Chapter 8 : Genomic Signatures of Intracellularity: Evolutionary Patterns and Paces in Bacterial Mutualists and Parasites

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Genomic Signatures of Intracellularity: Evolutionary Patterns and Paces in Bacterial Mutualists and Parasites, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815530/9781555814519_Chap08-1.gif /docserver/preview/fulltext/10.1128/9781555815530/9781555814519_Chap08-2.gif


This chapter highlights some intriguing patterns of genome change identified from genome-sequencing projects and molecular evolution studies. Trends include striking similarities between intracellular mutualists and parasites that may reflect common pressures of an intracellular lifestyle, as well as key differences that highlight distinct genomic consequences of their host associations. Bacteria form a variety of associations with host cells. At one end of the spectrum, the replication and spread of intracellular parasites impose a fitness cost to hosts. At the other end of the symbiotic spectrum, certain intracellular bacterial groups form exclusively mutualistic associations with hosts. Analysis of partial genome regions indicates that, compared with its relatives, the exceptionally small genome of associated with the aphid shows more extensive loss of metabolic than informational functions. Consistent with their infectious lifestyles, obligately intracellular parasites typically encode numerous mechanisms to invade host tissue and cells and to escape the host immune system. To date, genome-wide rate comparisons strongly suggest a consistent, genome-wide rate increase in intracellular species, as expected under the influences of increased mutation and/or genetic drift. The availability of two or more genomes for a particular group offers a window into the evolution of genome architecture, or changes in the order and strand orientation of shared loci. The rapid growth of genomics has elucidated processes that shape wide variation in genome size, gene content, patterns of DNA sequence evolution, and levels of genome fluidity in the bacterial world.

Citation: Jennifer J. 2007. Genomic Signatures of Intracellularity: Evolutionary Patterns and Paces in Bacterial Mutualists and Parasites, p 196-212. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch8

Key Concept Ranking

Rocky Mountain Spotted Fever
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Schematic representation of associates that bacteria form with hosts, nested by increasing intimacy of the association. Symbiotic bacteria, the broadest category, associate with hosts for some or all of the bacterium’s life cycle. Of these symbionts, some are endosymbiotic and can live within the tissues or cells. Endosymbionts that replicate within host cells are termed intracellular. Of these intracellular associates, certain highly specialized lineages have lost the ability to replicate outside of host cells and are obligately intracellular. The final category is the focus of this chapter.

Citation: Jennifer J. 2007. Genomic Signatures of Intracellularity: Evolutionary Patterns and Paces in Bacterial Mutualists and Parasites, p 196-212. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Genome size and %GC content of bacterial chromosome sequences, illustrating the small size and AT richness of obligate intracellular associates (labeled triangles). Chart is similar to published figures (e.g., reference ) and includes genomes that were publicly available as of July 2005, with the exception of multiple, closely related strains. Gray x, species possessed two or more chromosomes (mark reflects values for single chromosome). Reprinted with permission from reference . © (2005) Elsevier Science.

Citation: Jennifer J. 2007. Genomic Signatures of Intracellularity: Evolutionary Patterns and Paces in Bacterial Mutualists and Parasites, p 196-212. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Percentage of genes encoding particular biosynthetic functions. axis indicates proportion of ORFs involved in biosynthesis of (i) amino acids, (ii) cofactors, prosthetic groups, and carriers, and (iii) purines, pyrimidines, nucleotides and nucleosides. Boldface, obligately intracellular mutualists; underline, obligately intra-cellular pathogen. , and retain a free-living phase and were included for comparisons. Values for and the gamma- nutritional mutualists were based on reanalysis of genome sequences ( ). Data for other species were downloaded from the Comprehensive Microbial Resource at TIGR for a more consistent comparison across genomes ( ). However, as a result of differences in annotation and functional categorization, these counts may differ from original genome papers. Readers interested in particular taxa are encouraged to refer to original genome publications. In the rare cases where TIGR counted two largely overlapping, putative ORFs as two separate genes, these were counted as a single ORF for the purposes of this figure. Reprinted with permission from ( ). © (2005) Elsevier Science.

Citation: Jennifer J. 2007. Genomic Signatures of Intracellularity: Evolutionary Patterns and Paces in Bacterial Mutualists and Parasites, p 196-212. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch8
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Abbot, P., and, N. A. Moran. 2002. Extremely low levels of genetic polymorphism in endosymbionts (Buchnera) of aphids (Pemphigus). Mol. Ecol. 11:26492660.
2. 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. 32:402407.
3. Aksoy, S., and, R. V. Rio. 2005. Interactions among multiple genomes: tsetse, its symbionts and trypanosomes. Insect Biochem. Mol. Biol. 35:691698.
4. Andersson, J. O., and, S. G. Andersson. 1999. Genome degradation is an ongoing process in Rickettsia. Mol. Biol. Evol. 16:11781191.
5. Andersson, J. O., and, S. G. Andersson. 2001. Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes. Mol. Biol. Evol. 18:829839.
6. Andersson, S. G., and, C. G. Kurland. 1998. Reductive evolution of resident genomes. Trends Microbiol. 6:263268.
7. Batut, J.,, S. G. Andersson, and, D. O’ Callaghan. 2004. The evolution of chronic infection strategies in the alpha-Proteobacteria. Nat. Rev. Micro-biol. 2:933945.
8. Baumann, P.,, N. Moran, and, L. Baumann. 2000. Bacteriocyte-associated endosymbionts of insects. In M. Dworkin (ed.), The Prokaryotes: A Handbook on the Biology of Bacteria; Ecophysiology, Isolation, Identification, Applications. Springer-Verlag, New York, NY.
9. Belda, E.,, A. Moya, and, F. J. Silva. 2005. Genome rearrangement distances and gene order phylogeny in gamma-Proteobacteria. Mol. Biol. Evol. 22:14561467.
10. Bencina, D.,, B. Slavec, and, M. Narat. 2005. Antibody response to GroEL varies in patients with acute Mycoplasma pneumoniae infection. FEMS Immunol. Med. Microbiol. 43:399406.
11. Bordenstein, S. R., and, W. S. Reznikoff. 2005. Mobile DNA in obligate intracellular bacteria. Nat. Rev. Microbiol. 3:688699.
12. Brynnel, E. U.,, C. G. Kurland,, N. A. Moran, and, S. G. Andersson. 1998. Evolutionary rates for tuf genes in endosymbionts of aphids. Mol. Biol. Evol. 15:574582.
13. Buchner, P. 1965. Endosymbiosis of Animals with Plant Microorganisms. Interscience Publishers, New York, NY.
14. Burne, R. A., and, Y. Y. Chen. 2000. Bacterial ureases in infectious diseases. Microbes Infect. 2:533542.
15. Canback, B.,, I. Tamas, and, S. G. Andersson. 2004. A phylogenomic study of endosymbiotic bacteria. Mol. Biol. Evol. 21:11101122.
16. Chen, X.,, S. Li, and, S. Aksoy. 1999. Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J. Mol. Evol. 48:4958.
17. Clark, M. A.,, N. A. Moran, and, P. Baumann. 1999. Sequence evolution in bacterial endosymbionts having extreme base compositions. Mol. Biol. Evol. 16:15861598.
18. Cole, S. T.,, K. Eiglmeier,, J. Parkhill,, K. D. James,, N. R. Thomson,, P. R. Wheeler,, N. Honore,, T. Garnier,, C. Churcher,, D. Harris,, K. Mungall,, D. Basham,, D. Brown,, T. Chill-ingworth,, R. Connor,, R. M. Davies,, K. Devlin,, S. Duthoy,, T. Feltwell,, A. Fraser,, N. Hamlin,, S. Holroyd,, T. Hornsby,, K. Jagels,, C. Lacroix,, J. Maclean,, S. Moule,, L. Murphy,, K. Oliver,, M. A. Quail,, M. A. Rajandream,, K. M. Rutherford,, S. Rutter,, K. Seeger,, S. Simon,, M. Simmonds,, J. Skelton,, R. Squares,, S. Squares,, K. Stevens,, K. Taylor,, S. Whitehead,, J. R. Woodward, and, B. G. Barrell. 2001. Massive gene decay in the leprosy bacillus. Nature 409:10071011.
19. Collins, N. E.,, J. Liebenberg,, E. P. de Villiers,, K. A. Brayton,, E. Louw,, A. Pretorius,, F. E. Faber,, H. van Heerden,, A. Josemans,, M. van Kleef,, H. C. Steyn,, M. F. van Strijp,, E. Zwey-garth,, F. Jongejan,, J. C. Maillard,, D. Berthier,, M. Botha,, F. Joubert,, C. H. Corton,, N. R. Thomson,, M. T. Allsopp, and, B. A. Allsopp. 2005. The genome of the heartwater agent Ehrlichia ruminantium contains multiple tandem repeats of actively variable copy number. Proc. Natl. Acad. Sci. USA 102:838843.
20. Corsaro, D., and, D. Venditti. 2004. Emerging chlamydial infections. Crit. Rev. Microbiol. 30:75106.
21. 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: 1239712402.
22. Dale, C.,, B. Wang,, N. Moran, and, H. Ochman. 2003. Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration. Mol. Biol. Evol. 20:11881194.
23. Degnan, P.,, A. Lazarus,, C. Brock, and, J. Wernegreen. 2004. Host-symbiont stability and fast evolutionary rates in an ant-bacterium association: cospeciation of Camponotus species and their endosymbionts, Candidatus Blochmannia. Syst. Biol. 53:95110.
24. Degnan, P. H.,, A. B. Lazarus, and, J. J. Werne-green. 2005. Genome sequence of Blochmannia pennsylvanicus indicates parallel evolutionary trends among bacterial mutualists of insects. Genome Res. 15:10231033.
25. Duron, O.,, J. Lagnel,, M. Raymond,, K. Bourtzis,, P. Fort, and, M. Weill. 2005. Transposable element polymorphism of Wolbachia in the mosquito Culex pipiens: evidence of genetic diversity, superinfection and recombination. Mol. Ecol. 14:15611573.
26. Everett, K.,, M Thao,, M. Horn,, G. Dyszynski, and, P. Baumann. 2005. Novel Chlamydiae in whiteflies and scale insects: endosymbionts “Candidatus Fritschea bemisiae” strain Falk and “Candidatus Fritschea eriococci” strain Elm. Int. J. Syst. Evol. Microbiol. 55:15811587.
27. Fares, M. A.,, A. Moya, and, E. Barrio. 2004. GroEL and the maintenance of bacterial endosymbiosis. Trends Genet. 20:413416.
28. Foster, J.,, M. Ganatra,, I. Kamal,, J. Ware,, K. Makarova,, N. Ivanova,, A. Bhattacharyya,, V. Kapatral,, S. Kumar,, J. Posfai,, T. Vincze,, J. Ingram,, L. Moran,, A. Lapidus,, M. Omelchenko,, N. Kyrpides,, E. Ghedin,, S. Wang,, E. Goltsman,, V. Joukov,, O. Ostrov-skaya,, K. Tsukerman,, M. Mazur,, D. Comb,, E. Koonin, and, B. Slatko. 2005. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 3:e121.
29. Frank, A. C.,, C. M. Alsmark,, M. Thollesson, and, S. G. Andersson. 2005. Functional divergence and horizontal transfer of type IV secretion systems. Mol. Biol. Evol. 22:13251336.
30. Frank, A. C.,, H. Amiri, and, S. G. Andersson. 2002. Genome deterioration: loss of repeated sequences and accumulation of junk DNA. Genetica 115:112.
31. Fredriksson, A.,, M. Ballesteros,, S. Dukan, and, T. Nystrom. 2005. Defense against protein carbonylation by DnaK/DnaJ and proteases of the heat shock regulon. J. Bacteriol. 187:42074213.
32. 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. 66:27482758.
33. Funk, D. J.,, J. J. Wernegreen, and, N. A. Moran. 2001. Intraspecific variation in symbiont genomes: bottlenecks and the aphid-Buchnera association. Genetics 157:477489.
34. Ghedin, E.,, S. Wang,, J. M. Foster, and, B. E. Slatko. 2004. First sequenced genome of a parasitic nematode. Trends Parasitol. 20:151153.
35. Gil, R.,, A. Latorre, and, A. Moya. 2004. Bacterial endosymbionts of insects: insights from comparative genomics. Environ. Microbiol. 6:11091122.
36. Gil, R.,, F. J. Silva,, E. Zientz,, F. Delmotte,, F. Gonzalez-Candelas,, A. Latorre,, C. Rausell,, J. Kamerbeek,, J. Gadau,, B. Holldobler,, R. C. van Ham,, R. Gross, and, A. Moya. 2003. The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc. Natl. Acad. Sci. USA 100:93889393.
37. Goebel, W., and, R. Gross. 2001. Intracellular survival strategies of mutualistic and parasitic prokaryotes. Trends Microbiol. 9:267273.
38. Gomez-Valero, L.,, A. Latorre, and, F. J. Silva. 2004. The evolutionary fate of nonfunctional DNA in the bacterial endosymbiont Buchnera aphidicola. Mol. Biol. Evol. 21:21722181.
39. Greub, G.,, F. Collyn,, L. Guy, and, C. A. Roten. 2004. A genomic island present along the bacterial chromosome of the Parachlamydiaceae UWE25, an obligate amoebal endosymbiont, encodes a potentially functional F-like conjugative DNA transfer system. BMC Microbiol. 4:48.
40. Hacker, J.,, U. Hentschel, and, U. Dobrindt. 2003. Prokaryotic chromosomes and disease. Science 301:790793.
41. Hechard, C.,, O. Grepinet, and, A. Rodolakis. 2004. Molecular cloning of the Chlamydophila abortus groEL gene and evaluation of its protective efficacy in a murine model by genetic vaccination. J. Med. Microbiol. 53:861868.
42. Herbeck, J. T.,, D. J. Funk,, P. H. Degnan, and, J. J. Wernegreen. 2003. A conservative test of genetic drift in the endosymbiotic bacterium Buchnera: slightly deleterious mutations in the chaperonin groEL. Genetics 165:16511660.
43. Hoerauf, A.,, K. Nissen-Pahle,, C. Schmetz,, K. Henkle-Duhrsen,, M. L. Blaxter,, D. W. Buttner,, M. Y. Gallin,, K. M. Al-Qaoud,, R. Lucius, and, B. Fleischer. 1999. Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J. Clin. Invest. 103:1118.
44. Horn, M.,, A. Collingro,, S. Schmitz-Esser,, C. L. Beier,, U. Purkhold,, B. Fartmann,, P. Brandt,, G. J. Nyakatura,, M. Droege,, D. Frishman,, T. Rattei,, H. W. Mewes, and, M. Wagner. 2004. Illuminating the evolutionary history of Chlamydiae. Science 304:728730.
45. Itoh, T.,, W. Martin, and, M. Nei. 2002. Acceleration of genomic evolution caused by enhanced mutation rate in endocellular symbionts. Proc. Natl. Acad. Sci. USA 99:1294412948.
46. Klasson, L., and, S. G. Andersson. 2004. Evolution of minimal-gene-sets in host-dependent bacteria. Trends Microbiol. 12:3743.
47. Lai, C. Y.,, P. Baumann, and, N. Moran. 1996. The endosymbiont (Buchnera sp.) of the aphid Diuraphis noxia contains plasmids consisting of trpEG and tandem repeats of trpEG pseudogenes. Appl. Environ. Microbiol. 62:332339.
48. Lee, I. M.,, Y. Zhao, and, K. D. Bottner. 2005. Novel insertion sequence–like elements in Phyto-plasma strains of the aster yellows group are putative new members of the IS3 family. FEMS Micro-biol. Lett. 242:353360.
49. Margulis, L. 1975. Symbiotic theory of the origin of eukaryotic organelles; criteria for proof. Symp. Soc. Exp. Biol. 1975(2a):2138.
50. Matthew, C. Z.,, A. C. Darby,, S. A. Young,, L. H. Hume, and, S. C. Welburn. 2005. The rapid isolation and growth dynamics of the tsetse symbiont Sodalis glossinidius. FEMS Microbiol. Lett. 248:6974.
51. McLeod, M. P.,, X. Qin,, S. E. Karpathy,, J. Gioia,, S. K. Highlander,, G. E. Fox,, T. Z. McNeill,, H. Jiang,, D. Muzny,, L. S. Jacob,, A. C. Hawes,, E. Sodergren,, R. Gill,, J. Hume,, M. Morgan,, G. Fan,, A. G. Amin,, R. A. Gibbs,, C. Hong,, X. J. Yu,, D. H. Walker, and, G. M. Weinstock. 2004. Complete genome sequence of Rickettsia typhi and comparison with sequences of other rickettsiae. J. Bacteriol. 186:58425855.
52. Mira, A.,, L. Klasson, and, S. G. Andersson. 2002. Microbial genome evolution: sources of variability. Curr. Opin. Microbiol. 5:506512.
53. Mira, A., and, N. A. Moran. 2002. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb. Ecol. 44:137143.
54. Mira, A.,, H. Ochman, and, N. A. Moran. 2001. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17:589596.
55. Moran, N., and, A. Telang. 1998. Bacteriocyte-associated symbionts of insects. Bioscience 48:295304.
56. Moran, N. A. 1996. Accelerated evolution and Muller’s rachet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. USA 93:28732878.
57. Moran, N. A. 2002. Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583586.
58. Moran, N. A. 2002. The ubiquitous and varied role of infection in the lives of animals and plants. Am. Nat. 60:S1S8.
59. Moran, N. A., and, A. Mira. 2001. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol. 2: RESEARCH 0054.
60. Moran, N. A.,, M. A. Munson,, P. Baumann, and, H. Ishikawa. 1993. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc. R. Soc. Lond. B 253:167171.
61. Moran, N. A., and, G. R. Plague. 2004. Genomic changes following host restriction in bacteria. Curr. Opin. Genet. Dev. 14:627633.
62. 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. 71:33023310.
63. Muller, J. 1964. The relation of recombination to mutational advance. Mutat. Res. 1:29.
64. Nogge, G. 1981. Significance of symbionts for the maintenance of an optimal nutritional state for successful reproduction in hematophagous arthropods. Parasitology 82:299304.
65. O’Neill, S.,, A. Hoffman, and, J. Werren. 1998. Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press, New York, NY.
66. Ochman, H., and, L. M. Davalos. 2006. The nature and dynamics of bacterial genomes. Science 311:17301733.
67. Ochman, H.,, S. Elwyn, and, N. A. Moran. 1999. Calibrating bacterial evolution. Proc. Natl. Acad. Sci. USA 96:1263812643.
68. Ochman, H., and, N. A. Moran. 2001. Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292:10961099.
69. Ogata, H.,, P. Renesto,, S. Audic,, C. Robert,, G. Blanc,, P. E. Fournier,, H. Parinello,, J. M. Claverie, and, D. Raoult. 2005. The genome sequence of Rickettsia felis identifies the first putative conjugative plasmid in an obligate intracellular parasite. PLoS Biol. 3:e248.
70. Reference deleted.
71. Ohta, T. 1973. Slightly deleterious mutant substitutions in evolution. Nature 246:9698.
72. Ohta, T., and, M. Kimura. 1971. On the constancy of the evolutionary rate of cistrons. J. Mol. Evol. 1:1825.
73. Oshima, K.,, S. Kakizawa,, H. Nishigawa,, H. Y. Jung,, W. Wei,, S. Suzuki,, R. Arashida,, D. Nakata,, S. Miyata,, M. Ugaki, and, S. Namba. 2004. Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nat. Genet. 36:2729.
74. 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 440:667670.
75. Palmer, G. H. 2002. The highest priority: what microbial genomes are telling us about immunity. Vet. Immunol. Immunopathol. 85:18.
76. Perez-Brocal, V.,, A. Latorre,, R. Gil, and, A. Moya. 2005. Comparative analysis of two genomic regions among four strains of Buchnera aphidicola, primary endosymbiont of aphids. Gene 345:7380.
77. Peterson, J. D.,, L. A. Umayam,, T. Dickinson,, E. K. Hickey, and, O. White. 2001. The comprehensive microbial resource. Nucleic Acids Res. 29:123125.
78. Renesto, P.,, S. Azza,, A. Dolla,, P. Fourquet,, G. Vestris,, J. P. Gorvel, and, D. Raoult. 2005. Proteome analysis of Rickettsia conorii by two-dimensional gel electrophoresis coupled with mass spectrometry. FEMS Microbiol. Lett. 245:231238.
79. Renesto, P.,, H. Ogata,, S. Audic,, J. M. Claverie, and, D. Raoult. 2005. Some lessons from Rickettsia genomics. FEMS Microbiol. Rev. 29:99117.
80. Rispe, C., and, N. A. Moran. 2000. Accumulation of deleterious mutations in endosymbionts: Muller’s ratchet with two levels of selection. Am. Nat. 156:425441.
81. Rocha, E. P., and, A. Danchin. 2002. Base composition bias might result from competition for metabolic resources. Trends Genet. 18:291294.
82. Salzberg, S. L.,, J. C. Hotopp,, A. L. Delcher,, M. Pop,, D. R. Smith,, M. B. Eisen, and, W. C. Nelson. 2005. Serendipitous discovery of Wolbachia genomes in multiple Drosophila species. Genome Biol. 6:R23.
83. Sandström, J.,, A. Telang, and, N. A. Moran. 2000. Nutritional enhancement of host plants by aphids—a comparison of three aphid species on grasses. J. Insect Physiol. 46:3340.
84. Sauer, C.,, D. Dudaczek,, B. Holldobler, and, R. Gross. 2002. Tissue localization of the endosymbiotic bacterium “Candidatus Blochmannia floridanus” in adults and larvae of the carpenter ant Camponotus floridanus. Appl. Environ. Microbiol. 68:41874193.
85. Schmitz-Esser, S.,, N. Linka,, A. Collingro,, C. L. Beier,, H. E. Neuhaus,, M. Wagner, and, M. Horn. 2004. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to chlamydiae and rickettsiae. J. Bacteriol. 186:683691.
86. Selander, R. K.,, D. A. Caugant, and, T. S. Whittam. 1987. Genetic structure and variation in natural populations of Escherichia coli, p. 1625– 1648. In F. Neidhardt (ed.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. ASM Press, Washington, DC.
87. Seshadri, R.,, I. T. Paulsen,, J. A. Eisen,, T. D. Read,, K. E. Nelson,, W. C. Nelson,, N. L. Ward,, H. Tettelin,, T. M. Davidsen,, M. J. Beanan,, R. T. Deboy,, S. C. Daugherty,, L. M. Brinkac,, R. Madupu,, R. J. Dodson,, H. M. Khouri,, K. H. Lee,, H. A. Carty,, D. Scanlan,, R. A. Heinzen,, H. A. Thompson,, J. E. Samuel,, C. M. Fraser, and, J. F. Heidelberg. 2003. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc. Natl. Acad. Sci. USA 100:54555460.
88. Sharp, P. M. 1991. Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium: codon usage, map position, and concerted evolution. J. Mol. Evol. 33:2333.
89. 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 407:8186.
90. Subtil, A., and, A. Dautry-Varsat. 2004. Chlamydia: five years A. G. (after genome). Curr. Opin. Microbiol. 7:8592.
91. 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 296:23762379.
92. 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. 16:149156.
93. Van Ham, R. C.,, 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 100:581586.
94. Wernegreen, J. J. 2005. For better or worse: Genomic consequences of intracellular mutualism and parasitism. Curr. Opin. Genet. Dev. 15:572583.
95. Wernegreen, J. J., and, D. J. Funk. 2004. Mutation exposed: a neutral explanation for extreme base composition of an endosymbiont genome. J. Mol. Evol. 59:849858.
96. Wernegreen, J. J., and, N. A. Moran. 2000. Decay of mutualistic potential in aphid endosymbionts through silencing of biosynthetic loci: Buchnera of Diuraphis. Proc. R. Soc. Lond. B Biol. Sci. 267:14231431.
97. Wernegreen, J. J., and, N. A. Moran. 1999. Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol. Biol. Evol. 16:8397.
98. Woolfit, M., and, L. Bromham. 2003. Increased rates of sequence evolution in endo-symbiotic bacteria and fungi with small effective population sizes. Mol. Biol. Evol. 20:15451555.
99. Wu, M.,, L. V. Sun,, J. Vamathevan,, M. Riegler,, R. Deboy,, J. C. Brownlie,, E. A. McGraw,, W. Martin,, C. Esser,, N. Ahmadinejad,, C. Wiegand,, R. Madupu,, M. J. Beanan,, L. M. Brinkac,, S. C. Daugherty,, A. S. Durkin,, J. F. Kolonay,, W. C. Nelson,, Y. Mohamoud,, P. Lee,, K. Berry,, M. B. Young,, T. Utterback,, J. Weidman,, W. C. Nierman,, I. T. Paulsen,, K. E. Nelson,, H. Tettelin,, S. L. O’Neill, and, J. A. Eisen. 2004. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2:E69.
100. Zientz, E.,, T. Dandekar, and, R. Gross. 2004. Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Micro-biol. Mol. Biol. Rev. 68:745770.


Generic image for table

Obligately intracellular bacteria for which full genome sequence data were published as of July 2005

Citation: Jennifer J. 2007. Genomic Signatures of Intracellularity: Evolutionary Patterns and Paces in Bacterial Mutualists and Parasites, p 196-212. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch8
Generic image for table

Signatures of distinct mechanisms that may contribute to rapid protein evolution in intracellular bacteria

Citation: Jennifer J. 2007. Genomic Signatures of Intracellularity: Evolutionary Patterns and Paces in Bacterial Mutualists and Parasites, p 196-212. In Pallen M, Nelson K, Preston G (ed), Bacterial Pathogenomics. ASM Press, Washington, DC. doi: 10.1128/9781555815530.ch8

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error