A Novel Human-Infection-Derived Bacterium Provides Insights into the Evolutionary Origins of Mutualistic Insect–Bacterial Symbioses
Despite extensive study, little is known about the origins of the mutualistic bacterial endosymbionts that inhabit approximately 10% of the world's insects. In this study, we characterized a novel opportunistic human pathogen, designated “strain HS,” and found that it is a close relative of the insect endosymbiont Sodalis glossinidius. Our results indicate that ancestral relatives of strain HS have served as progenitors for the independent descent of Sodalis-allied endosymbionts found in several insect hosts. Comparative analyses indicate that the gene inventories of the insect endosymbionts were independently derived from a common ancestral template through a combination of irreversible degenerative changes. Our results provide compelling support for the notion that mutualists evolve from pathogenic progenitors. They also elucidate the role of degenerative evolutionary processes in shaping the gene inventories of symbiotic bacteria at a very early stage in these mutualistic associations.
Vyšlo v časopise:
A Novel Human-Infection-Derived Bacterium Provides Insights into the Evolutionary Origins of Mutualistic Insect–Bacterial Symbioses. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1002990
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002990
Souhrn
Despite extensive study, little is known about the origins of the mutualistic bacterial endosymbionts that inhabit approximately 10% of the world's insects. In this study, we characterized a novel opportunistic human pathogen, designated “strain HS,” and found that it is a close relative of the insect endosymbiont Sodalis glossinidius. Our results indicate that ancestral relatives of strain HS have served as progenitors for the independent descent of Sodalis-allied endosymbionts found in several insect hosts. Comparative analyses indicate that the gene inventories of the insect endosymbionts were independently derived from a common ancestral template through a combination of irreversible degenerative changes. Our results provide compelling support for the notion that mutualists evolve from pathogenic progenitors. They also elucidate the role of degenerative evolutionary processes in shaping the gene inventories of symbiotic bacteria at a very early stage in these mutualistic associations.
Zdroje
1. AnderssonSG, KurlandCG (1998) Reductive evolution of resident genomes. Trends Microbiol 6: 263–268.
2. DaleC, MoranNA (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126: 453–465.
3. Pérez-BrocalV, GilR, RamosS, LamelasA, PostigoM, et al. (2006) A small microbial genome: the end of a long symbiotic relationship? Science 314: 312–313.
4. McCutcheonJP, MoranNA (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci U S A 104: 19392–19397.
5. NakabachiA, YamashitaA, TohH, IshikawaH, DunbarHE, et al. (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314: 267.
6. MoranNA, McCutcheonJP, NakabachiA (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165–190.
7. NovákováE, HypsaV, MoranNA (2009) Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol 9: 143.
8. SnyderAK, McMillenCM, WallenhorstP, RioRV (2011) The phylogeny of Sodalis-like symbionts as reconstructed using surface-encoding loci. FEMS Microbiol Lett 317: 143–151.
9. HuigensME, de AlmeidaRP, BoonsPA, LuckRF, Stouthamer (2004) Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc Biol Sci 271: 509–515.
10. JaenikeJ, PolakM, FiskinA, HelouM, MinhasM (2007) Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 3: 23–25.
11. MoranNA, DunbarHE (2006) Sexual acquisition of beneficial symbionts in aphids. Proc Natl Acad Sci U S A 103: 12803–12806.
12. HoffmannJA (1995) Innate immunity of insects. Curr Opin Immunol 7: 4–10.
13. PontesMH, SmithKL, De VooghtL, Van Den AbbeeleJ, DaleC (2011) Attenuation of the sensing capabilities of PhoQ in transition to obligate insect-bacterial association. PLoS Genet 7: e1002349 doi:10.1371/journal.pgen.1002349.
14. DaleC, YoungS, HaydonDT, WelburnSC (2001) The insect endosymbiont Sodalis glossinidius utilizes a type-III secretion system for cell invasion. Proc Natl Acad Sci U S A 98: 1883–1888.
15. DaleC, PlagueGR, WangB, OchmanH, MoranNA (2002) Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc Natl Acad Sci U S A 99: 12397–12402.
16. DegnanPH, YuY, SisnerosN, WingRA, MoranNA (2009) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci U S A 106: 9063–9068.
17. NovákováE, HypsaV (2007) A new Sodalis lineage from bloodsucking fly Craterina melbae (Diptera, Hippoboscoidea) originated independently of the tsetse flies symbiont Sodalis glossinidius. FEMS Microbiol Lett 269: 131–135.
18. DarbyAC, ChoiJ-H, WilkesT, HughesMA, WerrenJH, et al. (2009) Characteristics of the genome of Arsenophonus nasoniae, son-killer bacterium of the wasp Nasonia. Insect Mol Biol Suppl 1: 75–89.
19. StackebrandE, GoebelBM (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44: 846–849.
20. VerbargS, FrühlingA, CousinS, BrambillaE, GronowS, et al. (2008) Biostraticola tofi gen. nov., spec. nov., a novel member of the family Enterobacteriaceae. Curr Microbiol 56: 603–608.
21. KaiwaN, HosokawaT, KikuchiY, NikohN, MengXY, et al. (2010) Primary gut symbiont and secondary, Sodalis-allied symbiont of the Scutellerid stinkbug Cantao ocellatus. Appl Environ Microbiol 76: 3486–3494.
22. TojuH, HosokawaT, KogaR, NikohN, MengXY, et al. (2009) “Candidatus Curculioniphilus buchneri,” a novel clade of bacterial endocellular symbionts from weevils of the genus Curculio. Appl Environ Microbiol 76: 275–282.
23. TojuH, FukatsuT (2011) Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol Ecol 20: 853–868.
24. TohH, WeissBL, PerkinSA, YamashitaA, OshimaK, et al. (2006) Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16: 149–156.
25. BeldaE, MoyaA, BentleyS, SilvaFJ (2010) 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.
26. NeversP, SaedlerH (1977) Transposable genetic elements as agents of gene instability and chromosomal rearrangements. Nature 268: 109–115.
27. BickhartDM, GogartenJP, LapierreP, TisaLS, NormandP, et al. (2009) Insertion sequence content reflects genome plasticity in strains of the root nodule actinobacterium Frankia. BMC Genomics 10: 468.
28. ParkhillJ, BerryC (2003) Genomics: Relative pathogenic values. Nature 423: 23–25.
29. TampakakiAP, SkandalisN, GaziAD, BastakiMN, SarrisPF, et al. (2010) Playing the “Harp”: evolution of our understanding of hrp/hrc genes. Annu Rev Phytopathol 48: 347–370.
30. BurkeGR, MoranNA (2011) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3: 195–208.
31. McCutcheonJP, MoranNA (2011) Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10: 13–26.
32. TarchiniR, BiddleP, WinelandR, TingeyS, RafalskiA (2000) The complete sequence of 340 kb of DNA around the rice Adh1–adh2 region reveals interrupted colinearity with maize chromosome 4. Plant Cell 12: 381–391.
33. FeschotteC, MouchèsC (2000) Recent amplification of miniature inverted-repeat transposable elements in the vector mosquito Culex pipiens: characterization of the Mimo family. Gene 250: 109–116.
34. JurkaJ, KohanyO, PavlicekA, KapitonovVV, JurkaMV (2004) Duplication, coclustering, and selection of human Alu retrotransposons. Proc Natl Acad Sci U S A 101: 1268–1272.
35. TojuH, FukatsuT (2011) Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol Ecol 20: 853–868.
36. KaiwaN, HosokawaT, KikuchiY, NikohN, MengXY, et al. (2010) Primary gut symbiont and secondary, Sodalis-allied symbiont of the Scutellerid stinkbug Cantao ocellatus. Appl Environ Microbiol 76: 3486–3494.
37. GrünwaldS, PilhoferM, HöllW (2010) Microbial associations in gut systems of wood- and bark-inhabiting longhorned beetles [Coleoptera: Cerambycidae]. Syst Appl Microbiol 33: 25–34.
38. LefèvreC, CharlesH, VallierA, DelobelB, FarrellB, et al. (2004) Endosymbiont phylogenesis in the dryophthoridae weevils: evidence for bacterial replacement. Mol Biol Evol 21: 965–973.
39. ConordC, DespresL, VallierA, BalmandS, MiquelC, et al. (2008) Long-term evolutionary stability of bacterial endosymbiosis in curculionoidea: additional evidence of symbiont replacement in the dryophthoridae family. Mol Biol Evol 25: 859–868.
40. MorelliG, DidelotX, KusecekB, SchwarzS, BahlawaneC, et al. (2010) Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet 6: e1001036 doi:10.1371/journal.pgen.1001036.
41. MoranNA, McLaughlinH, SorekR (2009) The Dynamics and Time Scale of Ongoing Genomic Erosion in Symbiotic Bacteria. Science 323: 379–382.
42. GreenJ, BohannanBJ (2006) Spatial scaling of microbial diversity. Trends Ecol Evol 21: 501–507.
43. NadarasahG, StavrinidesJ (2011) Insects as alternative hosts for phytopathogenic bacteria. FEMS Microbiol Rev 35: 555–575.
44. StavrinidesJ, NoA, OchmanH (2010) A single genetic locus in the phytopathogen Pantoea stewartii enables gut colonization and pathogenicity in an insect host. Environ Microbiol 12: 147–155.
45. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
46. GuindonS, GascuelO (2001) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.
47. HasegawaM, KishinoH, YamoT (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22: 160–174.
48. MullikinJC, NingZ (2003) The phusion assembler. Genome Res 13: 81–90.
49. GordonD, AbajianC, GreenP (1998) Consed: a graphical tool for sequence finishing. Genome Res 8: 195–202.
50. RobbFT, MaederDL, BrownJR, DiRuggieroJ, StumpMD, et al. (2001) Genomic sequence of hyperthermophile, Pyrococcus furiosus: implications for physiology and enzymology. Methods Enzymol 330: 134–157.
51. BlankenbergD, Von KusterG, CoraorN, AnandaG, LazarusR, et al. (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol 19: Unit 19.10.1–21.
52. GoecksJ, NekrutenkoA, TaylorJ (2010) Galaxy Team (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86.
53. ZerbinoDR, BirneyE (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.
54. LukashinAV, BorodovskyM (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26: 1107–1115.
55. RutherfordK, ParkhillJ, CrookJ, HorsnellT, RiceP, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944–945.
56. TatusovRL, FedorovaND, JacksonJD, JacobsAR, KiryutinB, et al. (2003) The COG database: and updated version includes eukaryotes. BMC Bioinformatics 4: 41.
57. KrzywinskiM, ScheinJ, BirolI, ConnorsJ, GascoyneR, et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639–1645.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 11
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