera: Curculionidae). Insect Biochem. Mol. Biol. 23:403-411.
24. Heddi, A., C. Hubert, C. Khatchadourian, G. Bonnot, and P. Nardon. 1998. Molecular characterization of the principal symbiotic bacteria of the weevil Sitophilus oryzae: a peculiar G+C content of an endocytobiotic DNA. J. Mol. Evol. 47:52-61.
25. Heddi, A., A. M. Grenier, C. Khatchadourian, H. Charles, and P. Nardon. 1999. Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc. Natl. Acad. Sci. USA 96:6814-6819.
26. Heddi, A. 2003. Endosymbiosis in the weevil of the genus Sitophilus: genetic, physiological, and molecular interactions among associated genomes, p. 67-82. In K. Bourtzis and T. Miller (ed.), Insect symbiosis. CRC Press, Boca Raton, Fla.
27. Hentschel, U., and M. Steinert. 2001. Symbiosis and pathogenesis: common themes, different outcomes. Trends Microbiol. 9:585.
28. Hooper, L. V., and J. I. Gordon. 2001. Commensal host-bacterial relationships in the gut. Science 292:1115-1118.
29. Koonin, E. V. 2000. How many genes can make a cell: the minimal-gene set concept. Annu. Rev. Genomics Hum. Genet. 1:99-116.
30. Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. Wolfinger. 1996. SAS system for mixed models. SAS Institute, Inc., Cary, N.C.
31. Ma, W. C., and D. L. Denlinger. 1974. Secretory discharge and microflora of milk gland in tsetse flies. Nature 247:301-303.
32. 14C glucose during pregnancy. J. Insect Physiol. 22:195-200.
33. Moloo, S. K. 1976. Aspects of the nutrition of adult female Glossina morsitans during pregnancy. J. Insect Physiol. 22:563-567.
34. Montllor, C. B., A. Maxmen, and A. H. Purcell. 2002. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum, under heat stress. Ecol. Entomol. 27:189-195.
35. Moran, N. A. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583-586.
36. Moran, N. A., and A. Mira. 14 November 2001, posting date. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biology 2:0054.1-0054.12. [Online.] http://genomebiology.com/2001/2/12/research/0054.1.
37. Moran, N. A., C. Dale, H. Dunbar, W. A. Smith, and H. Ochman. 2003. Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ. Microbiol. 5:116-126.
38. Munson, M. A., P. Baumann, M. A. Clark, L. Baumann, and N. A. Moran. 1991. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J. Bacteriol. 173:6321-6324.
39. Nardon, P. 1973. Obtention d'une souche aposymbiotique chez le charancon Sitophilus sasakii Tak: differentes methods et comparaison avec la souche symbiotique d'origine. C. R. Acad. Sci. 277D:981-984.
40. Nogge, G. 1981. Significance of symbionts for the maintenance of an optional nutritional state for successful reproduction in hematophagous arthropods. Parasitology 82:101-104.
41. Oliver, K. M., J. A. Russell, N. A. Moran, and M. S. Hunter. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl. Acad. Sci. USA 100:1803-1807.
42. O'Neill, S. L., R. H. Gooding, and S. Aksoy. 1993. Phylogenetically distant symbiotic microorganisms reside in Glossina midgut and ovary tissues. Med. Vet. Entomol. 7:377-383.
43. Sandstrom, 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.
44. 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.
45. Silva, F. J., A. Latorre, and A. Moya. 2001. Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet. 17:615-618.
46. Steinert, M., U. Hentschel, and J. Hacker. 2000. Symbiosis and pathogenesis: evolution of the microbe-host interaction. Naturwissenschaften 87:1-11.
47. Tamas, I., L. Klasson, B. Canback, A. K. Naslund, A. Eriksson, J. J. Wernegreen, J. P. Sandstrom, N. A. Moran, and S. G. E. Andersson. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376-2379.
48. 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. Mot. Ecol. 11:2123-2135.
49. van Ham, R. C. H. J., J. Kamerbeek, C. Palacios, C. Rausell, F. Abascal, U. Bastolla, J. M. Fernandez, L. Jimenez, M. Postigo, F. J. Silva, J. Tamames, E. Viguera, A. Latorre, A. Valencia, F. Moran, and A. Moya. 2003. Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. USA 100:581-586.
50. Welburn, S. C., I. Maudlin, and D. S. Ellis. 1987. In vitro cultivation of rickettsia-like organisms from Glossina spp. Ann. Trop. Med. Parasitol. 81:331-335.
51. Welburn, S. C., K. Arnold, I. Maudlin, and G. W. Goday. 1993. Rickettsia-like organisms and chitinase production in relation to transmission of trypanosomes by tsetse flies. Parasitology 107:141-145.
52. Wernegreen, J. J., P. H. Degnan, A. B. Lazarus, C. Palacios, and S. R. Bordenstein. 2003. Genome evolution in an insect cell: distinct features of an ant-bacterial partnership. Biol. Bull. 204:221-231.
53. Ziegler, R. 1996. Energy metabolism, p. 356-370. In B. J. Beaty and W. C. Marquardt (ed.), The biology of disease vectors. University Press of Colorado, Niwot, Colo.