Serratia symbiotica from the aphid Cinara cedri: A missing link from facultative to obligate insect endosymbiont

PLoS Genetics

Volumn 7, Issue 11, 2011, Pages

  Lamelas, Araceli ^a,b   Gosalbes, María José ^a   Manzano Marín, Alejandro ^a   Peretó, Juli ^a   Moya, Andrés ^a   Latorre, Amparo ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

RIBOFLAVIN; TRYPTOPHAN; AMINO ACID; BACTERIAL PROTEIN;

ACYRTHOSIPHON PISUM; APHID; ARTICLE; BACTERIAL METABOLISM; BUCHNERA APHIDICOLA; CINARA CEDRI; CONTROLLED STUDY; ENDOSYMBIONT; GENE SEQUENCE; GENETIC CONSERVATION; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; SERRATIA; SERRATIA SYMBIOTICA; TRYPTOPHAN METABOLISM; ANIMAL; BACTERIAL GENOME; BIOSYNTHESIS; BUCHNERA; CLASSIFICATION; ENTEROBACTERIACEAE; EVOLUTION; GENETICS; METABOLISM; MICROBIOLOGY; PHYLOGENY; PSEUDOGENE; SYMBIOSIS;

ACYRTHOSIPHON PISUM; APHIDIDAE; BACTERIA (MICROORGANISMS); BUCHNERA (PROTEOBACTERIA); BUCHNERA APHIDICOLA; CANDIDATUS SERRATIA SYMBIOTICA; CINARA CEDRI; HEXAPODA;

AMINO ACIDS; ANIMALS; APHIDS; BACTERIAL PROTEINS; BIOLOGICAL EVOLUTION; BUCHNERA; ENTEROBACTERIACEAE; GENOME, BACTERIAL; METABOLIC NETWORKS AND PATHWAYS; PHYLOGENY; PSEUDOGENES; RIBOFLAVIN; SERRATIA; SYMBIOSIS; TRYPTOPHAN;

EID: 81755163088     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002357     Document Type: Article

References (50)

1. 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.
2. Moran NA, McCutcheon JP, Nakabachi A, (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190.
3. Baumann P, (2005) Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59: 155-189.
4. Douglas AE, (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43: 17-37.
5. Oliver KM, Degnan PH, Burke GR, Moran NA, (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55: 247-266.
6. Russell JA, Moran NA, (2005) Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appl Environ Microbiol 71: 7987-7994.
7. Lamelas A, Pérez-Brocal V, Gómez-Valero L, Gosalbes MJ, Moya A, et al. (2008) Evolution of the secondary symbiont "Candidatus Serratia symbiotica" in aphid species of the subfamily Lachninae. Appl Environ Microbiol 74: 4236-4240.
8. Burke GR, Normark BB, Favret C, Moran NA, (2009) Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae. Appl Environ Microbiol 75: 5328-5335.
9. Moran NA, Russell JA, Koga R, Fukatsu T, (2005) Evolutionary Relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl Environ Microbiol 71: 3302-3310.
10. Degnan PH, Leonardo TE, Cass BN, Hurwitz B, Stern D, et al. (2009) Dynamics of genome evolution in facultative symbionts of aphids. Environ Microbiol 12: 2060-2069.
11. Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA, (2009) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci U S A 106: 9063-9068.
12. Burke GR, Moran NA, (2011) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3: 195-208.
13. Pérez-Brocal V, Gil R, Ramos S, Lamelas A, Postigo M, et al. (2006) A small microbial genome: The end of a long symbiotic relationship? Science 314: 312-313.
14. Gómez-Valero L, Soriano-Navarro M, Pérez-Brocal V, Heddi A, Moya A, et al. (2004) Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the Aphid Cinara cedri. J Bacteriol 186: 6626-6633.
15. Gosalbes MJ, Lamelas A, Moya A, Latorre A, (2008) The striking case of tryptophan provision in the cedar aphid Cinara cedri. J Bacteriol 190: 6026-6029.
16. Consortium TIAG, (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8: e1000313 doi:10.1371/journal.pbio.1000313.
17. Wilson ACC, Ashton PD, Calevro F, Charles H, Colella S, et al. (2010) Genomic insight into the amino acid relations of the pea aphid Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol 19: 249-258.
18. Hansen AK, Moran NA, (2011) Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proc Natl Acad Sci U S A 108: 2849-2854.
19. Shigenobu S, Wilson ACC, (2011) Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont. Cell Mol Life Sci 68: 1297-1309.
20. Bohlin J, Skjerve E, Ussery DW, (2008) Investigations of oligonucleotide usage variance within and between prokaryotes. PLoS Comput Biol 4: e1000057 doi:10.1371/journal.pcbi.1000057.
21. Bohlin J, Snipen L, Hardy SP, Kristoffersen aB, Lagesen K, et al. (2010) Analysis of intra-genomic GC conent homogeneity within prokaryotes. BMC Genomics 11: 464.
22. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
23. Ramsey JS, MacDonald SJ, Jander G, Nakabachi A, Thomas GH, et al. (2010) Genomic evidence for complementary purine metabolism in the pea aphid, Acyrthosiphon pisum, and its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol 19 (Suppl 2): 241-248.
24. 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.
25. Tamas I, Klasson L, Canback B, Naslund AK, Eriksson AS, et al. (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376-2379.
26. van Ham RC, Kamerbeek J, Palacios C, Rausell C, Abascal F, et al. (2003) Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 100: 581-586.
27. Lamelas A, Gosalbes MJ, Moya A, Latorre A, (2011) New clues about the evolutionary history of metabolic losses in bacterial endosymbionts, provided by the genome of Buchnera aphidicola from the aphid Cinara tujafilina. Appl Environ Microbiol 77: 4446-4454.
28. Silva FJ, Latorre A, Moya A, (2001) Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet 17: 615-618.
29. Belda E, Moya A, Bentley S, Silva FJ, 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.
30. Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, et al. (2001) Massive gene decay in the leprosy bacillus. Nature 409: 1007-1011.
31. Fukatsu T, Nikoh N, Kawai R, Koga R, (2000) The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: homoptera). Appl Environ Microbiol 66: 2748-2758.
32. Chen D-Q, Montllor CB, Purcell AH, (2000) Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol Exp Appl 95: 315-323.
33. Montllor CB, Maxmen A, Purcell AH, (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27: 189-195.
34. Russell JA, Moran NA, (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc Biol Sci 273: 603-610.
35. Gil R, Silva FJ, Zientz E, Delmotte F, Gonzalez-Candelas F, et al. (2003) The genome sequence of Blochmannia floridanus: Comparative analysis of reduced genomes. Proc Natl Acad Sci U S A 100: 9388-9393.
36. Ausubel FM, (1999) Short protocols in molecular biology: a compendium of methods from Current protocols in molecular biology. 44th edn New York Wiley.
37. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
38. Staden R, Beal KF, Bonfield JK, (2000) The Staden package. Methods Mol Biol 132: 115-130.
39. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL, (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27: 4636-4641.
40. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
41. Lowe TM, Eddy SR, (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
42. Regalia M, Rosenblad MA, Samuelsson T, (2002) Prediction of signal recognition particle RNA genes. Nucleic Acids Res 30: 3368-3377.
43. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, et al. (2005) Rfam: Annotating Non-Coding RNAs in Complete Genomes. Nucleic Acids Res 33: D121-D141, 2005.
44. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, et al. (2004) The Pfam protein families database. Nucleic Acids Res 32: D138-D141.
45. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M, (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: W182-185.
46. Chang A, Scheer M, Grote A, Schomburg I, Schomburg D, (2009) BRENDA, AMENDA and FRENDA the enzyme information system: new content and tools in 2009. Nucleic Acids Res 37: D588-592.
47. Caspi R, Foerster H, Fulcher CA, Kaipa P, Krummenacker M, et al. (2008) The MetaCyc Database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res 36: D623-631.
48. RDC-Team (2010) R: A language for statistical computing. R Foundation For Statistical Computing, Vienna, Austria, 2.11.1.
49. Van Dongen S, (2000) Graph clustering by flow simulation [PhD Thesis] Utrecht, The Netherlands University of Utrecht.
50. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12.