1887

Abstract

Using microarray-based comparative genome hybridization (mCGH), the genomic content of Mel from was compared to the closely related from (Inn), (San), and three strains from (Au, Ri, Sim). A large number of auxiliary genes are identified in these five strains, with most absent/divergent genes being unique to a given strain. Each strain caused an average of ∼60 genes to be removed from the core genome. As such, these organisms do not appear to have the streamlined genomes expected of obligate intracellular bacteria. Prophage, hypothetical and ankyrin repeat genes are over-represented in the absent/divergent genes, with 21–87 % of absent/divergent genes coming from prophage regions. The only Mel region absent/divergent in all five query strains is that containing WD_0509 to WD_0511, including a DNA mismatch repair protein MutL-2, a degenerate RNase, and a conserved hypothetical protein. A region flanked by the two portions of the WO-B prophage in Mel is found in four of the five strains as well as on a plasmid of a rickettsial endosymbiont of , suggesting lateral gene transfer between these two obligate intracellular species. Overall, these insect-associated have highly mosaic genomes, with lateral gene transfer playing an important role in their diversity and evolution.

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2009-07-01
2019-11-16
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References

  1. Alsmark, C. M., Frank, A. C., Karlberg, E. O., Legault, B. A., Ardell, D. H., Canbäck, B., Eriksson, A. S., Näslund, A. K., Handley, S. A. & other authors ( 2004; ). The louse-borne human pathogen Bartonella quintana is a genomic derivative of the zoonotic agent Bartonella henselae. Proc Natl Acad Sci U S A 101, 9716–9721.[CrossRef]
    [Google Scholar]
  2. Arca, B., Lombardo, F., Valenzuela, J. G., Francischetti, I. M., Marinotti, O., Coluzzi, M. & Ribeiro, J. M. ( 2005; ). An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J Exp Biol 208, 3971–3986.[CrossRef]
    [Google Scholar]
  3. Baldo, L., Bordenstein, S., Wernegreen, J. J. & Werren, J. H. ( 2006a; ). Widespread recombination throughout Wolbachia genomes. Mol Biol Evol 23, 437–449.
    [Google Scholar]
  4. Baldo, L., Dunning Hotopp, J. C., Jolley, K. A., Bordenstein, S. R., Biber, S. A., Choudhury, R. R., Hayashi, C., Maiden, M. C., Tettelin, H. & Werren, J. H. ( 2006b; ). Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72, 7098–7110.[CrossRef]
    [Google Scholar]
  5. Behr, M. A., Wilson, M. A., Gill, W. P., Salamon, H., Schoolnik, G. K., Rane, S. & Small, P. M. ( 1999; ). Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284, 1520–1523.[CrossRef]
    [Google Scholar]
  6. Benson, M. J., Gawronski, J. D., Eveleigh, D. E. & Benson, D. R. ( 2004; ). Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellfleet, Cape Cod, Massachusetts. Appl Environ Microbiol 70, 616–620.[CrossRef]
    [Google Scholar]
  7. Bordenstein, S. R. & Reznikoff, W. S. ( 2005; ). Mobile DNA in obligate intracellular bacteria. Nat Rev Microbiol 3, 688–699.[CrossRef]
    [Google Scholar]
  8. Bordenstein, S. & Rosengaus, R. B. ( 2005; ). Discovery of a novel Wolbachia supergroup in Isoptera. Curr Microbiol 51, 393–398.[CrossRef]
    [Google Scholar]
  9. Bordenstein, S. R. & Wernegreen, J. J. ( 2004; ). Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Mol Biol Evol 21, 1981–1991.[CrossRef]
    [Google Scholar]
  10. Bordenstein, S. R., Paraskevopoulos, C., Dunning Hotopp, J. C., Sapountzis, P., Lo, N., Bandi, C., Tettelin, H., Werren, J. H. & Bourtzis, K. ( 2008; ). Parasitism and mutualism in Wolbachia: what the phylogenomic trees can and can not say. Mol Biol Evol 26, 231–241.[CrossRef]
    [Google Scholar]
  11. Boucher, Y., Nesbo, C. L. & Doolittle, W. F. ( 2001; ). Microbial genomes: dealing with diversity. Curr Opin Microbiol 4, 285–289.[CrossRef]
    [Google Scholar]
  12. Bouchon, D., Rigaud, T. & Juchault, P. ( 1998; ). Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc Biol Sci 265, 1081–1090.[CrossRef]
    [Google Scholar]
  13. Casiraghi, M., Favia, G., Cancrini, G., Bartoloni, A. & Bandi, C. ( 2001; ). Molecular identification of Wolbachia from the filarial nematode Mansonella ozzardi. Parasitol Res 87, 417–420.[CrossRef]
    [Google Scholar]
  14. Casiraghi, M., Bain, O., Guerrero, R., Martin, C., Pocacqua, V., Gardner, S. L., Franceschi, A. & Bandi, C. ( 2004; ). Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. Int J Parasitol 34, 191–203.[CrossRef]
    [Google Scholar]
  15. Casiraghi, M., Bordenstein, S. R., Baldo, L., Lo, N., Beninati, T., Wernegreen, J. J., Werren, J. H. & Bandi, C. ( 2005; ). Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiology 151, 4015–4022.[CrossRef]
    [Google Scholar]
  16. Caturegli, P., Asanovich, K. M., Walls, J. J., Bakken, J. S., Madigan, J. E., Popov, V. L. & Dumler, J. S. ( 2000; ). ankA: an Ehrlichia phagocytophila group gene encoding a cytoplasmic protein antigen with ankyrin repeats. Infect Immun 68, 5277–5283.[CrossRef]
    [Google Scholar]
  17. Czarnetzki, A. B. & Tebbe, C. C. ( 2004; ). Detection and phylogenetic analysis of Wolbachia in Collembola. Environ Microbiol 6, 35–44.
    [Google Scholar]
  18. Dobson, S. L., Marsland, E. J. & Rattanadechakul, W. ( 2002; ). Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160, 1087–1094.
    [Google Scholar]
  19. Dumler, J. S., Barbet, A. F., Bekker, C. P., Dasch, G. A., Palmer, G. H., Ray, S. C., Rikihisa, Y. & Rurangirwa, F. R. ( 2001; ). Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol 51, 2145–2165.[CrossRef]
    [Google Scholar]
  20. Dunning Hotopp, J. C., Grifantini, R., Kumar, N., Tzeng, Y. L., Fouts, D., Frigimelica, E., Draghi, M., Giuliani, M. M., Rappuoli, R. & other authors ( 2006a; ). Comparative genomics of Neisseria meningitidis: core genome, islands of horizontal transfer and pathogen-specific genes. Microbiology 152, 3733–3749.[CrossRef]
    [Google Scholar]
  21. Dunning Hotopp, J. C., Lin, M., Madupu, R., Crabtree, J., Angiuoli, S. V., Eisen, J. A., Seshadri, R., Ren, Q., Wu, M. & other authors ( 2006b; ). Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2, e21 [CrossRef]
    [Google Scholar]
  22. Dunning Hotopp, J. C., Clark, M. E., Oliveira, D. C., Foster, J. M., Fischer, P., Torres, M. C., Giebel, J. D., Kumar, N., Ishmael, N. & other authors ( 2007; ). Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753–1756.[CrossRef]
    [Google Scholar]
  23. Dyer, K. A. & Jaenike, J. ( 2005; ). Evolutionary dynamics of a spatially structured host-parasite association: Drosophila innubila and male-killing Wolbachia. Evolution 59, 1518–1528.[CrossRef]
    [Google Scholar]
  24. Foster, J., Ganatra, M., Kamal, I., Ware, J., Makarova, K., Ivanova, N., Bhattacharyya, A., Kapatral, V., Kumar, S. & other authors ( 2005; ). The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3, e121 [CrossRef]
    [Google Scholar]
  25. Heath, B. D., Butcher, R. D., Whitfield, W. G. & Hubbard, S. F. ( 1999; ). Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9, 313–316.[CrossRef]
    [Google Scholar]
  26. Hedges, L. M., Brownlie, J. C., O'Neill, S. L. & Johnson, K. N. ( 2008; ). Wolbachia and virus protection in insects. Science 322, 702 [CrossRef]
    [Google Scholar]
  27. Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A. & Werren, J. H. ( 2008; ). How many species are infected with Wolbachia? – A statistical analysis of current data. FEMS Microbiol Lett 281, 215–220.[CrossRef]
    [Google Scholar]
  28. Hoffmann, A. A., Turelli, M. & Simmons, G. M. ( 1986; ). Unidirectional incompatibility between populations of Drosophila simulans. Evolution 40, 692–701.[CrossRef]
    [Google Scholar]
  29. Hoffmann, A. A., Clancy, D. & Duncan, J. ( 1996; ). Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity 76, 1–8.[CrossRef]
    [Google Scholar]
  30. Hogg, J. S., Hu, F. Z., Janto, B., Boissy, R., Hayes, J., Keefe, R., Post, J. C. & Ehrlich, G. D. ( 2007; ). Characterization and modeling of the Haemophilus influenzae core and supragenomes based on the complete genomic sequences of Rd and 12 clinical nontypeable strains. Genome Biol 8, R103 [CrossRef]
    [Google Scholar]
  31. Holden, P. R., Brookfield, J. F. & Jones, P. ( 1993; ). Cloning and characterization of an ftsZ homologue from a bacterial symbiont of Drosophila melanogaster. Mol Gen Genet 240, 213–220.[CrossRef]
    [Google Scholar]
  32. Howell, M. L., Alsabbagh, E., Ma, J. F., Ochsner, U. A., Klotz, M. G., Beveridge, T. J., Blumenthal, K. M., Niederhoffer, E. C., Morris, R. E. & other authors ( 2000; ). AnkB, a periplasmic ankyrin-like protein in Pseudomonas aeruginosa, is required for optimal catalase B (KatB) activity and resistance to hydrogen peroxide. J Bacteriol 182, 4545–4556.[CrossRef]
    [Google Scholar]
  33. Huigens, M. E., de Almeida, R. P., Boons, P. A., Luck, R. F. & Stouthamer, R. ( 2004; ). Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc Biol Sci 271, 509–515.[CrossRef]
    [Google Scholar]
  34. Iturbe-Ormaetxe, I., Burke, G. R., Riegler, M. & O'Neill, S. L. ( 2005a; ). Distribution, expression, and motif variability of ankyrin domain genes in Wolbachia pipientis. J Bacteriol 187, 5136–5145.[CrossRef]
    [Google Scholar]
  35. Iturbe-Ormaetxe, I., Riegler, M. & O'Neill, S. L. ( 2005b; ). New names for old strains? Wolbachia wSim is actually wRi. Genome Biol 6, 401(author reply 401)[CrossRef]
    [Google Scholar]
  36. Klasson, L., Walker, T., Sebaihia, M., Sanders, M. J., Quail, M. A., Lord, A., Sanders, S., Earl, J., O'Neill, S. L. & other authors ( 2008; ). Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Mol Biol Evol 25, 1877–1887.[CrossRef]
    [Google Scholar]
  37. Klasson, L., Westberg, J., Sapountzis, P., Näslund, K., Lutnaes, Y., Darby, A. C., Veneti, Z., Chen, L., Braig, H. R. & other authors ( 2009; ). The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci U S A 106, 5725–5730.[CrossRef]
    [Google Scholar]
  38. Kondo, N., Nikoh, N., Ijichi, N., Shimada, M. & Fukatsu, T. ( 2002; ). Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci U S A 99, 14280–14285.[CrossRef]
    [Google Scholar]
  39. Korochkina, S., Barreau, C., Pradel, G., Jeffery, E., Li, J., Natarajan, R., Shabanowitz, J., Hunt, D., Frevert, U. & Vernick, K. D. ( 2006; ). A mosquito-specific protein family includes candidate receptors for malaria sporozoite invasion of salivary glands. Cell Microbiol 8, 163–175.[CrossRef]
    [Google Scholar]
  40. Kumagai, H., Hakoyama, T., Umehara, Y., Sato, S., Kaneko, T., Tabata, S. & Kouchi, H. ( 2007; ). A novel ankyrin-repeat membrane protein, IGN1, is required for persistence of nitrogen-fixing symbiosis in root nodules of Lotus japonicus. Plant Physiol 143, 1293–1305.[CrossRef]
    [Google Scholar]
  41. Lan, R. & Reeves, P. R. ( 2000; ). Intraspecies variation in bacterial genomes: the need for a species genome concept. Trends Microbiol 8, 396–401.[CrossRef]
    [Google Scholar]
  42. Lo, N., Casiraghi, M., Salati, E., Bazzocchi, C. & Bandi, C. ( 2002; ). How many Wolbachia supergroups exist? Mol Biol Evol 19, 341–346.[CrossRef]
    [Google Scholar]
  43. Lo, N., Paraskevopoulos, C., Bourtzis, K., O'Neill, S. L., Werren, J. H., Bordenstein, S. R. & Bandi, C. ( 2007; ). Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int J Syst Evol Microbiol 57, 654–657.[CrossRef]
    [Google Scholar]
  44. Masui, S., Kamoda, S., Sasaki, T. & Ishikawa, H. ( 2000; ). Distribution and evolution of bacteriophage WO in Wolbachia, the endosymbiont causing sexual alterations in arthropods. J Mol Evol 51, 491–497.
    [Google Scholar]
  45. Medini, D., Donati, C., Tettelin, H., Masignani, V. & Rappuoli, R. ( 2005; ). The microbial pan-genome. Curr Opin Genet Dev 15, 589–594.[CrossRef]
    [Google Scholar]
  46. Noda, H., Munderloh, U. G. & Kurtti, T. J. ( 1997; ). Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl Environ Microbiol 63, 3926–3932.
    [Google Scholar]
  47. O'Neill, S. L., Giordano, R., Colbert, A. M., Karr, T. L. & Robertson, H. M. ( 1992; ). 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A 89, 2699–2702.[CrossRef]
    [Google Scholar]
  48. Park, J., Kim, K. J., Choi, K. S., Grab, D. J. & Dumler, J. S. ( 2004; ). Anaplasma phagocytophilum AnkA binds to granulocyte DNA and nuclear proteins. Cell Microbiol 6, 743–751.[CrossRef]
    [Google Scholar]
  49. Rasgon, J. L. & Scott, T. W. ( 2004; ). Phylogenetic characterization of Wolbachia symbionts infecting Cimex lectularius L. and Oeciacus vicarius Horvath (Hemiptera: Cimicidae). J Med Entomol 41, 1175–1178.[CrossRef]
    [Google Scholar]
  50. Rolain, J. M., Franc, M., Davoust, B. & Raoult, D. ( 2003; ). Molecular detection of Bartonella quintana, B. koehlerae, B. henselae, B. clarridgeiae, Rickettsia felis, and Wolbachia pipientis in cat fleas, France. Emerg Infect Dis 9, 338–342.[CrossRef]
    [Google Scholar]
  51. Salzberg, S. L., Dunning Hotopp, J. C., Delcher, A. L., Pop, M., Smith, D. R., Eisen, M. B. & Nelson, W. C. ( 2005; ). Serendipitous discovery of Wolbachia genomes in multiple Drosophila species. Genome Biol 6, R23 [CrossRef]
    [Google Scholar]
  52. Sambrook, J., Firitsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  53. Steiner, F. E., Pinger, R. R., Vann, C. N., Grindle, N., Civitello, D., Clay, K. & Fuqua, C. ( 2008; ). Infection and co-infection rates of Anaplasma phagocytophilum variants, Babesia spp., Borrelia burgdorferi, and the rickettsial endosymbiont in Ixodes scapularis (Acari: Ixodidae) from sites in Indiana, Maine, Pennsylvania, and Wisconsin. J Med Entomol 45, 289–297.[CrossRef]
    [Google Scholar]
  54. Stouthamer, R., Breeuwer, J. A. & Hurst, G. D. ( 1999; ). Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53, 71–102.[CrossRef]
    [Google Scholar]
  55. Teixeria, L., Ferreira, A. & Ashburner, M. ( 2008; ). The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6, e1000002
    [Google Scholar]
  56. Tettelin, H., Nelson, K. E., Paulsen, I. T., Eisen, J. A., Read, T. D., Peterson, S., Heidelberg, J., DeBoy, R. T., Haft, D. H. & other authors ( 2001; ). Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293, 498–506.[CrossRef]
    [Google Scholar]
  57. Tettelin, H., Masignani, V., Cieslewicz, M. J., Donati, C., Medini, D., Ward, N. L., Angiuoli, S. V., Crabtree, J., Jones, A. L. & other authors ( 2005; ). Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A 102, 13950–13955.[CrossRef]
    [Google Scholar]
  58. Tettelin, H., Riley, D., Cattuto, C. & Medini, D. ( 2008; ). Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11, 472–477.[CrossRef]
    [Google Scholar]
  59. Turelli, M. & Hoffmann, A. A. ( 1995; ). Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140, 1319–1338.
    [Google Scholar]
  60. Vandekerckhove, T. T., Watteyne, S., Willems, A., Swings, J. G., Mertens, J. & Gillis, M. ( 1999; ). Phylogenetic analysis of the 16S rDNA of the cytoplasmic bacterium Wolbachia from the novel host Folsomia candida (Hexapoda, Collembola) and its implications for wolbachial taxonomy. FEMS Microbiol Lett 180, 279–286.[CrossRef]
    [Google Scholar]
  61. Verne, S., Johnson, M., Bouchon, D. & Grandjean, F. ( 2007; ). Evidence for recombination between feminizing Wolbachia in the isopod genus Armadillidium. Gene 397, 58–66.[CrossRef]
    [Google Scholar]
  62. Voronin, D. A. & Kiseleva, E. V. ( 2007; ). Functional role of proteins containing ankyrin repeats. Tsitologiia 49, 989–999.
    [Google Scholar]
  63. Weinert, L. A., Werren, J. H., Aebi, A., Stone, G. N. & Jiggins, F. M. ( 2009; ). Evolution and diversity of Rickettsia bacteria. BMC Biol 7, 6 [CrossRef]
    [Google Scholar]
  64. Wernegreen, J. J., Lazarus, A. B. & Degnan, P. H. ( 2002; ). Small genome of Candidatus Blochmannia, the bacterial endosymbiont of Camponotus, implies irreversible specialization to an intracellular lifestyle. Microbiology 148, 2551–2556.
    [Google Scholar]
  65. Werren, J. H., Zhang, W. & Guo, L. R. ( 1995; ). Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Biol Sci 261, 55–63.[CrossRef]
    [Google Scholar]
  66. Werren, J. H., Baldo, L. & Clark, M. E. ( 2008; ). Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6, 741–751.[CrossRef]
    [Google Scholar]
  67. Woolfit, M., Iturbe-Ormaetxe, I., McGraw, E. A. & O'Neill, S. L. ( 2009; ). An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Mol Biol Evol 26, 367–374.[CrossRef]
    [Google Scholar]
  68. Wu, M., Sun, L. V., Vamathevan, J., Riegler, M., Deboy, R., Brownlie, J. C., McGraw, E. A., Martin, W., Esser, C. & other authors ( 2004; ). Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2, e69 [CrossRef]
    [Google Scholar]
  69. Zabalou, S., Charlat, S., Nirgianaki, A., Lachaise, D., Mercot, H. & Bourtzis, K. ( 2004; ). Natural Wolbachia infections in the Drosophila yakuba species complex do not induce cytoplasmic incompatibility but fully rescue the wRi modification. Genetics 167, 827–834.[CrossRef]
    [Google Scholar]
  70. Zabalou, S., Apostolaki, A., Pattas, S., Veneti, Z., Paraskevopoulos, C., Livadaras, I., Markakis, G., Brissac, T., Merçot, H. & Bourtzis, K. ( 2008; ). Multiple rescue factors within a Wolbachia strain. Genetics 178, 2145–2160.[CrossRef]
    [Google Scholar]
  71. Zeh, J. A. & Zeh, D. W. ( 2006; ). Male-killing Wolbachia in a live-bearing arthropod: brood abortion as a constraint on the spread of a selfish microbe. J Invertebr Pathol 92, 33–38.[CrossRef]
    [Google Scholar]
  72. Zeh, D. W., Zeh, J. A. & Bonilla, M. M. ( 2005; ). Wolbachia, sex ratio bias and apparent male killing in the harlequin beetle riding pseudoscorpion. Heredity 95, 41–49.[CrossRef]
    [Google Scholar]
  73. Zhang, K., Martiny, A. C., Reppas, N. B., Barry, K. W., Malek, J., Chisholm, S. W. & Church, G. M. ( 2006; ). Sequencing genomes from single cells by polymerase cloning. Nat Biotechnol 24, 680–686.[CrossRef]
    [Google Scholar]
  74. Zhou, W., Rousset, F. & O'Neil, S. ( 1998; ). Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci 265, 509–515.[CrossRef]
    [Google Scholar]
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