#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Comparative Genomics of and the Bacterial Species Concept


The importance of host-specialization to speciation processes in obligate host-associated bacteria is well known, as is also the ability of recombination to generate cohesion in bacterial populations. However, whether divergent strains of highly recombining intracellular bacteria, such as Wolbachia, can maintain their genetic distinctness when infecting the same host is not known. We first developed a protocol for the genome sequencing of uncultivable endosymbionts. Using this method, we have sequenced the complete genomes of the Wolbachia strains wHa and wNo, which occur as natural double infections in Drosophila simulans populations on the Seychelles and in New Caledonia. Taxonomically, wHa belong to supergroup A and wNo to supergroup B. A comparative genomics study including additional strains supported the supergroup classification scheme and revealed 24 and 33 group-specific genes, putatively involved in host-adaptation processes. Recombination frequencies were high for strains of the same supergroup despite different host-preference patterns, leading to genomic cohesion. The inferred recombination fragments for strains of different supergroups were of short sizes, and the genomes of the co-infecting Wolbachia strains wHa and wNo were not more similar to each other and did not share more genes than other A- and B-group strains that infect different hosts. We conclude that Wolbachia strains of supergroup A and B represent genetically distinct clades, and that strains of different supergroups can co-exist in the same arthropod host without converging into the same species. This suggests that the supergroups are irreversibly separated and that barriers other than host-specialization are able to maintain distinct clades in recombining endosymbiont populations. Acquiring a good knowledge of the barriers to genetic exchange in Wolbachia will advance our understanding of how endosymbiont communities are constructed from vertically and horizontally transmitted genes.


Vyšlo v časopise: Comparative Genomics of and the Bacterial Species Concept. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003381
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003381

Souhrn

The importance of host-specialization to speciation processes in obligate host-associated bacteria is well known, as is also the ability of recombination to generate cohesion in bacterial populations. However, whether divergent strains of highly recombining intracellular bacteria, such as Wolbachia, can maintain their genetic distinctness when infecting the same host is not known. We first developed a protocol for the genome sequencing of uncultivable endosymbionts. Using this method, we have sequenced the complete genomes of the Wolbachia strains wHa and wNo, which occur as natural double infections in Drosophila simulans populations on the Seychelles and in New Caledonia. Taxonomically, wHa belong to supergroup A and wNo to supergroup B. A comparative genomics study including additional strains supported the supergroup classification scheme and revealed 24 and 33 group-specific genes, putatively involved in host-adaptation processes. Recombination frequencies were high for strains of the same supergroup despite different host-preference patterns, leading to genomic cohesion. The inferred recombination fragments for strains of different supergroups were of short sizes, and the genomes of the co-infecting Wolbachia strains wHa and wNo were not more similar to each other and did not share more genes than other A- and B-group strains that infect different hosts. We conclude that Wolbachia strains of supergroup A and B represent genetically distinct clades, and that strains of different supergroups can co-exist in the same arthropod host without converging into the same species. This suggests that the supergroups are irreversibly separated and that barriers other than host-specialization are able to maintain distinct clades in recombining endosymbiont populations. Acquiring a good knowledge of the barriers to genetic exchange in Wolbachia will advance our understanding of how endosymbiont communities are constructed from vertically and horizontally transmitted genes.


Zdroje

1. MiraA, Martin-CuadradoAB, D'AuriaG, Rodriguez-ValeraF (2010) The bacterial pan-genome:a new paradigm in microbiology. Int Microbiol 13: 45–57.

2. GeversD, CohanFM, LawrenceJG, SprattBG, CoenyeT, et al. (2005) Opinion: Re-evaluating prokaryotic species. Nat Rev Microbiol 3: 733–739.

3. HanageWP, FraserC, SprattBG (2005) Fuzzy species among recombinogenic bacteria. BMC Biol 3: 6.

4. AchtmanM, WagnerM (2008) Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6: 431–440.

5. WhitakerRJ (2006) Allopatric origins of microbial species. Philos Trans R Soc Lond B Biol Sci 361: 1975–1984.

6. HuntDE, DavidLA, GeversD, PreheimSP, AlmEJ, et al. (2008) Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320: 1081–1085.

7. BecraftED, CohanFM, KuhlM, JensenSI, WardDM (2011) Fine-scale distribution patterns of Synechococcus ecological diversity in microbial mats of Mushroom Spring, Yellowstone National Park. Appl Environ Microbiol 77: 7689–7697.

8. ConnorN, SikorskiJ, RooneyAP, KopacS, KoeppelAF, et al. (2010) Ecology of speciation in the genus Bacillus. Appl Environ Microbiol 76: 1349–1358.

9. Cadillo-QuirozH, DidelotX, HeldNL, HerreraA, DarlingA, et al. (2012) Patterns of gene flow define species of thermophilic Archaea. PLoS Biol 10: e1001265 doi:10.1371/journal.pbio.1001265.

10. FraserC, HanageWP, SprattBG (2007) Recombination and the nature of bacterial speciation. Science 315: 476–480.

11. FalushD, TorpdahlM, DidelotX, ConradDF, WilsonDJ, et al. (2006) Mismatch induced speciation in Salmonella: model and data. Philos Trans R Soc Lond B Biol Sci 361: 2045–2053.

12. HanageWP, SprattBG, TurnerKM, FraserC (2006) Modelling bacterial speciation. Philos Trans R Soc Lond B Biol Sci 361: 2039–2044.

13. CohanFM (2006) Towards a conceptual and operational union of bacterial systematics, ecology, and evolution. Philos Trans R Soc Lond B Biol Sci 361: 1985–1996.

14. CohanFM, KoeppelAF (2008) The origins of ecological diversity in prokaryotes. Curr Biol 18: R1024–1034.

15. WiedenbeckJ, CohanFM (2011) Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35: 957–976.

16. LuoC, WalkST, GordonDM, FeldgardenM, TiedjeJM, et al. (2011) Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci U S A 108: 7200–7205.

17. VosM, DidelotX (2009) A comparison of homologous recombination rates in bacteria and archaea. ISME J 3: 199–208.

18. VerginKL, TrippHJ, WilhelmLJ, DenverDR, RappeMS, et al. (2007) High intraspecific recombination rate in a native population of Candidatus pelagibacter ubique (SAR11). Environ Microbiol 9: 2430–2440.

19. ViklundJ, EttemaTJ, AnderssonSG (2012) Independent genome reduction and phylogenetic reclassification of the oceanic SAR11 clade. Mol Biol Evol 29: 599–615.

20. TamasI, KlassonL, CanbackB, NaslundAK, ErikssonAS, et al. (2002) 50 million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376–2379.

21. WerrenJH, BaldoL, ClarkME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741–751.

22. TaylorMJ, BandiC, HoeraufA (2005) Wolbachia bacterial endosymbionts of filarial nematodes. Adv Parasitol 60: 245–284.

23. DarbyAC, ArmstrongSD, BahGS, KaurG, HughesMA, et al. (2012) Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res

24. WeeksAR, TurelliM, HarcombeWR, ReynoldsKT, HoffmannAA (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5: e114 doi:10.1371/journal.pbio.0050114.

25. OsborneSE, LeongYS, O'NeillSL, JohnsonKN (2009) Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 5: e1000656 doi:10.1371/journal.ppat.1000656.

26. TeixeiraL, FerreiraA, AshburnerM (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6: e2 doi:10.1371/journal.pbio.0060002.

27. BrownlieJC, CassBN, RieglerM, WitsenburgJJ, Iturbe-OrmaetxeI, et al. (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5: e1000368 doi:10.1371/journal.ppat.1000368.

28. SaridakiA, BourtzisK (2010) Wolbachia: more than just a bug in insects genitals. Curr Opin Microbiol 13: 67–72.

29. AugustinosAA, Santos-GarciaD, DionyssopoulouE, MoreiraM, PapapanagiotouA, et al. (2011) Detection and characterization of Wolbachia infections in natural populations of aphids: is the hidden diversity fully unraveled? PLoS ONE 6: e28695 doi:10.1371/journal.pone.0028695.

30. WerrenJH, ZhangW, GuoLR (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Biol Sci 261: 55–63.

31. BaldoL, Dunning HotoppJC, JolleyKA, BordensteinSR, BiberSA, et al. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72: 7098–7110.

32. LoN, ParaskevopoulosC, BourtzisK, O'NeillSL, WerrenJH, et al. (2007) Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int J Syst Evol Microbiol 57: 654–657.

33. BaldoL, LoN, WerrenJH (2005) Mosaic nature of the wolbachia surface protein. J Bacteriol 187: 5406–5418.

34. BordensteinSR, WernegreenJJ (2004) Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Mol Biol Evol 21: 1981–1991.

35. Iturbe-OrmaetxeI, WoolfitM, RancesE, DuplouyA, O'NeillSL (2011) A simple protocol to obtain highly pure Wolbachia endosymbiont DNA for genome sequencing. J Microbiol Methods 84: 134–136.

36. MavinguiP, VanVT, LabeyrieE, RancesE, VavreF, et al. (2005) Efficient procedure for purification of obligate intracellular Wolbachia pipientis and representative amplification of its genome by multiple-displacement amplification. Appl Environ Microbiol 71: 6910–6917.

37. WuM, SunLV, VamathevanJ, RieglerM, DeboyR, et al. (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2: e69 doi:10.1371/journal.pbio.0020069.

38. KlassonL, WestbergJ, SapountzisP, NaslundK, LutnaesY, et al. (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci U S A 106: 5725–5730.

39. KlassonL, WalkerT, SebaihiaM, SandersMJ, QuailMA, et al. (2008) Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Mol Biol Evol 25: 1877–1887.

40. FosterJ, GanatraM, KamalI, WareJ, MakarovaK, et al. (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3: e121 doi:10.1371/journal.pbio.0030121.

41. MavinguiP, Valiente MoroC, Tran-VanV, Wisniewski-DyeF, RaquinV, et al. (2012) Whole-genome sequence of Wolbachia strain wAlbB, an endosymbiont of tiger mosquito vector Aedes albopictus. J Bacteriol 194: 1840.

42. KentBN, SalichosL, GibbonsJG, RokasA, NewtonIL, et al. (2011) Complete bacteriophage transfer in a bacterial endosymbiont (Wolbachia) determined by targeted genome capture. Genome Biol Evol 3: 209–218.

43. MercotH, CharlatS (2004) Wolbachia infections in Drosophila melanogaster and D. simulans: polymorphism and levels of cytoplasmic incompatibility. Genetica 120: 51–59.

44. JamesAC, DeanMD, McMahonME, BallardJW (2002) Dynamics of double and single Wolbachia infections in Drosophila simulans from New Caledonia. Heredity (Edinb) 88: 182–189.

45. SolignacM (2004) Mitochondrial DNA in the Drosophila melanogaster complex. Genetica 120: 41–50.

46. BallardJW (2004) Sequential evolution of a symbiont inferred from the host: Wolbachia and Drosophila simulans. Mol Biol Evol 21: 428–442.

47. DeanMD, BallardJW (2005) High divergence among Drosophila simulans mitochondrial haplogroups arose in midst of long term purifying selection. Mol Phylogenet Evol 36: 328–337.

48. GarriganD, KinganSB, GenevaAJ, AndolfattoP, ClarkAG, et al. (2012) Genome sequencing reveals complex speciation in the Drosophila simulans clade. Genome Res 22: 1499–1511.

49. AmarnehB, De Leon-RangelJ, VikSB (2006) Construction of a deletion strain and expression vector for the Escherichia coli NADH:ubiquinone oxidoreductase (Complex I). Biochim Biophys Acta 1757: 1557–1560.

50. Hovel-MinerG, FaucherSP, CharpentierX, ShumanHA (2010) ArgR-regulated genes are derepressed in the Legionella-containing vacuole. J Bacteriol 192: 4504–4516.

51. AktoriesK (2011) Bacterial protein toxins that modify host regulatory GTPases. Nat Rev Microbiol 9: 487–498.

52. YarbroughML, LiY, KinchLN, GrishinNV, BallHL, et al. (2009) AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323: 269–272.

53. WorbyCA, MattooS, KrugerRP, CorbeilLB, KollerA, et al. (2009) The fic domain: regulation of cell signaling by adenylylation. Mol Cell 34: 93–103.

54. PalaniveluDV, GoepfertA, MeuryM, GuyeP, DehioC, et al. (2011) Fic domain-catalyzed adenylylation: insight provided by the structural analysis of the type IV secretion system effector BepA. Protein Sci 20: 492–499.

55. HenrichfreiseB, SchieferA, SchneiderT, NzukouE, PoellingerC, et al. (2009) Functional conservation of the lipid II biosynthesis pathway in the cell wall-less bacteria Chlamydia and Wolbachia: why is lipid II needed? Mol Microbiol 73: 913–923.

56. Rossello-MoraR, AmannR (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25: 39–67.

57. KonstantinidisKT, TiedjeJM (2005) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 102: 2567–2572.

58. StackebrandtE, EbersJ (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiology Today 152–155.

59. CohanFM (2001) Bacterial species and speciation. Syst Biol 50: 513–524.

60. BandiC, AndersonTJ, GenchiC, BlaxterML (1998) Phylogeny of Wolbachia in filarial nematodes. Proc Biol Sci 265: 2407–2413.

61. CasiraghiM, AndersonTJ, BandiC, BazzocchiC, GenchiC (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122 Pt 1: 93–103.

62. BaldoL, BordensteinS, WernegreenJJ, WerrenJH (2006) Widespread recombination throughout Wolbachia genomes. Mol Biol Evol 23: 437–449.

63. VenetiZ, ClarkME, KarrTL, SavakisC, BourtzisK (2004) Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl Environ Microbiol 70: 5366–5372.

64. GottliebY, GhanimM, GueguenG, KontsedalovS, VavreF, et al. (2008) Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J 22: 2591–2599.

65. RussellJA, Goldman-HuertasB, MoreauCS, BaldoL, StahlhutJK, et al. (2009) Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Evolution 63: 624–640.

66. StahlhutJK, DesjardinsCA, ClarkME, BaldoL, RussellJA, et al. (2010) The mushroom habitat as an ecological arena for global exchange of Wolbachia. Mol Ecol 19: 1940–1952.

67. BaldoL, AyoubNA, HayashiCY, RussellJA, StahlhutJK, et al. (2008) Insight into the routes of Wolbachia invasion: high levels of horizontal transfer in the spider genus Agelenopsis revealed by Wolbachia strain and mitochondrial DNA diversity. Mol Ecol 17: 557–569.

68. JigginsFM, BentleyJK, MajerusME, HurstGD (2002) Recent changes in phenotype and patterns of host specialization in Wolbachia bacteria. Mol Ecol 11: 1275–1283.

69. DenamurE, LecointreG, DarluP, TenaillonO, AcquavivaC, et al. (2000) Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell 103: 711–721.

70. CohanFM, AracenaS (2012) Prokaryotic Sex: Eukaryote-like Qualities of Recombination in an Archaean Lineage. Current Biology 22: R601–R602.

71. FariaR, NavarroA (2010) Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25: 660–669.

72. RetchlessAC, LawrenceJG (2007) Temporal fragmentation of speciation in bacteria. Science 317: 1093–1096.

73. CohanFM, PerryEB (2007) A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17: R373–386.

74. MillerWJ, EhrmanL, SchneiderD (2010) Infectious speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum. PLoS Pathog 6: e1001214 doi:10.1371/journal.ppat.1001214.

75. BordensteinSR, O'HaraFP, WerrenJH (2001) Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409: 707–710.

76. WagnerA, LewisC, BichselM (2007) A survey of bacterial insertion sequences using IScan. Nucleic Acids Research 35: 5284–5293.

77. CerveauN, LeclercqS, LeroyE, BouchonD, CordauxR (2011) Short- and long-term evolutionary dynamics of bacterial insertion sequences: insights from Wolbachia endosymbionts. Genome Biol Evol 3: 1175–1186.

78. MercotH, LlorenteB, JacquesM, AtlanA, Montchamp-MoreauC (1995) Variability within the Seychelles cytoplasmic incompatibility system in Drosophila simulans. Genetics 141: 1015–1023.

79. O'NeillSL, KarrTL (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348: 178–180.

80. Chevreux B, Wetter T., Suhai S (1999) Genome Sequence Assembly Using Trace Signals and Additional Sequence Information. Computer Science and Biology: Proceedings of the German Conference on Bioinformatics (GCB) 99. pp. 44–56.

81. DarlingAE, MauB, PernaNT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5: e11147 doi:10.1371/journal.pone.0011147.

82. CarverTJ, RutherfordKM, BerrimanM, RajandreamMA, BarrellBG, et al. (2005) ACT: the Artemis Comparison Tool. Bioinformatics 21: 3422–3423.

83. GordonD, AbajianC, GreenP (1998) Consed: a graphical tool for sequence finishing. Genome Res 8: 195–202.

84. LohseM, BolgerAM, NagelA, FernieAR, LunnJE, et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 40: W622–627.

85. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.

86. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.

87. SchmiederR, EdwardsR (2011) Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS ONE 6: e17288 doi:10.1371/journal.pone.0017288.

88. StewartAC, OsborneB, ReadTD (2009) DIYA: a bacterial annotation pipeline for any genomics lab. Bioinformatics 25: 962–963.

89. HyattD, ChenGL, LocascioPF, LandML, LarimerFW, et al. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.

90. PatiA, IvanovaNN, MikhailovaN, OvchinnikovaG, HooperSD, et al. (2010) GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes. Nat Methods 7: 455–457.

91. BatemanA, BirneyE, CerrutiL, DurbinR, EtwillerL, et al. (2002) The Pfam protein families database. Nucleic Acids Res 30: 276–280.

92. RutherfordK, ParkhillJ, CrookJ, HorsnellT, RiceP, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944–945.

93. GuyL, KultimaJR, AnderssonSG (2010) genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26: 2334–2335.

94. SiguierP, PerochonJ, LestradeL, MahillonJ, ChandlerM (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34: D32–36.

95. LiL, StoeckertCJJr, RoosDS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189.

96. KatohK, MisawaK, KumaK, MiyataT (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059–3066.

97. StamatakisA (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.

98. YangZ (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.

99. BruenTC, PhilippeH, BryantD (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172: 2665–2681.

100. PadidamM, SawyerS, FauquetCM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265: 218–225.

101. DidelotX, FalushD (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175: 1251–1266.

102. MattooS, DurrantE, ChenMJ, XiaoJ, LazarCS, et al. (2011) Comparative analysis of Histophilus somni immunoglobulin-binding protein A (IbpA) with other fic domain-containing enzymes reveals differences in substrate and nucleotide specificities. J Biol Chem 286: 32834–32842.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#