from the Aphid : A Missing Link from Facultative to Obligate Insect Endosymbiont
The genome sequencing of Buchnera aphidicola BCc from the aphid Cinara cedri, which is the smallest known Buchnera genome, revealed that this bacterium had lost its symbiotic role, as it was not able to synthesize tryptophan and riboflavin. Moreover, the biosynthesis of tryptophan is shared with the endosymbiont Serratia symbiotica SCc, which coexists with B. aphidicola in this aphid. The whole-genome sequencing of S. symbiotica SCc reveals an endosymbiont in a stage of genome reduction that is closer to an obligate endosymbiont, such as B. aphidicola from Acyrthosiphon pisum, than to another S. symbiotica, which is a facultative endosymbiont in this aphid, and presents much less gene decay. The comparison between both S. symbiotica enables us to propose an evolutionary scenario of the transition from facultative to obligate endosymbiont. Metabolic inferences of B. aphidicola BCc and S. symbiotica SCc reveal that most of the functions carried out by B. aphidicola in A. pisum are now either conserved in B. aphidicola BCc or taken over by S. symbiotica. In addition, there are several cases of metabolic complementation giving functional stability to the whole consortium and evolutionary preservation of the actors involved.
Vyšlo v časopise:
from the Aphid : A Missing Link from Facultative to Obligate Insect Endosymbiont. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002357
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002357
Souhrn
The genome sequencing of Buchnera aphidicola BCc from the aphid Cinara cedri, which is the smallest known Buchnera genome, revealed that this bacterium had lost its symbiotic role, as it was not able to synthesize tryptophan and riboflavin. Moreover, the biosynthesis of tryptophan is shared with the endosymbiont Serratia symbiotica SCc, which coexists with B. aphidicola in this aphid. The whole-genome sequencing of S. symbiotica SCc reveals an endosymbiont in a stage of genome reduction that is closer to an obligate endosymbiont, such as B. aphidicola from Acyrthosiphon pisum, than to another S. symbiotica, which is a facultative endosymbiont in this aphid, and presents much less gene decay. The comparison between both S. symbiotica enables us to propose an evolutionary scenario of the transition from facultative to obligate endosymbiont. Metabolic inferences of B. aphidicola BCc and S. symbiotica SCc reveal that most of the functions carried out by B. aphidicola in A. pisum are now either conserved in B. aphidicola BCc or taken over by S. symbiotica. In addition, there are several cases of metabolic complementation giving functional stability to the whole consortium and evolutionary preservation of the actors involved.
Zdroje
1. MoyaAPeretoJGilRLatorreA 2008 Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9 218 229
2. MoranNAMcCutcheonJPNakabachiA 2008 Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42 165 190
3. BaumannP 2005 Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59 155 189
4. DouglasAE 1998 Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43 17 37
5. OliverKMDegnanPHBurkeGRMoranNA 2010 Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55 247 266
6. RussellJAMoranNA 2005 Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appl Environ Microbiol 71 7987 7994
7. LamelasAPérez-BrocalVGómez-ValeroLGosalbesMJMoyaA 2008 Evolution of the secondary symbiont “Candidatus Serratia symbiotica” in aphid species of the subfamily Lachninae. Appl Environ Microbiol 74 4236 4240
8. BurkeGRNormarkBBFavretCMoranNA 2009 Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae. Appl Environ Microbiol 75 5328 5335
9. MoranNARussellJAKogaRFukatsuT 2005 Evolutionary Relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl Environ Microbiol 71 3302 3310
10. DegnanPHLeonardoTECassBNHurwitzBSternD 2009 Dynamics of genome evolution in facultative symbionts of aphids. Environ Microbiol 12 2060 2069
11. DegnanPHYuYSisnerosNWingRAMoranNA 2009 Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci U S A 106 9063 9068
12. BurkeGRMoranNA 2011 Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3 195 208
13. Pérez-BrocalVGilRRamosSLamelasAPostigoM 2006 A small microbial genome: The end of a long symbiotic relationship? Science 314 312 313
14. Gómez-ValeroLSoriano-NavarroMPérez-BrocalVHeddiAMoyaA 2004 Coexistence of Wolbachia with Buchnera aphidicola and a secondary symbiont in the Aphid Cinara cedri. J Bacteriol 186 6626 6633
15. GosalbesMJLamelasAMoyaALatorreA 2008 The striking case of tryptophan provision in the cedar aphid Cinara cedri. J Bacteriol 190 6026 6029
16. ConsortiumTIAG 2010 Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8 e1000313 doi:10.1371/journal.pbio.1000313
17. WilsonACCAshtonPDCalevroFCharlesHColellaS 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. HansenAKMoranNA 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. ShigenobuSWilsonACC 2011 Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont. Cell Mol Life Sci 68 1297 1309
20. BohlinJSkjerveEUsseryDW 2008 Investigations of oligonucleotide usage variance within and between prokaryotes. PLoS Comput Biol 4 e1000057 doi:10.1371/journal.pcbi.1000057
21. BohlinJSnipenLHardySPKristoffersenaBLagesenK 2010 Analysis of intra-genomic GC conent homogeneity within prokaryotes. BMC Genomics 11 464
22. TatusovRLFedorovaNDJacksonJDJacobsARKiryutinB 2003 The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4 41
23. RamseyJSMacDonaldSJJanderGNakabachiAThomasGH 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. ShigenobuSWatanabeHHattoriMSakakiYIshikawaH 2000 Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407 81 86
25. TamasIKlassonLCanbackBNaslundAKErikssonAS 2002 50 million years of genomic stasis in endosymbiotic bacteria. Science 296 2376 2379
26. van HamRCKamerbeekJPalaciosCRausellCAbascalF 2003 Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 100 581 586
27. LamelasAGosalbesMJMoyaALatorreA 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. SilvaFJLatorreAMoyaA 2001 Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet 17 615 618
29. BeldaEMoyaABentleySSilvaFJ 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. ColeSTEiglmeierKParkhillJJamesKDThomsonNR 2001 Massive gene decay in the leprosy bacillus. Nature 409 1007 1011
31. FukatsuTNikohNKawaiRKogaR 2000 The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: homoptera). Appl Environ Microbiol 66 2748 2758
32. ChenD-QMontllorCBPurcellAH 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. MontllorCBMaxmenAPurcellAH 2002 Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27 189 195
34. RussellJAMoranNA 2006 Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc Biol Sci 273 603 610
35. GilRSilvaFJZientzEDelmotteFGonzalez-CandelasF 2003 The genome sequence of Blochmannia floridanus: Comparative analysis of reduced genomes. Proc Natl Acad Sci U S A 100 9388 9393
36. AusubelFM 1999 Short protocols in molecular biology: a compendium of methods from Current protocols in molecular biology. 44th edn New York Wiley
37. AltschulSFMaddenTLSchafferAAZhangJZhangZ 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402
38. StadenRBealKFBonfieldJK 2000 The Staden package. Methods Mol Biol 132 115 130
39. DelcherALHarmonDKasifSWhiteOSalzbergSL 1999 Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27 4636 4641
40. RutherfordKParkhillJCrookJHorsnellTRiceP 2000 Artemis: sequence visualization and annotation. Bioinformatics 16 944 945
41. LoweTMEddySR 1997 tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25 955 964
42. RegaliaMRosenbladMASamuelssonT 2002 Prediction of signal recognition particle RNA genes. Nucleic Acids Res 30 3368 3377
43. Griffiths-JonesSMoxonSMarshallMKhannaA 2005 Rfam: Annotating Non-Coding RNAs in Complete Genomes. Nucleic Acids Res 33 D121 D141, 2005
44. BatemanACoinLDurbinRFinnRDHollichV 2004 The Pfam protein families database. Nucleic Acids Res 32 D138 D141
45. MoriyaYItohMOkudaSYoshizawaACKanehisaM 2007 KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35 W182 185
46. ChangAScheerMGroteASchomburgISchomburgD 2009 BRENDA, AMENDA and FRENDA the enzyme information system: new content and tools in 2009. Nucleic Acids Res 37 D588 592
47. CaspiRFoersterHFulcherCAKaipaPKrummenackerM 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 DongenS 2000 Graph clustering by flow simulation [PhD Thesis] Utrecht, The Netherlands University of Utrecht
50. KurtzSPhillippyADelcherALSmootMShumwayM 2004 Versatile and open software for comparing large genomes. Genome Biol 5 R12
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 11
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Evidence-Based Annotation of Gene Function in MR-1 Using Genome-Wide Fitness Profiling across 121 Conditions
- De Novo Origins of Human Genes
- TRY-5 Is a Sperm-Activating Protease in Seminal Fluid
- Relative Burden of Large CNVs on a Range of Neurodevelopmental Phenotypes