Differential genome evolution between companion symbionts in an Insect-Bacterial symbiosis

mBio

Volumn 5, Issue 5, 2014, Pages

  Bennett, Gordon M ^a   McCutcheon, John P ^b   MacDonald, Bradon R ^c   Romanovicz, Dwight ^a   Moran, Nancy A ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF MONTANA   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIUM; BACTEROIDETES; CANDIDATUS BAUMANNIA CICADELLINICOLA; CANDIDATUS SULCIA MUELLERI; CELL STRUCTURE; CLADISTICS; FEMALE; GAMMAPROTEOBACTERIA; GENE MUTATION; GENE SEQUENCE; GENOMIC INSTABILITY; GRAPHOCEPHALA ATROPUNCTATA; HOMALODISCA VITRIPENNIS; INSECT; LEAFHOPPER; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SYMBIONT; SYMBIOSIS; ANIMAL; DNA REPLICATION; DNA SEQUENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEMIPTERA; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); HEXAPODA;

ANIMALS; BACTEROIDETES; DNA REPLICATION; EVOLUTION, MOLECULAR; FEMALE; GAMMAPROTEOBACTERIA; GENOME, BACTERIAL; HEMIPTERA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 84908406671     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01697-14     Document Type: Article

References (88)

1. Buchner P. 1965. Endosymbiosis of animals with plant microorganisms. John Wiley & Sons, New York, NY.
2. Moran NA. 1996. Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc. Natl. Acad. Sci. U. S. A. 93:2873-2878. http:// dx.doi.org/10.1073/pnas.93.7.2873.
3. Moran NA, Baumann P. 2000. Bacterial endosymbionts in animals. Curr. Opin. Microbiol. 3:270 -275. http://dx.doi.org/10.1016/S1369- 5274(00)00088-6.
4. Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE, Moran NA, Hattori M. 2006. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314:267. http://dx.doi.org/10.1126/ science.1134196.
5. Pérez-Brocal V, Gil R, Ramos S, Lamelas A, Postigo M, Michelena JM, Silva FJ, Moya A, Latorre A. 2006. A small microbial genome: the end of a long symbiotic relationship? Science 314:312-313. http://dx.doi.org/ 10.1126/science.1130441.
6. 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. http://dx.doi.org/10.1371/ journal.pgen.1000565.
7. 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. http://dx.doi.org/10.1093/gbe/evt118.
8. McCutcheon JP, von Dohlen CD. 2011. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr. Biol. 21: 1366-1372. http://dx.doi.org/10.1016/j.cub.2011.06.051.
9. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, Hattori M, Aksoy S. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32:402- 407. http:// dx.doi.org/10.1038/ng986.
10. Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, Lee SH, Robertson HM, Kennedy RC, Elhaik E, Gerlach D, Kriventseva EV, Elsik CG, Graur D, Hill CA, Veenstra JA, Walenz B, Tubío JM, Ribeiro JM, Rozas J, Johnston JS, Reese JT, Popadic A, Tojo M, Raoult D, Reed DL, Tomoyasu Y, Kraus E, Krause E, Mittapalli O, Margam VM, Li HM, Meyer JM, Johnson RM, Romero-Severson J, Vanzee JP, Alvarez- Ponce D, Vieira FG, Aguadé M, Guirao-Rico S, Anzola JM, Yoon KS, Strycharz JP, Unger MF, Christley S, Lobo NF, Seufferheld MJ, Wang N, Dasch GA, Struchiner CJ, Madey G, Hannick LI, Bidwell S, Joardar V, Caler E, Shao R, Barker SC, Cameron S, Bruggner RV, Regier A, Johnson J, Viswanathan L, Utterback TR, Sutton GG, Lawson D, Waterhouse RM, Venter JC, Strausberg RL, Berenbaum MR, Collins FH, Zdobnov EM, Pittendrigh BR. 2010. Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc. Natl. Acad. Sci. U. S. A. 107: 12168-12173. http://dx.doi.org/10.1073/pnas.1003379107.
11. Wu D, Daugherty SC, Van Aken SE, Pai GH, Watkins KL, Khouri H, Tallon LJ, Zaborsky JM, Dunbar HE, Tran PL, Moran NA, Eisen JA. 2006. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biol. 4:e188. http://dx.doi.org/10.1371/ journal.pbio.0040188.
12. 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. http://dx.doi.org/10.1073/pnas.0708855104.
13. McCutcheon JP, Moran NA. 2010. Functional convergence in reduced genomes of bacterial symbionts spanning 200 million years of evolution. Genome Biol. Evol. 3:708-718. http://dx.doi.org/10.1093/gbe/evq055.
14. McCutcheon JP, Moran NA. 2011. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10:13-26. http://dx.doi.org/10.1038/ nrmicro2670.
15. Moran NA, Bennett GM. 2 June 2014. The tiniest tiny genomes. Annu. Rev. Microbiol. 64:195-215. http://dx.doi.org/10.1146/annurev-micro- 091213-112901.
16. Neef A, Latorre A, Peretó J, Silva FJ, Pignatelli M, Moya A. 2011. Genome economization in the endosymbiont of the wood roach Cryptocercus punctulatus due to drastic loss of amino acid synthesis capabilities. Genome Biol. Evol. 3:1437-1448. http://dx.doi.org/10.1093/gbe/evr118.
17. Sabree ZL, Huang CY, Okusu A, Moran NA, Normark BB. 2013. The nutrient supplying capabilities of Uzinura, an endosymbiont of armoured scale insects. Environ. Microbiol. 15:1988 -1999. http://dx.doi.org/ 10.1111/1462-2920.12058.
18. Lamelas A, Gosalbes MJ, Manzano-Marín A, Peretó J, Moya A, Latorre A. 2011. Serratia symbiotica from the aphid Cinara cedri: a missing link from facultative to obligate insect endosymbiont. PLoS Genet. 7:e1002357. http://dx.doi.org/10.1371/journal.pgen.1002357.
19. Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, Tanaka M, Satoh N, Bachtrog D, Wilson AC, von Dohlen CD, Fukatsu T, Mc- Cutcheon JP. 2013. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153: 1567-1578. http://dx.doi.org/10.1016/j.cell.2013.05.040.
20. López-Madrigal S, Latorre A, Porcar M, Moya A, Gil R. 2011. Complete genome sequence of "Candidatus Tremblaya princeps" strain PCVAL, an intriguing translational machine below the living-cell status. J. Bacteriol. 193:5587-5588. http://dx.doi.org/10.1128/JB.05749-11.
21. Degnan PH, Ochman H, Moran NA. 2011. Sequence conservation and functional constraint on intergenic spacers in reduced genomes of the obligate symbiont Buchnera. PLoS Genet. 7:e1002252. http://dx.doi.org/ 10.1371/journal.pgen.1002252.
22. Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A, Gurgui M, Oldham NJ, van Echten-Deckert G, Okamura K, Yamamoto K, Inoue H, Ohkuma M, Hongoh Y, Miyagishima SY, Hattori M, Piel J, Fukatsu T. 2013. Defensive bacteriome symbiont with a drastically reduced genome. Curr. Biol. 23:1478 -1484. http://dx.doi.org/10.1016/ j.cub.2013.06.027.
23. Sabree ZL, Huang CY, Arakawa G, Tokuda G, Lo N, Watanabe H, Moran NA. 2012. Genome shrinkage and loss of nutrient-providing potential in the obligate symbiont of the primitive termite Mastotermes darwiniensis. Appl. Environ. Microbiol. 78:204 -210. http://dx.doi.org/ 10.1128/AEM.06540-11.
24. Jiang ZF, Xia F, Johnson KW, Bartom E, Tuteja JH, Stevens R, Grossman RL, Brumin M, White KP, Ghanim M. 2012. Genome sequences of the primary endosymbiont "Candidatus Portiera aleyrodidarum" in the whitefly Bemisia tabaci B and Q biotypes. J. Bacteriol. 194:6678-6679. doi:10.1128/JB.01841-12. PubMed.
25. Santos-Garcia D, Farnier PA, Beitia F, Zchori-Fein E, Vavre F, Mouton L, Moya A, Latorre A, Silva FJ. 2012. Complete genome sequence of "Candidatus Portiera aleyrodidarum" BT-QVLC, an obligate symbiont that supplies amino acids and carotenoids to Bemisia tabaci. J. Bacteriol. 194:6654-6655. http://dx.doi.org/10.1128/JB.01793-12.
26. Sloan DB, Moran NA. 2012. Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol. Lett. 8:986 -989. http://dx.doi.org/10.1098/ rsbl.2012.0664.
27. Sloan DB, Moran NA. 2012. Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Mol. Biol. Evol. 29:3781-3792. http://dx.doi.org/10.1093/molbev/mss180.
28. Patiño-Navarrete R, Moya A, Latorre A, Peretó J. 2013. Comparative genomics of Blattabacterium cuenoti: the frozen legacy of an ancient endosymbiont genome. Genome Biol. Evol. 5:351-361. http://dx.doi.org/ 10.1093/gbe/evt011.
29. Moran NA, Tran P, Gerardo NM. 2005. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl. Environ. Microbiol. 71:8802-8810. http://dx.doi.org/10.1128/AEM.71.12.8802-8810.2005.
30. Urban JM, Cryan JR. 2012. Two ancient bacterial endosymbionts have coevolved with the planthoppers (Insecta: Hemiptera: Fulgoroidea).BMC Evol. Biol. 12:87. http://dx.doi.org/10.1186/1471-2148-12-87.
31. Koga R, Moran NA. 2014. Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont. ISME J. 8:1237-1246. http://dx.doi.org/10.1038/ismej.2013.235.
32. Koga R, Bennett GM, Cryan JR, Moran NA. 2013. Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ. Microbiol. 15:2073-2081. http://dx.doi.org/10.1111/1462- 2920.12121.
33. Moran NA, Dale C, Dunbar H, Smith WA, Ochman H. 2003. Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome. Environ. Microbiol. 5:116 -126. http://dx.doi.org/10.1046/j.1462-2920.2003.00391.x.
34. Takiya DM, Tran PL, Dietrich CH, Moran NA. 2006. Co-cladogenesis spanning three phyla: leafhoppers (Insecta: Hemiptera: Cicadellidae) and their dual bacterial symbionts. Mol. Ecol. 15:4175- 4191. http:// dx.doi.org/10.1111/j.1365-294X.2006.03071.x.
35. Purcell AH. 1976. Seasonal changes in host plant preference of the bluegreen sharpshooter Hordnia circellata (Homoptera: Cicadellidae). Pan- Pac. Entomol. 52:33-37.
36. Woyke T, Tighe D, Mavromatis K, Clum A, Copeland A, Schackwitz W, Lapidus A, Wu D, McCutcheon JP, McDonald BR, Moran NA, Bristow J, Cheng JF. 2010. One bacterial cell, one complete genome. PLoS One 5:e10314. http://dx.doi.org/10.1371/journal.pone.0010314.
37. Gil R, Sabater-Muñoz B, Perez-Brocal V, Silva FJ, Latorre A. 2006. Plasmids in the aphid endosymbiont Buchnera aphidicola with the smallest genomes. A puzzling evolutionary story. Gene 370:17-25. http:// dx.doi.org/10.1016/j.gene.2005.10.043.
38. van Ham RC, Moya A, Latorre A. 1997. Putative evolutionary origin of plasmids carrying the genes involved in leucine biosynthesis in Buchnera aphidicola (endosymbiont of aphids). J. Bacteriol. 179:4768-4777.
39. Matuszewska M, Kuczyńska-Wisńik D, Laskowska E, Liberek K. 2005. The small heat shock protein IbpA of Escherichia coli cooperates with IbpB in stabilization of thermally aggregated proteins in a disaggregation competent state. J. Biol. Chem. 280:12292-12298. http://dx.doi.org/10.1074/ jbc.M412706200.
40. Chiba S, Ito K, Akiyama Y. 2006. The Escherichia coli plasma membrane contains two PHB (prohibitin homology) domain protein complexes of opposite orientations. Mol. Microbiol. 60:448-457. http://dx.doi.org/ 10.1111/j.1365-2958.2006.05104.x.
41. Akiyama Y. 2009. Quality control of cytoplasmic membrane proteins in Escherichia coli. J. Biochem. 146:449-454. http://dx.doi.org/10.1093/jb/ mvp071.
42. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81-86. http://dx.doi.org/10.1038/35024074.
43. Wilson AC, Ashton PD, Calevro F, Charles H, Colella S, Febvay G, Jander G, Kushlan PF, Macdonald SJ, Schwartz JF, Thomas GH, Douglas AE. 2010. 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):249 -258. http://dx.doi.org/ 10.1111/j.1365-2583.2009.00942.x.
44. Hansen AK, Moran NA. 2011. Aphid genome expression reveals hostsymbiont cooperation in the production of amino acids. Proc. Natl. Acad. Sci. U. S. A. 108:2849-2854. http://dx.doi.org/10.1073/pnas.1013465108.
45. Douglas AE. 1988. Experimental studies on the mycetome symbiosis in the leafhopper Euscelis incisus. J. Insect Physiol. 34:1-10. http:// dx.doi.org/10.1016/0022-1910(88)90033-9.
46. Charles H, Balmand S, Lamelas A, Cottret L, Pérez-Brocal V, Burdin B, Latorre A, Febvay G, Colella S, Calevro F, Rahbé Y. 2011. A genomic reappraisal of symbiotic function in the aphid/Buchnera symbiosis: reduced transporter sets and variable membrane organisations. PLoS One 6:e29096. http://dx.doi.org/10.1371/journal.pone.0029096.
47. Bos MP, Robert V, Tommassen J. 2007. Biogenesis of the gram-negative bacterial outer membrane. Annu. Rev. Microbiol. 61:191-214. http:// dx.doi.org/10.1146/annurev.micro.61.080706.093245.
48. Raetz CR, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700. http://dx.doi.org/10.1146/ annurev.biochem.71.110601.135414.
49. Walburger A, Lazdunski C, Corda Y. 2002. The Tol/pal system function requires an interaction between the C-terminal domain of TolA and the N-terminal domain of TolB. Mol. Microbiol. 44:695-708. http:// dx.doi.org/10.1046/j.1365-2958.2002.02895.x.
50. Cascales E, Lloubès R. 2004. Deletion analyses of the peptidoglycanassociated lipoprotein Pal reveals three independent binding sequences including a TolA box. Mol. Microbiol. 51:873- 885. http://dx.doi.org/ 10.1046/j.1365-2958.2003.03881.x.
51. Typas A, Banzhaf M, Gross CA, Vollmer W. 2011. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 10:123-136. http://dx.doi.org/10.1038/nrmicro2677.
52. Dubuisson JF, Vianney A, Hugouvieux-Cotte-Pattat N, Lazzaroni JC. 2005. Tol-pal proteins are critical cell envelope components of Erwinia chrysanthemi affecting cell morphology and virulence. Microbiology 151(Pt 10):3337-3347. http://dx.doi.org/10.1099/mic.0.28237-0.
53. McCutcheon JP, McDonald BR, Moran NA. 2009. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc. Natl. Acad. Sci. U. S. A. 106:15394 -15399. http://dx.doi.org/10.1073/ pnas.0906424106.
54. Oakeson KF, Gil R, Clayton AL, Dunn DM, von Niederhausern AC, Hamil C, Aoyagi A, Duval B, Baca A, Silva FJ, Vallier A, Jackson DG, Latorre A, Weiss RB, Heddi A, Moya A, Dale C. 2014. Genome degeneration and adaptation in a nascent stage of symbiosis. Genome Biol. Evol. 6:76-93. http://dx.doi.org/10.1093/gbe/evt210.
55. Vigneron A, Charif D, Vincent-Monégat C, Vallier A, Gavory F, Wincker P, Heddi A. 2012. Host gene response to endosymbiont and pathogen in the cereal weevil Sitophilus oryzae. BMC Microbiol. 12(Suppl 1):S14. http://dx.doi.org/10.1186/1471-2180-12-S1-S14.
56. Ryan VT, Grimwade JE, Camara JE, Crooke E, Leonard AC. 2004. Escherichia coli prereplication complex assembly is regulated by dynamic interplay among Fis, IHF and DnaA. Mol. Microbiol. 51:1347-1359. http://dx.doi.org/10.1046/j.1365-2958.2003.03906.x.
57. Fuller RS, Kornberg A. 1983. Purified dnaA protein in initiation of replication at the Escherichia coli chromosomal origin of replication. Proc. Natl. Acad. Sci. U. S. A. 80:5817-5821. http://dx.doi.org/10.1073/ pnas.80.19.5817.
58. Sánchez-Pulido L, Devos D, Genevrois S, Valencia M. 2003. POTRA: a conserved domain in the FtsQ family and a class of _-barrel outer membrane proteins. Trends Biochem. Sci. 28:523-526. http://dx.doi.org/ 10.1016/j.tibs.2003.08.003.
59. Lutkenhaus J, Pichoff S, Du S. 2012. Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton 69:778 -790. http://dx.doi.org/10.1002/ cm.21054.
60. Vicente M, Rico AI, Martínez-Arteaga R, Mingorance J. 2006. Septum enlightenment: assembly of bacterial division proteins. J. Bacteriol. 188: 19-27. http://dx.doi.org/10.1128/JB.188.1.19-27.2006.
61. Höltje JV. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181-203.
62. Gerding MA, Ogata Y, Pecora ND, Niki H, de Boer PA. 2007. The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. Coli. Mol. Microbiol. 63:1008-1025. http://dx.doi.org/10.1111/ j.1365-2958.2006.05571.x.
63. Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J, Nichols RJ, Zietek M, Beilharz K, Kannenberg K, von Rechenberg M, Breukink E, den Blaauwen T, Gross CA, Vollmer W. 2010. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143: 1097-1109. http://dx.doi.org/10.1016/j.cell.2010.11.038.
64. Heidrich C, Templin MF, Ursinus A, Merdanovic M, Berger J, Schwarz H, De Pedro MA, Höltje JV. 2001. Involvement of N-acetylmuramyl-lalanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol. 41:167-178. http://dx.doi.org/10.1046/ j.1365-2958.2001.02499.x.
65. Boutte CC, Crosson S. 2013. Bacterial lifestyle shapes stringent response activation. Trends Microbiol. 21:174 -180. http://dx.doi.org/10.1016/ j.tim.2013.01.002.
66. Husník F, Chrudimský T, Hypša V. 2011. Multiple origins of endosymbiosis within the Enterobacteriaceae (_-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biol. 9:87. http://dx.doi.org/ 10.1186/1741-7007-9-87.
67. Clayton AL, Oakeson KF, Gutin M, Pontes A, Dunn DM, Niederhausern AC, Weiss RB, Fisher M, Dale C. 2012. A novel humaninfection- derived bacterium provides insights into the evolutionary origins of mutualistic insect- bacterial symbioses. PLoS Genet. 8:e1002990. http://dx.doi.org/10.1371/journal.pgen.1002990.
68. Rosas-Pérez T, Rosenblueth M, Rincón-Rosales R, Mora J, Martínez- Romero E. 2014. Genome sequence of "Candidatus Walczuchella monophlebidarum" the flavobacterial endosymbiont of Llaveia axin axin (Hemiptera: Coccoidea: Monophlebidae). Genome Biol. Evol. 6:714-726. http://dx.doi.org/10.1093/gbe/evu049.
69. Snyder AK, McMillen CM, Wallenhorst P, Rio RV. 2011. The phylogeny of Sodalis-like symbionts as reconstructed using surface-encoding loci. FEMS Microbiol. Lett. 317:143-151. http://dx.doi.org/10.1111/j.1574- 6968.2011.02221.x.
70. Conord C, Despres L, Vallier A, Balmand S, Miquel C, Zundel S, Lemperiere G, Heddi A. 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. http://dx.doi.org/10.1093/molbev/msn027.
71. Moran NA, McLaughlin HJ, Sorek R. 2009. The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323:379-382. http://dx.doi.org/10.1126/science.1167140.
72. Rispe C, Delmotte F, van Ham RC, Moya A. 2004. Mutational and selective pressures on codon and amino acid usage in Buchnera, endosymbiotic bacteria of aphids. Genome Res. 14:44 -53. http://dx.doi.org/ 10.1101/gr.1358104.
73. Sloan DB, Nakabachi A, Richards S, Qu J, Murali SC, Gibbs RA, Moran NA. 2014. Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol. Biol. Evol. 31:857-871. http://dx.doi.org/10.1093/molbev/msu004.
74. Markowitz VM, Mavromatis K, Ivanova NN, Chen IM, Chu K, Kyrpides NC. 2009. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 25:2271-2278. http://dx.doi.org/ 10.1093/bioinformatics/btp393.
75. Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673-679. http://dx.doi.org/10.1093/bioinformatics/btm009.
76. Finn RD, Clements J, Eddy SR. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39:W29-W37. http:// dx.doi.org/10.1093/nar/gkr367.
77. Gao F, Zhang CT. 2008. Ori-finder: a web-based system for finding oriCs in unannotated bacterial genomes. BMC Bioinformatics 9:79. http:// dx.doi.org/10.1186/1471-2105-9-79.
78. Gao F, Luo H, Zhang CT. 2013. DoriC 5.0: an updated database of oriC regions in both bacterial and archaeal genomes. Nucleic Acids Res. 41: D90-D93. http://dx.doi.org/10.1093/nar/gkt090.
79. Tatusov RL, Koonin EV, Lipman DJ. 1997. A genomic perspective on protein families. Science 278:631- 637. http://dx.doi.org/10.1126/ science.278.5338.631.
80. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for comparative genomics. Genome Res. 19:1639-1645. http://dx.doi.org/10.1101/ gr.092759.109.
81. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. http:// dx.doi.org/10.1093/nar/gkh340.
82. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
83. Wang Z, Wu M. 2013. A phylum-level bacterial phylogenetic marker database. Mol. Biol. Evol. 30:1258 -1262. http://dx.doi.org/10.1093/ molbev/mst059.
84. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30:772-780. http://dx.doi.org/10.1093/molbev/mst010.
85. Darriba D, Taboada GL, Doallo R, Posada D. 2014. High-performance computing selection of models of DNA substitution for multicore clusters. Int. J. High Perform. Comput. Appl. 28:112-125. http://dx.doi.org/ 10.1177/1094342013495095.
86. Dayhoff MO, Schwartz RM, Orcutt BC. 1978. A model of evolutionary change in proteins, chapter 22, p 345-352. In Dayhoff MO (ed), Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver Spring, MD.
87. Abascal F, Zardoya R, Telford MJ. 2010. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 38:W7-W13. http://dx.doi.org/10.1093/nar/gkq291.
88. Yang Z, Nielsen R. 2000. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17:32-43. http://dx.doi.org/10.1093/oxfordjournals.molbev.a026236.