Wolbachia genome integrated in an insect chromosome: evolution and fate of laterally transferred endosymbiont genes.

Naruo Nikoh, Kohjiro Tanaka, Fukashi Shibata, Natsuko Kondo, Masahiro Hizume, Masakazu Shimada, Takema Fukatsu
Author Information
  1. Naruo Nikoh: Division of Natural Sciences, The University of the Air, Chiba 261-8586, Japan.

Abstract

Recent accumulation of microbial genome data has demonstrated that lateral gene transfers constitute an important and universal evolutionary process in prokaryotes, while those in multicellular eukaryotes are still regarded as unusual, except for endosymbiotic gene transfers from mitochondria and plastids. Here we thoroughly investigated the bacterial genes derived from a Wolbachia endosymbiont on the nuclear genome of the beetle Callosobruchus chinensis. Exhaustive PCR detection and Southern blot analysis suggested that approximately 30% of Wolbachia genes, in terms of the gene repertoire of wMel, are present on the insect nuclear genome. Fluorescent in situ hybridization located the transferred genes on the proximal region of the basal short arm of the X chromosome. Molecular evolutionary and other lines of evidence indicated that the transferred genes are probably derived from a single lateral transfer event. The transferred genes were, for the length examined, structurally disrupted, freed from functional constraints, and transcriptionally inactive. Hence, most, if not all, of the transferred genes have been pseudogenized. Notwithstanding this, the transferred genes were ubiquitously detected from Japanese and Taiwanese populations of C. chinensis, while the number of the transferred genes detected differed between the populations. The transferred genes were not detected from congenic beetle species, indicating that the transfer event occurred after speciation of C. chinensis, which was estimated to be one or several million years ago. These features of the laterally transferred endosymbiont genes are compared with the evolutionary patterns of mitochondrial and plastid genome fragments acquired by nuclear genomes through recent endosymbiotic gene transfers.

References

  1. Annu Rev Microbiol. 2001;55:709-42 [PMID: 11544372]
  2. PLoS Pathog. 2006 Oct;2(10):e94 [PMID: 17040125]
  3. Cell Mol Life Sci. 2005 Jun;62(11):1182-97 [PMID: 15761667]
  4. Genome Res. 2002 Jun;12(6):885-93 [PMID: 12045142]
  5. J Mol Evol. 2003 Feb;56(2):169-74 [PMID: 12574863]
  6. Appl Environ Microbiol. 2004 Sep;70(9):5366-72 [PMID: 15345422]
  7. Nat Rev Genet. 2003 Feb;4(2):121-32 [PMID: 12560809]
  8. Mol Ecol. 2002 Feb;11(2):167-80 [PMID: 11856419]
  9. Plant Physiol. 2002 Jul;129(3):957-66 [PMID: 12114552]
  10. Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14280-5 [PMID: 12386340]
  11. Science. 1992 Apr 3;256(5053):89-92 [PMID: 1566060]
  12. BMC Evol Biol. 2004 Jan 28;4:2 [PMID: 15005799]
  13. Nature. 2000 May 18;405(6784):299-304 [PMID: 10830951]
  14. Trends Genet. 1998 Aug;14(8):307-11 [PMID: 9724962]
  15. Proc Biol Sci. 2000 Jul 7;267(1450):1277-85 [PMID: 10972121]
  16. J Mol Evol. 1980 Sep;16(1):23-36 [PMID: 6449605]
  17. PLoS Biol. 2005 Apr;3(4):e121 [PMID: 15780005]
  18. PLoS Biol. 2004 Mar;2(3):E69 [PMID: 15024419]
  19. Science. 2007 Sep 21;317(5845):1753-6 [PMID: 17761848]
  20. Nat Rev Genet. 2004 Feb;5(2):123-35 [PMID: 14735123]
  21. Bioinformatics. 2002 Mar;18(3):502-4 [PMID: 11934758]
  22. Brief Bioinform. 2004 Jun;5(2):150-63 [PMID: 15260895]
  23. Bioessays. 2003 Mar;25(3):259-65 [PMID: 12596230]
  24. Bull Entomol Res. 2004 Feb;94(1):75-80 [PMID: 14972052]
  25. Bioinformatics. 2003 Aug 12;19(12):1572-4 [PMID: 12912839]
  26. J Eukaryot Microbiol. 1999 Jul-Aug;46(4):320-6 [PMID: 10461380]
  27. Genes Genet Syst. 1999 Aug;74(4):117-27 [PMID: 10650839]
  28. Trends Genet. 2003 Jan;19(1):47-56 [PMID: 12493248]
  29. Genomics. 2002 Jul;80(1):71-7 [PMID: 12079285]
  30. Trends Ecol Evol. 2001 Jun 1;16(6):314-321 [PMID: 11369110]
  31. Appl Environ Microbiol. 2007 Jul;73(13):4332-41 [PMID: 17496135]
  32. Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 [PMID: 7984417]

MeSH Term

Animals
Base Sequence
Blotting, Southern
Chromosome Mapping
Chromosomes
Coleoptera
Evolution, Molecular
Gene Transfer, Horizontal
Genome
In Situ Hybridization, Fluorescence
Likelihood Functions
Models, Genetic
Molecular Sequence Data
Phylogeny
Polymerase Chain Reaction
Polymorphism, Genetic
Pseudogenes
Reverse Transcriptase Polymerase Chain Reaction
Sequence Analysis, DNA
Symbiosis
Wolbachia

Word Cloud

Created with Highcharts 10.0.0genestransferredgenomegenetransfersevolutionaryWolbachiaendosymbiontnuclearchinensisdetectedlateralendosymbioticderivedbeetleinsecttransfereventpopulationsClaterallyRecentaccumulationmicrobialdatademonstratedconstituteimportantuniversalprocessprokaryotesmulticellulareukaryotesstillregardedunusualexceptmitochondriaplastidsthoroughlyinvestigatedbacterialCallosobruchusExhaustivePCRdetectionSouthernblotanalysissuggestedapproximately30%termsrepertoirewMelpresentFluorescentsituhybridizationlocatedproximalregionbasalshortarmXchromosomeMolecularlinesevidenceindicatedprobablysinglelengthexaminedstructurallydisruptedfreedfunctionalconstraintstranscriptionallyinactiveHencepseudogenizedNotwithstandingubiquitouslyJapaneseTaiwanesenumberdifferedcongenicspeciesindicatingoccurredspeciationestimatedoneseveralmillionyearsagofeaturescomparedpatternsmitochondrialplastidfragmentsacquiredgenomesrecentintegratedchromosome:evolutionfate

Similar Articles

Cited By