The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen,
How virulent infectious diseases emerge from non-pathogenic organisms is a challenging question. Here, we address this evolutionary issue in the case of Q fever. Its causative agent, the intracellular bacterium Coxiella burnetii, is extremely infectious to humans and a variety of animals. However, uncertainty persists regarding its evolutionary origin, including the identity and lifestyle of its ancestors. In this article, we show that C. burnetii arose from a rare evolutionary transformation of a maternally-inherited endosymbiont of ticks into a specialized and virulent pathogen of vertebrates. While arthropod symbionts are typically transmitted maternally and thought not to be infectious to vertebrates, we establish here that one Coxiella symbiont has evolved the necessary adaptations to exploit the vertebrate cell, leading to the emergence of Q fever.
Vyšlo v časopise:
The Recent Evolution of a Maternally-Inherited Endosymbiont of Ticks Led to the Emergence of the Q Fever Pathogen,. PLoS Pathog 11(5): e32767. doi:10.1371/journal.ppat.1004892
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004892
Souhrn
How virulent infectious diseases emerge from non-pathogenic organisms is a challenging question. Here, we address this evolutionary issue in the case of Q fever. Its causative agent, the intracellular bacterium Coxiella burnetii, is extremely infectious to humans and a variety of animals. However, uncertainty persists regarding its evolutionary origin, including the identity and lifestyle of its ancestors. In this article, we show that C. burnetii arose from a rare evolutionary transformation of a maternally-inherited endosymbiont of ticks into a specialized and virulent pathogen of vertebrates. While arthropod symbionts are typically transmitted maternally and thought not to be infectious to vertebrates, we establish here that one Coxiella symbiont has evolved the necessary adaptations to exploit the vertebrate cell, leading to the emergence of Q fever.
Zdroje
1. Madariaga MG, Rezai K, Trenholme GM, Weinstein RA. Q fever: a biological weapon in your backyard. Lancet Infect Dis. 2003;3: 709–721. 14592601
2. Raoult D, Marrie T, Mege J. Natural history and pathophysiology of Q fever. Lancet Infect Dis. 2005;5: 219–226. 15792739
3. Vanderburg S, Rubach MP, Halliday JE, Cleaveland S, Reddy EA, Crump JA. Epidemiology of Coxiella burnetii infection in Africa: a OneHealth systematic review. PLoS Negl Trop Dis. 2014;8: e2787. doi: 10.1371/journal.pntd.0002787 24722554
4. Angelakis E, Raoult D. Q Fever. Vet Microbiol. 2010;140: 297–309. doi: 10.1016/j.vetmic.2009.07.016 19875249
5. Bewley KR. Animal models of Q fever (Coxiella burnetii). Comp Med. 2013;63: 469–476. 24326221
6. van der Hoek W, Dijkstra F, Schimmer B, Schneeberger PM, Vellema P, Wijkmans C, et al. Q fever in the Netherlands: an update on the epidemiology and control measures. Euro Surveill 2010;15.
7. Russell-Lodrigue KE, Andoh M, Poels MWJ, Shive HR, Weeks BR, Zhang GQ, et al. Coxiella burnetii isolates cause genogroup-specific virulence in mouse and guinea pig models of acute Q fever. Infect Immun. 2009;77: 5640–5650. doi: 10.1128/IAI.00851-09 19786560
8. McDade JE. Historical aspects of Q fever. In: Marie TJ, editor. Q Fever Volume 1: The Disease. Boca Raton: CRC Press; 1990. pp. 5–21.
9. Oyston PC, Davies C. Q fever: the neglected biothreat agent. J Med Microbiol. 2011;60: 9–21. doi: 10.1099/jmm.0.024778-0 21030501
10. Weisburg WG, Dobson ME, Samuel JE, Dasch GA, Mallavia LP, Baca O, et al. Phylogenetic diversity of the Rickettsiae. J Bacteriol. 1989;171: 4202–4206. 2753854
11. Leclerque A, Kleespies RG. Type IV secretion system components as phylogenetic markers of entomopathogenic bacteria of the genus Rickettsiella. FEMS Microbiol Ecol. 2008;279: 167–173. doi: 10.1111/j.1574-6968.2007.01025.x 18179586
12. Bouchon D, Cordaux R, Grève P. Rickettsiella, intracellular pathogens of arthropods. In: Zchori-Fein E, Bourtzis K, editors. Manipulative Tenants. Boca Raton: CRC Press; 2012. pp. 127–148.
13. Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, et al. Symbiotic bacterium modifies aphid body color. Science 2010;330: 1102–1104. doi: 10.1126/science.1195463 21097935
14. Tan CK, Owens L. Infectivity, transmission and 16S rRNA sequencing of a rickettsia, Coxiella cheraxi sp. nov., from the freshwater crayfish Cherax quadricarinatus. Dis Aquat Organ. 2000;41: 115–122. 10918979
15. van Schaik EJ, Chen C, Mertens K, Weber MM, Samuel JE. Molecular pathogenesis of the obligate intracellular bacterium Coxiella burnetii. Nat Rev Microbiol. 2013;11: 561–573. doi: 10.1038/nrmicro3049 23797173
16. Smith TA, Driscoll T, Gillespie JJ, Raghavan R. A Coxiella-like Endosymbiont is a potential vitamin source for the Lone Star Tick. Genome Biol Evol. 2015;7: 831–838. doi: 10.1093/gbe/evv016 25618142
17. Noda H, Munderloh UG, Kurtti TJ. Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl Environ Microbiol. 1997;63: 3926–3932. 9327557
18. Almeida AP, Marcili A, Leite RC, Nieri-Bastos FA, Domingues LN, Ricardo Martins J, et al. Coxiella symbiont in the tick Ornithodoros rostratus (Acari: Argasidae). Ticks Tick Borne Dis. 2012;3: 203–206. doi: 10.1016/j.ttbdis.2012.02.003 22480930
19. Duron O, Jourdain E, McCoy KD. Diversity and global distribution of the Coxiella intracellular bacterium in seabird ticks. Ticks Tick Borne Dis. 2014;5: 557–563. doi: 10.1016/j.ttbdis.2014.04.003 24915875
20. Klyachko O, Stein BD, Grindle N, Clay K, Fuqua C. Localization and visualization of a Coxiella-type symbiont within the lone star tick, Amblyomma americanum. Appl Environ Microbiol. 2007;73: 6584–6594. 17720830
21. Machado-Ferreira E, Dietrich G, Hojgaard A, Levin M, Piesman J, Zeidner NS, et al. Coxiella symbionts in the Cayenne tick Amblyomma cajennense. Microb Ecol. 2011;62: 134–142. doi: 10.1007/s00248-011-9868-x 21611689
22. Lalzar I, Harrus S, Mumcuoglu KY, Gottlieb Y. Composition and seasonal variation of Rhipicephalus turanicus and Rhipicephalus sanguineus bacterial Communities. Appl Environ Microbiol. 2012;78: 4110–4116. doi: 10.1128/AEM.00323-12 22467507
23. Jasinskas A, Zhong J, Barbour AG. Highly prevalent Coxiella sp. bacterium in the tick vector Amblyomma americanum. Appl Environ Microbiol. 2007;73: 334–336. 17085709
24. Clay K, Klyachko O, Grindle N, Civitello D, Oleske D, Fuqua C. Microbial communities and interactions in the lone star tick, Amblyomma americanum. Mol Ecol. 2008;17: 4371–4381. 19378409
25. Wilkinson DA, Dietrich M, Lebarbenchon C, Jaeger A, Le Rouzic C, Lagadec E, et al. Massive infection of seabird ticks with bacterial species related to Coxiella burnetii. Appl Environ Microbiol. 2014;80: 3327–3333. doi: 10.1128/AEM.00477-14 24657860
26. Lalzar I, Friedmann Y, Gottlieb Y. Tissue tropism and vertical transmission of Coxiella in Rhipicephalus sanguineus and Rhipicephalus turanicus ticks. Environ Microbiol; 2014;16: 3657–3668. doi: 10.1111/1462-2920.12455 24650112
27. Zhong J, Jasinskas A, Barbour AG. Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS One. 2007;2: e405. 17476327
28. Moran NA, McCutcheon JP, Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet. 2008;42: 165–190. doi: 10.1146/annurev.genet.41.110306.130119 18983256
29. Wernegreen JJ. Endosymbiosis. Curr Biol. 2012;22: R555–561. doi: 10.1016/j.cub.2012.06.010 22835786
30. Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci USA. 2010;107: 769–774. doi: 10.1073/pnas.0911476107 20080750
31. Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, Hattori M, et al. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet. 2002;32: 402–407. 12219091
32. Husnik F, Chrudimsky T, Hypsa V. Multiple origins of endosymbiosis within the Enterobacteriaceae (gamma-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biol. 2011;9: 87. doi: 10.1186/1741-7007-9-87 22201529
33. Gomez-Valero L, Rusniok C, Buchrieser C. Legionella pneumophila: population genetics, phylogeny and genomics. Infect Genet Evol. 2009;9: 727–739. doi: 10.1016/j.meegid.2009.05.004 19450709
34. Leclerque A, Kleespies RG. A Rickettsiella bacterium from the hard tick, Ixodes woodi: molecular taxonomy combining multilocus sequence typing (MLST) with significance testing. PLoS One. 2012;7: e38062. doi: 10.1371/journal.pone.0038062 22675436
35. Omsland A, Beare PA, Hill J, Cockrell DC, Howe D, Virtaneva K, et al. Isolation from animal tissue and genetic transformation of Coxiella burnetii are facilitated by an improved axenic growth medium. Appl Environ Microbiol. 2011;77: 3720–3725. doi: 10.1128/AEM.02826-10 21478315
36. Sekeyová Z, Roux V, Raoult D. Intraspecies diversity of Coxiella burnetii as revealed by com1 and mucZ sequence comparison. FEMS Microbiol Lett. 1999;180: 61–67. 10547445
37. Pearson T, Hornstra HM, Sahl JW, Schaack S, Schupp JM, Beckstrom-Sternberg SM, et al. When outgroups fail; phylogenomics of rooting the emerging pathogen, Coxiella burnetii. Syst Biol. 2013;62: 752–762. doi: 10.1093/sysbio/syt038 23736103
38. Seshadri R, Paulsen IT, Eisen JA, Read TD, Nelson KE, Nelson WC, et al. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci USA. 2003;100: 5455–5460. 12704232
39. Beare PA, Unsworth N, Andoh M, Voth DE, Omsland A, Gilk SD, et al. Comparative genomics reveal extensive transposon-mediated genomic plasticity and diversity among potential effector proteins within the genus Coxiella. Infect Immun. 2009;77: 642–656. doi: 10.1128/IAI.01141-08 19047403
40. Engelstadter J, Hurst GDD. The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst. 2009;40: 127–149.
41. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstadter J, et al. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 2008;6: 27. doi: 10.1186/1741-7007-6-27 18577218
42. Zug R, Hammerstein P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One. 2012;7: e38544. doi: 10.1371/journal.pone.0038544 22685581
43. Shivaprasad HL, Cadenas MB, Diab SS, Nordhausen R, Bradway D, Crespo R, et al. Coxiella-like infection in psittacines and a toucan. Avian Dis. 2008;52: 426–432. 18939630
44. Woc-Colburn AM, Garner MM, Bradway D, West G, D'Agostino J, Trupkiewicz J, et al. Fatal coxiellosis in Swainson's Blue Mountain Rainbow Lorikeets (Trichoglossus haematodus moluccanus). Vet Pathol. 2008;45: 247–254. doi: 10.1354/vp.45-2-247 18424842
45. Vapniarsky N, Barr BC, Murphy B. Systemic Coxiella-like infection with myocarditis and hepatitis in an eclectus parrot (Eclectus roratus). Vet Pathol. 2012;49: 717–722. doi: 10.1177/0300985811409251 21712515
46. Duron O, Wilkes TE, Hurst GDD. Interspecific transmission of a male-killing bacterium on an ecological timescale. Ecol Lett. 2010;13: 1139–1148. doi: 10.1111/j.1461-0248.2010.01502.x 20545734
47. Duron O, Schneppat UE, Berthomieu A, Goodman SE, Droz B, Paupy C, et al. Origin, acquisition and diversification of heritable bacterial endosymbionts in louse flies and bat flies. Mol Ecol. 2014;23: 2105–2017. doi: 10.1111/mec.12704 24612422
48. Jousselin E, Coeur d'Acier A, Vanlerberghe-Masutti F, Duron O. Evolution and diversity of Arsenophonus endosymbionts in aphids. Mol Ecol. 2013;22: 260–270. doi: 10.1111/mec.12092 23106652
49. Novakova E, Hypsa V, Moran NA. Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol. 2009;9: 143. doi: 10.1186/1471-2180-9-143 19619300
50. Bressan A. Emergence and evolution of Arsenophonus bacteria as insect-vectored plant pathogens. Infect Genet Evol. 2014;22: 81–90. doi: 10.1016/j.meegid.2014.01.004 24444593
51. Benson MJ, Gawronski JD, Eveleigh DE, Benson DR. Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellfleet, Cape Cod, Massachusetts. Appl Environ Microbiol. 2004;70: 616–620. 14711698
52. van Overbeek L, Gassner F, van der Plas CL, Kastelein P, Nunes-da Rocha U, Takken W. Diversity of Ixodes ricinus tick-associated bacterial communities from different forests. FEMS Microbiol Ecol. 2008;66: 72–84. doi: 10.1111/j.1574-6941.2008.00468.x 18355299
53. Duron O. Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts. Heredity 2013;111: 330–337. doi: 10.1038/hdy.2013.56 23759724
54. Baldo L, Werren JH. Revisiting Wolbachia supergroup typing based on WSP: spurious lineages and discordance with MLST. Curr Microbiol. 2007;55: 81–87. 17551786
55. Degnan PH, Moran NA. Evolutionary genetics of a defensive facultative symbiont of insects: exchange of toxin-encoding bacteriophage. Mol Ecol. 2008;17: 916–929. doi: 10.1111/j.1365-294X.2007.03616.x 18179430
56. Nikoh N, Hosokawa T, Moriyama M, Oshima K, Hattori M, Fukatsu T. Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc Natl Acad Sci USA. 2014;111: 10257–10262. doi: 10.1073/pnas.1409284111 24982177
57. Duron O. Arsenophonus insect symbionts are commonly infected with APSE, a bacteriophage involved in protective symbiosis. FEMS Microbiol Ecol. 2014;90: 184–194. doi: 10.1111/1574-6941.12381 25041857
58. Perlman SJ, Hunter MS, Zchori-Fein E. The emerging diversity of Rickettsia. Proc R Soc Lond B Biol Sci. 2006;273: 2097–106.
59. Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM. Evolution and diversity of Rickettsia bacteria. BMC Biol. 2009;7: 6. doi: 10.1186/1741-7007-7-6 19187530
60. Clayton AL, Oakeson KF, Gutin M, Pontes A, Dunn DM, von Niederhausern AC, et al. A novel human-infection-derived bacterium provides insights into the evolutionary origins of mutualistic insect–bacterial symbioses. PLoS Genet. 2012;8: e1002990. doi: 10.1371/journal.pgen.1002990 23166503
61. Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics 2002; 2: 3. doi: 10.1002/0471250953.bi0203s00 18792934
62. Kumar S, Tamura K, Nei M. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 2004;5: 150–163. 15260895
63. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17: 540–552. 10742046
64. Librado P, Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009;25: 1451–1452. doi: 10.1093/bioinformatics/btp187 19346325
65. Sawyer SA. GENECONV: A computer package for the statistical detection of gene conversion. http://www.math.wustl.edu/~sawy.
66. Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics. 2000;16: 562–563. 10980155
67. Martin D, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics. 2010;26: 2462–2463. doi: 10.1093/bioinformatics/btq467 20798170
68. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23: 254–267. 16221896
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Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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