Purifying selection and molecular adaptation in the genome of Verminephrobacter, the heritable symbiotic bacteria of earthworms

Genome Biology and Evolution

Volumn 4, Issue 3, 2012, Pages 307-315

  Kjeldsen, Kasper U ^a   Bataillon, Thomas ^a   Pinel, Nicolás ^b   De Mita, Stéphane ^c   Lund, Marie B ^a   Panitz, Frank ^a   Bendixen, Christian ^a   Stahl, David A ^b   Schramm, Andreas ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF WASHINGTON   (United States)

^c INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Evolution; Extracellular symbiont; Genome reduction; Nonsynonymous substitutions; Positive selection; Purifying selection; Symbiosis

Indexed keywords

ACIDOVORAX; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA;

ANIMAL; ARTICLE; BACTERIAL GENOME; COMAMONADACEAE; GENETICS; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; OLIGOCHAETA; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; COMAMONADACEAE; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; OLIGOCHAETA; SYMBIOSIS;

EID: 84863191156     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evs014     Document Type: Article

References (47)

1. Adin DM, Engle JT, Goldman WE, McFall-Ngai MJ, Stabb EV. 2009. Mutations in ampG and lytic transglycosylase genes affect the net release of peptidoglycan monomers from Vibrio fischeri. J Bacteriol. 191:2012-2022.
2. AdinDM,et al.2008.Characterization of htrB andmsbBmutants of the light organ symbiont Vibrio fischeri. Appl Environ Microbiol. 74:633-644.
3. Alm E, Huang K, Arkin A. 2006. The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLoS Comput Biol. 2:e143.
4. Altura MA, Stabb E, Goldman W, Apicella M, McFall-Ngai MJ. 2011. Attenuation of host NO production by MAMPs potentiates development of the host in the squid-vibrio symbiosis. Cell Microbiol. 13:527-537.
5. Andersson SG, Kurland CG. 1998. Reductive evolution of resident genomes. Trends Microbiol. 6:263-268.
6. Bright M, Bulgheresi S. 2010. A complex journey: transmission of microbial symbionts. Nat Rev Microbiol. 8:218-230.
7. Chen SL, et al. 2006. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci U S A. 103:5977-5982.
8. Cloud-Hansen KA, et al. 2006. Breaching the great wall: peptidoglycan and microbial interactions. Nat Rev Microbiol. 4:710-716.
9. Davidson SK, Stahl DA. 2006. Transmission of nephridial bacteria of the earthworm Eisenia fetida. Appl Environ Microbiol. 72:769-775.
10. Davidson SK, Stahl DA. 2008. Selective recruitment of bacteria during embryogenesis of an earthworm. ISME J. 2:510-518.
11. Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673-679.
12. Dubilier N, Bergin C, Lott C. 2008. Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol. 6:725-740.
13. Felsenstein J. 1974. The evolutionary advantage of recombination. Genetics 78:737-756.
14. Fitzpatrick DA, Creevey CJ, McInerney JO. 2005. Evidence of positive Darwinian selection in putative meningococcal vaccine antigens. J Mol Evol. 61:90-98.
15. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
16. Hershberg R, Petrov DA. 2008. Selection on codon bias. Annu Rev Genet. 42:287-299.
17. Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T. 2006. Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol. 4:e337.
18. Kikuchi Y, et al. 2009. Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol. 7:2.
19. Kuo CH, Moran NA, Ochman H. 2009. The consequences of genetic drift for bacterial genome complexity. Genome Res. 19: 1450-1454.
20. Kuwahara H, et al. 2008. Reductive genome evolution in chemoautotrophic intracellular symbionts of deep-sea Calyptogena clams. Extremophiles 12:365-374.
21. Lund MB, et al. 2010. Diversity and host specificity of the Verminephrobacter-earthworm symbiosis. Environ Microbiol. 12: 2142-2151.
22. Lund MB, Holmstrup M, Lomstein BA, Damgaard C, Schramm A. 2010. Beneficial effect of Verminephrobacter nephridial symbionts on the fitness of the earthworm Aporrectodea tuberculata. Appl Environ Microbiol. 76:4738-4743.
23. Lund MB, Schätzle S, Schramm A, Kjeldsen KU. 2012. Verminephrobacter aporrectodeae sp. nov. subsp. tuberculatae and subsp. caliginosae; the specific nephridial symbionts of the earthworms Aporrectodea tuberculata and A. caliginosa. Antonie Van Leeuwenhoek. 101:507-514.
24. Marchler-Bauer A, et al. 2002. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res. 30:281-283.
25. Moran NA. 1996. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 93:2873-2878.
26. Moran NA, McCutcheon JP, Nakabachi A. 2008. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet. 42:165-190.
27. Moran NA, McLaughlin HJ, Sorek R. 2009. The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323: 379-382.
28. Moya A, Pereto J, Gil R, Latorre A. 2008. Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet. 9:218-229.
29. Novembre JA. 2002. Accounting for background nucleotide composition when measuring codon usage bias. Mol Biol Evol. 19:1390-1394.
30. Novichkov PS, Wolf YI, Dubchak I, Koonin EV. 2009. Trends in prokaryotic evolution revealed by comparison of closely related bacterial and archaeal genomes. J Bacteriol. 191:65-73.
31. Pandazis G. 1931. Zur Frage der Bakteriensymbiose bei Oligochaeten. Zentralbl Bakteriol. 120:440-453.
32. Pérez-Brocal V, Gil R, Moya A, Latorre A. 2011. New insights on the evolutionary history of aphids and their primary endosymbiont Buchnera aphidicola. Int J Evol Biol. 2011:250154.
33. Pinel N. 2009. Physiological and genomic insights into the biology of Verminephrobacter eiseniae, a bacterial symbiont of the earthworm Eisenia fetida [PhD dissertation]. [Seattle (WA)]: University of Washington.
34. Pinel N, Davidson SK, Stahl DA. 2008. Verminephrobacter eiseniae gen. nov., sp. nov., a nephridial symbiont of the earthworm Eisenia foetida (Savigny). Int J Syst Evol Microbiol. 58:2147-2157.
35. Pruitt KD, Tatusova T, Maglott DR. 2007. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35:D61-D65.
36. Schramm A, et al. 2003. Acidovorax-like symbionts in the nephridia of earthworms. Environ Microbiol. 5:804-809.
37. SoyerY, OrsiRH, Rodriguez-RiveraLD, Sun Q,WiedmannM.2009.Genome wide evolutionary analyses reveal serotype specific patterns of positive selection in selected Salmonella serotypes. BMC Evol Biol. 9:264.
38. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A. 100:9440-9445.
39. Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34:W609-W612.
40. Tatusov RL, et al. 2001. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res. 29:22-28.
41. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
42. Toft C, Andersson SG. 2010. Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet. 11:465-475.
43. Toft C, Williams TA, Fares MA. 2009. Genome-wide functional divergence after the symbiosis of proteobacteria with insects unraveled through a novel computational approach. PLoS Comput Biol. 5:e1000344.
44. Woyke T, et al. 2006. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443:950-955.
45. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24:1586-1591.
46. Zdobnov EM, Apweiler R. 2001. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847-848.
47. Zhang J, Nielsen R, Yang Z. 2005. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol. 22:2472-2479.