Genome degeneration and adaptation in a nascent stage of symbiosis

Genome Biology and Evolution

Volumn 6, Issue 1, 2014, Pages 76-93

  Oakeson, Kelly F ^a   Gil, Rosario ^b   Clayton, Adam L ^a   Dunn, Diane M ^c   Von Niederhausern, Andrew C ^c   Hamil, Cindy ^c   Aoyagi, Alex ^c   Duval, Brett ^c   Baca, Amanda ^a   Silva, Francisco J ^b   Vallier, Agnès ^d   Jackson, D Grant ^a   Latorre, Amparo ^b,e   Weiss, Robert B ^c   Heddi, Abdelaziz ^d   Moya, Andrés ^b,e   Dale, Colin ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF VALENCIA   (Spain)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d UA INRA 203   (France)

^e Vaccine Research Fundación para el Fomento de la Investigación Sanitaria   (Spain)

Author keywords

Comparative genomics; Degenerative genome evolution; IS elements; Pseudogenes; Recent symbiont

Indexed keywords

ADAPTATION; ANIMAL; ARTICLE; BACTERIAL GENOME; BEETLE; COMPARATIVE GENOMICS; DEGENERATIVE GENOME EVOLUTION; ENTEROBACTERIACEAE; GENETICS; IS ELEMENTS; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PSEUDOGENE; RECENT SYMBIONT; SYMBIOSIS;

COMPARATIVE GENOMICS; DEGENERATIVE GENOME EVOLUTION; IS ELEMENTS; PSEUDOGENES; RECENT SYMBIONT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BASE SEQUENCE; BEETLES; ENTEROBACTERIACEAE; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; SYMBIOSIS;

EID: 84892496453     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt210     Document Type: Article

References (138)

1. Ades SE, Grigorova IL, Gross CA. 2003. Regulation of the alternative sigma factor E during initiation, adaptation, and shutoff of the extracytoplasmic heat shock response in Escherichia coli. J Bacteriol. 185: 2512-2519.
2. Akman L, et al. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet. 32: 402-407.
3. Andersson JO, Andersson SGE. 1999. Genome degradation is an ongoing process in Rickettsia. Mol Biol Evol. 16:1178-1191.
4. Anselme C, et al. 2008. Identification of the Weevil immune genes and their expression in the bacteriome tissue. BMC Biol. 6:43.
5. Belda E, Moya A, Bentley S, Silva F. 2010. Mobile genetic element proliferation and gene inactivation impact over the genome structure and metabolic capabilities of Sodalis glossinidius, the secondary endosymbiont of tsetse flies. BMC Genomics 11:449.
6. Bennett GM, Moran NA. 2013. Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol Evol. 5:1675-1688.
7. Bigot S, et al. 2005. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J. 24:3770-3780.
8. Blakely G, et al. 1993. Two related recombinases are required for sitespecific recombination at dif and cer in E coli. K12. Cell 75:351-361.
9. Braendle C, et al. 2003. Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PLoS Biol. 1:E21.
10. Carnoy C, Roten C-A. 2009. The dif/Xer recombination systems in proteobacteria. PLoS One 4(9):e6531.
11. Carver TJ, et al. 2005. ACT: the artemis comparison tool. Bioinformatics 21:3422-3423.
12. Caspi R, et al. 2010. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 38:D473-D479.
13. Chain PSG, et al. 2004. Insights into the evolution of Yersinia pestis throughwhole-genome comparisonwith Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A. 101:13826-13831.
14. Charles H, Heddi A, Guillaud J, Nardon C, Nardon P. 1997. A molecular aspect of symbiotic interactions between the weevil Sitophilus oryzae and its endosymbiotic bacteria: over-expression of a chaperonin. Biochem Biophys Res Commun. 239:769-774.
15. Charles H, Heddi A, RahbéY. 2001. A putative insect intracellular endosymbiont stem clade, within the Enterobacteriaceae, inferred from phylogenetic analysis based on a heterogeneous model of DNA evolution. C R Acad Sci III. 324:489-494.
16. Chrudimský T, Husník F, Novakova E, Hypsa V. 2012. Candidatus Sodalis melophagi sp. nov.: phylogenetically independent comparative model to the tsetse fly symbiont Sodalis glossinidius. PLoS One 7:e40354.
17. Clayton AL, et al. 2012. A novel human-infection-derived bacterium provides insights into the evolutionary origins of mutualistic insect- bacterial symbioses. PLoS Genet. 8:e1002990.
18. Conesa A, et al. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
19. Conord C, et al. 2008. Long-term evolutionary stability of bacterial endosymbiosis in curculionoidea: additional evidence of symbiont replacement in the dryophthoridae family. Mol Biol Evol. 25:859-868.
20. Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. 2002. Mobile DNA II. Washington, DC: ASM Press.
21. Dale C, Jones T, Pontes M. 2005. Degenerative evolution and functional diversification of type-III secretion systems in the insect endosymbiont Sodalis glossinidius. Mol Biol Evol. 22:758-766.
22. Dale C, Wang B, Moran N, Ochman H. 2003. Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration. Mol Biol Evol. 20:1188-1194.
23. Dale C, Young SA, Haydon DT, Welburn SC. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Sci U S A. 98:1883-1888.
24. Darcan C, Ozkanca R, Flint KP. 2003. Survival of nonspecific porin-deficient mutants of Escherichia coli in black sea water. Lett Appl Microbiol. 37:380-385.
25. Derbyshire KM, Grindley ND. 1996. Cis preference of the IS903 transposase is mediated by a combination of transposase instability and inefficient translation. Mol Microbiol. 21:1261-1272.
26. Derbyshire KM, Kramer M, Grindley ND. 1990. Role of instability in the cis action of the insertion sequence IS903 transposase. Proc Natl Acad Sci U S A. 87:4048-4052.
27. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
28. Erickson JW, Vaughn V, Walter WA, Neidhardt FC, Gross CA. 1987. Regulation of the promoters and transcripts of rpoH, the Escherichia coli heat shock regulatory gene. Genes Dev. 1:419-432.
29. Fang Z, et al. 1999. IS6110-mediated deletions of wild-type chromosomes of Mycobacterium tuberculosis. J Bacteriol. 181:1014-1020.
30. FaresMA, Moya A, Barrio E. 2004. GroEL and themaintenance of bacterial endosymbiosis. Trends Genet. 20:413-416.
31. Figueira R, Holden DW. 2012. Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology 158: 1147-1161.
32. Fischer S, et al. 2002. Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new ortholog groups. Hoboken (NJ): John Wiley & Sons, Inc.
33. Francino MP, Ochman H. 1997. Strand asymmetries in DNA evolution. Trends Genet. 13:240-245.
34. Frank AC, Lobry JR. 1999. Asymmetric substitution patterns: a review of possible underlying mutational or selective mechanisms. Gene 238: 65-77.
35. Gao R, Mack TR, Stock AM. 2007. Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem Sci. 32: 225-234.
36. Gardner AM, Gessner CR, Gardner PR. 2003. Regulation of the nitric oxide reduction operon (norRVW) in Escherichia coli. Role of NorR and sigma54 in the nitric oxide stress response. J Biol Chem. 278: 10081-10086.
37. Gil Garcia R, et al. 2008. Massive presence of insertion sequences in the genome of SOPE, the primary endosymbiont of the rice weevil "Sitophilus oryzae.". Int Microbiol. 11:41-48.
38. Gil R, Latorre A, Moya A. 2010. Evolution of prokaryote-animal symbiosis from a genomics perspective. In: Hackstein JHP, editor. (Endo)symbiotic methanogenic Archaea. Microbiology monographs. Vol. 19. Berlin (Germany): Springer. p. 207-233.
39. Gil R, Silva FJ, PeretóJ, Moya A. 2004. Determination of the core of a minimal bacterial gene set. Microbiol Mol Biol Rev. 68:518-537, table of contents.
40. Gordon D, Abajian C, Green P. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8:195-202.
41. Grossman AD, Erickson JW, Gross CA. 1984. The htpR gene product of E. coli is a sigma factor for heat-shock promoters. Cell 38:383-390.
42. Guindon S, et al. 2010. New algorithms and methods to estimate maximum- likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 59:307-321.
43. Hasegawa M, Kishino H, Yano T. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 22:160-174.
44. Heddi A, Charles H, Khatchadourian C, Bonnot G, Nardon P. 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.
45. Heddi A, Grenier AM, Khatchadourian C, Charles H, Nardon P. 1999. Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci U S A. 96:6814-6819.
46. Heffernan EJ, et al. 1994. Specificity of the complement resistance and cell association phenotypes encoded by the outer membrane protein genes rck from Salmonella typhimurium and ail from Yersinia enterocolitica. Infect Immun. 62:5183-5186.
47. Heinrichs DE, Yethon JA, Whitfield C. 1998. Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol Microbiol. 30:221-232.
48. Hirschman J, Wong PK, Sei K, Keener J, Kustu S. 1985. Products of nitrogen regulatory genes ntrA and ntrC of enteric bacteria activate glnA transcription in vitro: evidence that the ntrA product is a sigma factor. Proc Natl Acad Sci U S A. 82:7525-7529.
49. Hueck CJ. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev. 62:379-433.
50. Hunt TP, Magasanik B. 1985. Transcription of glnA by purified Escherichia coli components: core RNA polymerase and the products of glnF, glnG, and glnL. Proc Natl Acad Sci U S A. 82:8453-8457.
51. International Aphid Genomics Consortium. 2010. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. 8:e1000313.
52. Ishikawa H. 1984. Alteration with age of symbiosis of gene expression in aphid endosymbionts. BioSystems 17:127-134.
53. Jin Q, et al. 2002. Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res. 30:4432-4441.
54. Jishage M, Iwata A, Ueda S, Ishihama A. 1996. Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of four species of sigma subunit under various growth conditions. J Bacteriol. 178:5447-5451.
55. Kato J-I, Suzuki H, Hirota Y. 1985. Dispensability of either penicillin-binding protein -1a or -1b involved in the essential process for cell elongation in Escherichia coli. Mol Gen Genet. 200:272-277.
56. Keseler IM, et al. 2013. EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res. 41:D605-D612.
57. Klappenbach JA, Dunbar JM, Schmidt TM. 2000. rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol. 66:1328-1333.
58. Kuempel PL, Henson JM, Dircks L, Tecklenburg M, Lim DF. 1991. dif, a recA-independent recombination site in the terminus region of the chromosome of Escherichia coli. New Biol. 3:799-811.
59. Lefèvre C, et al. 2004. Endosymbiont phylogenesis in the dryophthoridae weevils: evidence for bacterial replacement. Mol Biol Evol. 21: 965-973.
60. Levy O, et al. 2005. Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc Natl Acad Sci U S A. 102:17618-17623.
61. Li L. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189.
62. Lima T, et al. 2009. HAMAP: a database of completely sequenced microbial proteome sets and manually curated microbial protein families in UniProtKB/Swiss-Prot. Nucleic Acids Res. 37:D471-D478.
63. Lobry JR. 1996. Asymmetric substitution patterns in the two DNA strands of bacteria. Mol Biol Evol. 13:660-665.
64. Login FH, et al. 2011. Antimicrobial peptides keep insect endosymbionts under control. Science 334:362-365.
65. Maciag A, et al. 2011. In vitro transcription profiling of the S subunit of bacterial RNA polymerase: re-definition of the S regulon and identification of S-specific promoter sequence elements. Nucleic Acids Res. 39:5338-5355.
66. Maezawa K, et al. 2006. Hundreds of flagellar basal bodies cover the cell surface of the endosymbiotic bacterium Buchnera aphidicola sp. strain APS. J Bacteriol. 188:6539-6543.
67. Mahillon J, Chandler M. 1998. Insertion sequences.Microbiol Mol Biol Rev. 62:725-774.
68. Maltz MA, Weiss BL, O'Neill M, Wu Y, Aksoy S. 2012. OmpA-mediated biofilm formation is essential for the commensal bacterium Sodalis glossinidius to colonize the tsetse fly gut. Appl Environ Microbiol. 78:7760-7768.
69. Margulies M, et al. 2005. Genome sequencing in microfabricated highdensity picolitre reactors. Nature 437:376-380.
70. McCutcheon JP, McDonald BR, Moran NA. 2009. Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet. 5:e1000565.
71. McCutcheon JP, Moran NA. 2007. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci U S A. 104:19392-19397.
72. McCutcheon JP, Moran NA. 2010. Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol Evol. 2:708-718.
73. McCutcheon JP, Moran NA. 2011. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol. 10:13-26.
74. Mira A, Ochman H, Moran NA. 2001. Deletional bias and the evolution of bacterial genomes. Trends Genet. 17:589-596.
75. Mitrophanov AY, Groisman EA. 2008. Signal integration in bacterial twocomponent regulatory systems. Genes Dev. 22:2601-2611.
76. Moran NA. 1996. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 93:2873-2878.
77. Moran NA, McCutcheon JP, Nakabachi A. 2008. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet. 42: 165-190.
78. Moran NA, Plague GR. 2004. Genomic changes following host restriction in bacteria. Curr Opin Genet Dev. 14:627-633.
79. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35:W182-W185.
80. Moya A, PeretóJ, Gil R, Latorre A. 2008. Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet. 9: 218-229.
81. Mullikin JC, Ning Z. 2003. The phusion assembler. Genome Res. 13: 81-90.
82. Murray RG, Stackebrandt E. 1995. Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol. 45:186-187.
83. Nakabachi A, et al. 2006. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314:267.
84. Nakayama K, et al. 2008. The Whole-genome sequencing of the obligate intracellular bacterium Orientia tsutsugamushi revealed massive gene amplification during reductive genome evolution. DNA Res. 15: 185-199.
85. Nierman WC, et al. 2004. Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad Sci U S A. 101:14246-14251.
86. Ogata H, et al. 1999. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 27:29-34.
87. Paradis-Bleau C, et al. 2010. Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143: 1110-1120.
88. Parkhill J, et al. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet. 35:32-40.
89. Pei AY, et al. 2010. Diversity of 16S rRNA genes within individual prokaryotic genomes. Appl Environ Microbiol. 76:3886-3897.
90. Pérez-Brocal V, et al. 2006. A small microbial genome: the end of a long symbiotic relationship? Science 314:312-313.
91. Pierantoni U. 1927. L'organo simbiotico nello sviluppo di Calandra oryzae. Rend Reale Acad Sci Fis Mat Napoli. 35:244-250.
92. Plague GR, Dunbar HE, Tran PL, Moran NA. 2008. Extensive proliferation of transposable elements in heritable bacterial symbionts. J Bacteriol. 190:777-779.
93. Pontes MH, Smith KL, De Vooght L, Van Den Abbeele J, Dale C. 2011. Attenuation of the sensing capabilities of PhoQ in transition to obligate insect-bacterial association. PLoS Genet. 7:e1002349.
94. Ramos-Morales F, Prieto AI, Beuzón CR, Holden DW, Casadesús J. 2003. Role for Salmonella enterica enterobacterial common antigen in bile resistance and virulence. J Bacteriol. 185:5328-5332.
95. ReguéM, et al. 2001. Genetic characterization of the Klebsiella pneumoniaewaa gene cluster, involved in core lipopolysaccharide biosynthesis. J Bacteriol. 183:3564-3573.
96. Reimmann C, et al. 1989. Genetic structure, function and regulation of the transposable element IS21. Mol Gen Genet. 215:416-424.
97. Reitzer LJ, et al. 1987. Mutations that create new promoters suppress the sigma 54 dependence of glnA transcription in Escherichia coli. J Bacteriol. 169:4279-4284.
98. Rio RVM, Lefèvre C, Heddi A, Aksoy S. 2003. Comparative genomics of insect-symbiotic bacteria: influence of host environment on microbial genome composition. Appl Environ Microbiol. 69:6825-6832.
99. Roberts D, Hoopes BC, McClureWR, Kleckner N. 1985. IS10 transposition is regulated by DNA adenine methylation. Cell 43:117-130.
100. Rocha EP. 2004. The replication-related organization of bacterial genomes. Microbiology 150:1609-1627.
101. Rocha EP, et al. 2006. Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol. 239:226-235.
102. Rodionov DA, Mironov AA, Gelfand MS. 2002. Conservation of the biotin regulon and the BirA regulatory signal in Eubacteria and Archaea. Genome Res. 12:1507-1516.
103. Rutherford K, et al. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945.
104. Sanishvili R, et al. 2003. Integrating structure, bioinformatics, and enzymology to discover function: BioH, a new carboxylesterase from Escherichia coli. J Biol Chem. 278:26039-26045.
105. Scheer M, et al. 2011. BRENDA, the enzyme information system in 2011. Nucleic Acids Res. 39:D670-D676.
106. Scheffers D-J, Pinho MG. 2005. Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev. 69:585-607.
107. Schmitz-Esser S, Penz T, Spang A, Horn M. 2011. A bacterial genome in transition - an exceptional enrichment of IS elements but lack of evidence for recent transposition in the symbiont Amoebophilus asiaticus. BMC Evol Biol. 11:270.
108. Schnetz K, Rak B. 1992. IS5: a mobile enhancer of transcription in Escherichia coli. Proc Natl Acad Sci U S A. 89:1244-1248.
109. Sedgwick SG, Smerdon SJ. 1999. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci. 24: 311-316.
110. Silva FJ, Latorre A, Moya A. 2003. Why are the genomes of endosymbiotic bacteria so stable? Trends Genet. 19:176-180.
111. Sivanathan V, et al. 2009. KOPS-guided DNA translocation by FtsK safeguards Escherichia coli chromosome segregation. Mol Microbiol. 71: 1031-1042.
112. Song H, et al. 2010. The early stage of bacterial genome-reductive evolution in the host. PLoS Pathog. 6:e1000922.
113. Spratt BG. 1975. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc Natl Acad Sci U S A. 72:2999-3003.
114. Spratt BG, Jobanputra V. 1977. Mutants of Escherichia coli which lack a component of penicillin-binding protein 1 are viable. FEBS Lett. 79: 374-378.
115. Stevenson BS, Schmidt TM. 2004. Life history implications of rRNA gene copy number in Escherichia coli. Appl Environ Microbiol. 70: 6670-6677.
116. Stoll S, Feldhaar H, Gross R. 2009. Transcriptional profiling of the endosymbiont Blochmannia floridanus during different developmental stages of its holometabolous ant host. Environ Microbiol. 11:877-888.
117. Suzuki H, Nishimura Y, Hirota Y. 1978. On the process of cellular division in Escherichia coli: a series of mutants of E. coli altered in the penicillinbinding proteins. Proc Natl Acad Sci U S A. 75:664-668.
118. Tram U, Ferree PM, Sullivan W. 2003. Identification of Wolbachia - host interacting factors through cytological analysis. Microbes Infect. 5: 999-1011.
119. Tram U, Sullivan W. 2002. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296:1124-1126.
120. Typas A, et al. 2010. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143:1097-1109.
121. Valle J, Vergara-Irigaray M, Merino N, Penadés JR, Lasa I. 2007. sigmaB regulates IS256-mediated Staphylococcus aureus biofilm phenotypic variation. J Bacteriol. 189:2886-2896.
122. van Domselaar GH, et al. 2005. BASys: a web server for automated bacterial genome annotation. Nucleic Acids Res. 33:W455-W459.
123. Varani AM, Siguier P, Gourbeyre E, Charneau V, Chandler M. 2011. ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol. 12:R30.
124. Větrovský T, Baldrian P. 2013. The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS One 8:e57923.
125. Vigneron A, et al. 2012. Host gene response to endosymbiont and pathogen in the cereal weevil Sitophilus oryzae. BMC Microbiol. 12(1 Suppl):S14.
126. Viñuelas J, et al. 2007, Conservation of the links between gene transcription and chromosomal organization in the highly reduced genome of Buchnera aphidicola. BMC Genomics 8, 143.
127. Vogt J, Schulz GE. 1999. The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence. Structure 7:1301-1309.
128. Wagner A, Lewis C, Bichsel M. 2007. A survey of bacterial insertion sequences using IScan. Nucleic Acids Res. 35:5284-5293.
129. Wang QP, Kaguni JM. 1989. A novel sigma factor is involved in expression of the rpoH gene of Escherichia coli. J Bacteriol. 171:4248-4253.
130. Wei J, et al. 2003. Complete genome sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T. Infect Immun. 71: 2775-2786.
131. Weiss BL, Wu Y, Schwank JJ, Tolwinski NS, Aksoy S. 2008. An insect symbiosis is influenced by bacterium-specific polymorphisms in outer-membrane protein A. Proc Natl Acad Sci U S A. 105: 15088-15093.
132. Wicker C. 1983. Differential vitamin and choline requirements of symbiotic and aposymbiotic s. oryzae (coleoptera: curculionidae). Comp Biochem Physiol Part A Physiol. 76:177-182.
133. Wientjes FB, Nanninga N. 1991. On the role of the high molecular weight penicillin-binding proteins in the cell cycle of Escherichia coli. Res Microbiol. 142:333-344.
134. Wuyts J. 2001. Distribution of substitution rates and location of insertion sites in the tertiary structure of ribosomal RNA. Nucleic Acids Res. 29: 5017-5028.
135. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
136. Yethon JA. 1998. Involvement of waaY, waaQ, and waaP in the modification of Escherichia coli lipopolysaccharide and their role in the formation of a stable outer membrane. J Biol Chem. 273: 26310-26316.
137. Young GM, Schmiel DH,Miller VL. 1999. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci U S A. 96: 6456-6461.
138. Yura T, Tobe T, Ito K, Osawa T. 1984. Heat shock regulatory gene (htpR) of Escherichia coli is required for growth at high temperature but is dispensable at low temperature. Proc Natl Acad Sci U S A. 81: 6803-6807.