Quorum sensing sets the stage for the establishment and vertical transmission of Sodalis praecaptivus in tsetse flies

English version

Autoři: Miguel Medina Munoz ^aff001; Noah Spencer ^aff001; Shinichiro Enomoto ^aff002; Colin Dale ^aff002; Rita V. M. Rio ^aff001
Působiště autorů: Department of Biology, Eberly College of Arts and Sciences, West Virginia University, Morgantown, WV, United States of America ^aff001; Department of Biology, University of Utah, Salt Lake City, UT, United States of America ^aff002
Vyšlo v časopise: Quorum sensing sets the stage for the establishment and vertical transmission of Sodalis praecaptivus in tsetse flies. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008992
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008992

Souhrn

Bacterial virulence factors facilitate host colonization and set the stage for the evolution of parasitic and mutualistic interactions. The Sodalis-allied clade of bacteria exhibit striking diversity in the range of both plant and animal feeding insects they inhabit, suggesting the appropriation of universal molecular mechanisms that facilitate establishment. Here, we report on the infection of the tsetse fly by free-living Sodalis praecaptivus, a close relative of many Sodalis-allied symbionts. Key genes involved in quorum sensing, including the homoserine lactone synthase (ypeI) and response regulators (yenR and ypeR) are integral for the benign colonization of S. praecaptivus. Mutants lacking ypeI, yenR and ypeR compromised tsetse survival as a consequence of their inability to repress virulence. Genes under quorum sensing, including homologs of the binary insecticidal toxin PirAB and a putative symbiosis-promoting factor CpmAJ, demonstrated negative and positive impacts, respectively, on tsetse survival. Taken together with results obtained from experiments involving weevils, this work shows that quorum sensing virulence suppression plays an integral role in facilitating the establishment of Sodalis-allied symbionts in diverse insect hosts. This knowledge contributes to the understanding of the early evolutionary steps involved in the formation of insect-bacterial symbiosis. Further, despite having no established history of interaction with tsetse, S. praecaptivus can infect reproductive tissues, enabling vertical transmission through adenotrophic viviparity within a single host generation. This creates an option for the use of S. praecaptivus in the biocontrol of insect disease vectors via paratransgenesis.

Klíčová slova:

Insect vectors – Insects – Microinjection – Symbiosis – Virulence factors – Weevils – Quorum sensing – Tsetse fly

Zdroje

1. Shin SC, Kim SH, You H, Kim B, Kim AC, Lee KA, et al. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science. 2011;334(6056):670–4. doi: 10.1126/science.1212782 22053049

2. Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab. 2011;14(3):403–14. doi: 10.1016/j.cmet.2011.07.012 21907145

3. Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, et al. Symbiotic bacterium modifies aphid body color. Science. 2010;330(6007):1102–4. doi: 10.1126/science.1195463 21097935

4. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31. doi: 10.1038/nature05414 17183312

5. Rook G, Backhed F, Levin BR, McFall-Ngai MJ, McLean AR. Evolution, human-microbe interactions, and life history plasticity. Lancet. 2017;390(10093):521–30. doi: 10.1016/S0140-6736(17)30566-4 28792414

6. Kondorosi E, Mergaert P, Kereszt A. A paradigm for endosymbiotic life: cell differentiation of Rhizobium bacteria provoked by host plant factors. Annu Rev Microbiol. 2013;67:611–28. doi: 10.1146/annurev-micro-092412-155630 24024639

7. Nyholm SV, McFall-Ngai MJ. The winnowing: establishing the squid-vibrio symbiosis. Nature Reviews Microbiology. 2004;2(8):632–42. doi: 10.1038/nrmicro957 15263898

8. Sorensen MES, Lowe CD, Minter EJA, Wood AJ, Cameron DD, Brockhurst MA. The role of exploitation in the establishment of mutualistic microbial symbioses. FEMS Microbiol Lett. 2019;366(12).

9. 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

10. Werren JH, Windsor DM. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc Biol Sci. 2000;267(1450):1277–85. doi: 10.1098/rspb.2000.1139 10972121

11. Gasparich GE, Whitcomb RF, Dodge D, French FE, Glass J, Williamson DL. The genus Spiroplasma and its non-helical descendants: phylogenetic classification, correlation with phenotype and roots of the Mycoplasma mycoides clade. Int J Syst Evol Microbiol. 2004;54(Pt 3):893–918. doi: 10.1099/ijs.0.02688-0 15143041

12. Darby AC, Cho NH, Fuxelius HH, Westberg J, Andersson SG. Intracellular pathogens go extreme: genome evolution in the Rickettsiales. Trends Genet. 2007;23(10):511–20. doi: 10.1016/j.tig.2007.08.002 17822801

13. Arora AK, Douglas AE. Hype or opportunity? Using microbial symbionts in novel strategies for insect pest control. Journal of insect physiology. 2017;103:10–7. doi: 10.1016/j.jinsphys.2017.09.011 28974456

14. Rio RVM, Hu Y., and Aksoy S. Strategies of the home-team: Symbioses exploited for vector-borne disease control. Trends Microbiol. 2004;12:325–36. doi: 10.1016/j.tim.2004.05.001 15223060

15. Novakova E, Hypsa V. A new Sodalis lineage from bloodsucking fly Craterina melbae (Diptera, Hippoboscoidea) originated independently of the tsetse flies symbiont Sodalis glossinidius. FEMS Microbiol Lett. 2007;269(1):131–5. doi: 10.1111/j.1574-6968.2006.00620.x 17227456

16. Fukatsu T, Koga R., Smith W.A, Tanaka K, Nikoh N, Sasaki-Fakatus K, Yoshizawa K, Dale Cand D.H. Clayton. Bacterial endosymbiont of the slender pigeon louse, Columbicola columbae, allied to endosymbionts of grain weevils and tsetse flies. Appl Environ Microbiol. 2007;73:6660–8. doi: 10.1128/AEM.01131-07 17766458

17. Grunwald S, Pilhofer M., and Holl W. Microbial associations in guts systems of wood- and bark- inhabiting longhorned beetles [Coleoptera: Cerambyicidae]. Syst Appl Microbiol. 2010;33:25–34. doi: 10.1016/j.syapm.2009.10.002 19962263

18. Toju H, Fukatsu T. Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol Ecol. 2011;20(4):853–68. doi: 10.1111/j.1365-294X.2010.04980.x 21199036

19. TH Kaiwa N., Kikuchi Y., Nikoh N., Meng X.Y., Kimura N., Ito M., and Fukatsu T. Primary gut symbiont and secodary, Sodalis-allied symbiont of the scutellerid stinkbug Cantao ocellatus. Appl Environ Microbiol. 2010;76:3486–94. doi: 10.1128/AEM.00421-10 20400564

20. Toju HTH, Koga R., Nikoh N., Meng X.Y., Kimura N., and Fukatsu T. "Candidatus Curculioniphilus buchneri" a novel clade of bacterial endocellular symbionts from weevels of the genus Curculio. Appl Environ Microbiol. 2010;76:275–82. doi: 10.1128/AEM.02154-09 19880647

21. Kaiwa N, Hosokawa T, Kikuchi Y, Nikoh N, Meng XY, Kimura N, et al. Bacterial symbionts of the giant jewel stinkbug Eucorysses grandis (Hemiptera: Scutelleridae). Zoolog Sci. 2011;28(3):169–74. doi: 10.2108/zsj.28.169 21385056

22. Boyd BM, Allen JM, Koga R, Fukatsu T, Sweet AD, Johnson KP, et al. Two Bacterial Genera, Sodalis and Rickettsia, Associated with the Seal Louse Proechinophthirus fluctus (Phthiraptera: Anoplura). Appl Environ Microbiol. 2016;82(11):3185–97. doi: 10.1128/AEM.00282-16 26994086

23. Santos-Garcia D, Silva FJ, Morin S, Dettner K, Kuechler SM. The All-Rounder Sodalis: A New Bacteriome-Associated Endosymbiont of the Lygaeoid Bug Henestaris halophilus (Heteroptera: Henestarinae) and a Critical Examination of Its Evolution. Genome biology and evolution. 2017;9(10):2893–910. doi: 10.1093/gbe/evx202 29036401

24. Rubin BER, Sanders JG, Turner KM, Pierce NE, Kocher SD. Social behaviour in bees influences the abundance of Sodalis (Enterobacteriaceae) symbionts. R Soc Open Sci. 2018;5(7):180369. doi: 10.1098/rsos.180369 30109092

25. 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 genetics. 2012;8(11):e1002990. doi: 10.1371/journal.pgen.1002990 23166503

26. Snyder AK, Adkins K.Z. and RVM. Rio. Use of the Internal Transcribed Spacer (ITS) regions to examine symbiont divergence and as a diagnostic tool for Sodalis-related bacteria. Insects. 2011;2:515–31.

27. Enomoto S, Chari A, Clayton AL, Dale C. Quorum Sensing Attenuates Virulence in Sodalis praecaptivus. Cell host & microbe. 2017;21(5):629–36 e5.

28. Nealson KH, Platt T, Hastings JW. Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol. 1970;104(1):313–22. doi: 10.1128/JB.104.1.313-322.1970 5473898

29. Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol. 1994;176(2):269–75. doi: 10.1128/jb.176.2.269-275.1994 8288518

30. Papenfort K, Bassler BL. Quorum sensing signal-response systems in Gram-negative bacteria. Nature Reviews Microbiology. 2016;14(9):576–88. doi: 10.1038/nrmicro.2016.89 27510864

31. Toh H, Weiss BL, Perkin SA, Yamashita A, Oshima K, Hattori M, et al. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res. 2006;16(2):149–56. doi: 10.1101/gr.4106106 16365377

32. Weiss BL, Maltz MA, Vigneron A, Wu Y, Walter KS, O'Neill MB, et al. Colonization of the tsetse fly midgut with commensal Kosakonia cowanii Zambiae inhibits trypanosome infection establishment. PLoS pathogens. 2019;15(2):e1007470. doi: 10.1371/journal.ppat.1007470 30817773

33. Waterfield N, Kamita SG, Hammock BD, ffrench-Constant R. The Photorhabdus Pir toxins are similar to a developmentally regulated insect protein but show no juvenile hormone esterase activity. FEMS Microbiol Lett. 2005;245(1):47–52. doi: 10.1016/j.femsle.2005.02.018 15796978

34. Pontes MH, Babst M, Lochhead R, Oakeson K, Smith K, Dale C. Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius. PloS one. 2008;3(10):e3541. doi: 10.1371/journal.pone.0003541 18958153

35. Dale C, Welburn SC. The endosymbionts of tsetse flies-manipulating host-parasite interactions. International Journal of Parasitology. 2001;31:628–31. doi: 10.1016/s0020-7519(01)00151-5 11334953

36. Dale C, Maudlin I. Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int J Syst Bacteriol. 1999;49:267–75. doi: 10.1099/00207713-49-1-267 10028272

37. Demirbas-Uzel G, De Vooght L, Parker AG, Vreysen MJB, Mach RL, Van Den Abbeele J, et al. Combining paratransgenesis with SIT: impact of ionizing radiation on the DNA copy number of Sodalis glossinidius in tsetse flies. BMC Microbiol. 2018;18(Suppl 1):160. doi: 10.1186/s12866-018-1283-8 30470179

38. Phelps RJ, Vale GA. Studies on populations of Glossina morsitans morsitans and G. pallidipes (Diptera: Glossinidae) in Rhodesia. Journal of Applied Ecology. 1978;15(3):743–60.

39. Cheng Q, Aksoy S. Tissue tropism, transmission, and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol Biol. 1999;8(1):125–32. doi: 10.1046/j.1365-2583.1999.810125.x 9927181

40. Ma W D Denlinger. Secretory discharge and microflora of milk gland in tsetse flies. Nature. 1974;247:301–3.

41. Balmand S, Lohs C, Aksoy S, Heddi A. Tissue distribution and transmission routes for the tsetse fly endosymbionts. J Invertebr Pathol. 2013;112 Suppl:S116–22. doi: 10.1016/j.jip.2012.04.002 22537833

42. De Vooght L, Caljon G, Van Hees J, Van Den Abbeele J. Paternal Transmission of a Secondary Symbiont during Mating in the Viviparous Tsetse Fly. Mol Biol Evol. 2015;32(8):1977–80. doi: 10.1093/molbev/msv077 25851957

43. Bennett GM, Moran NA. Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole. Proc Natl Acad Sci U S A. 2015;112(33):10169–76. doi: 10.1073/pnas.1421388112 25713367

44. Wiegmann BM, Trautwein MD, Kim JW, Cassel BK, Bertone MA, Winterton SL, et al. Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol. 2009;7:34. doi: 10.1186/1741-7007-7-34 19552814

45. Baker JE. Development of four strains of Sitophilus oryzae (L.) (Coleoptera: Curculionidae) on barley, corn (maize), rice and wheat. Journal of Stored Products Research. 1988;24(4):193–8.

46. Weitz B. The feeding habits of Glossina. Bull World Health Organ. 1963;28(5–6):711–29. 13999790

47. Oakeson KF, Gil R, Clayton AL, Dunn DM, von Niederhausern AC, Hamil C, et al. Genome degeneration and adaptation in a nascent stage of symbiosis. Genome biology and evolution. 2014;6(1):76–93. doi: 10.1093/gbe/evt210 24407854

48. Moran NA A Mira. The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol. 2001;2:00054.1–0054.12.

49. Chapuis E, Pages S, Emelianoff V, Givaudan A, Ferdy JB. Virulence and pathogen multiplication: a serial passage experiment in the hypervirulent bacterial insect-pathogen Xenorhabdus nematophila. PloS one. 2011;6(1):e15872. doi: 10.1371/journal.pone.0015872 21305003

50. Chattopadhyay A, Bhatnagar NB, Bhatnagar R. Bacterial insecticidal toxins. Critical reviews in microbiology. 2004;30(1):33–54. doi: 10.1080/10408410490270712 15116762

51. Gross R, Vavre F, Heddi A, Hurst GD, Zchori-Fein E, Bourtzis K. Immunity and symbiosis. Mol Microbiol. 2009;73(5):751–9. doi: 10.1111/j.1365-2958.2009.06820.x 19656293

52. Tichy EM, Luisi BF, Salmond GP. Crystal structure of the carbapenem intrinsic resistance protein CarG. J Mol Biol. 2014;426(9):1958–70. doi: 10.1016/j.jmb.2014.02.016 24583229

53. Alizon S, Hurford A, Mideo N, Van Baalen M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol. 2009;22(2):245–59. doi: 10.1111/j.1420-9101.2008.01658.x 19196383

54. Sachs JL, Skophammer RG, Regus JU. Evolutionary transitions in bacterial symbiosis. P Natl Acad Sci USA. 2011;108 Suppl 2:10800–7.

55. De Vooght L, Van Keer S, Van Den Abbeele J. Towards improving tsetse fly paratransgenesis: stable colonization of Glossina morsitans morsitans with genetically modified Sodalis. BMC Microbiol. 2018;18(Suppl 1):165. doi: 10.1186/s12866-018-1282-9 30470181

56. Kariithi HM, Meki IK, Schneider DI, De Vooght L, Khamis FM, Geiger A, et al. Enhancing vector refractoriness to trypanosome infection: achievements, challenges and perspectives. BMC Microbiol. 2018;18(Suppl 1):179. doi: 10.1186/s12866-018-1280-y 30470182

57. Moloo SK. An artificial feeding technique for Glossina. Parasitology. 1971;63:507–12. doi: 10.1017/s0031182000080021 5139030

58. Balleza E, Kim JM, Cluzel P. Systematic characterization of maturation time of fluorescent proteins in living cells. Nat Methods. 2018;15(1):47–51. doi: 10.1038/nmeth.4509 29320486

59. Kim JM, Garcia-Alcala M, Balleza E, Cluzel P. Stochastic transcriptional pulses orchestrate flagellar biosynthesis in. Sci Adv. 2020;6(6):eaax0947. doi: 10.1126/sciadv.aax0947 32076637

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