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Consequences of chronic bacterial infection in Drosophila melanogaster


Autoři: Moria Cairns Chambers aff001;  Eliana Jacobson aff001;  Sarah Khalil aff001;  Brian P. Lazzaro aff001
Působiště autorů: Department of Entomology, Cornell University, Ithaca, New York, United States of America aff001;  Department of Biology, Bucknell University, Lewisburg, PA, United States of America aff002;  Cornell Institute of Host-Microbe Interactions and Disease, Cornell University, Ithaca, New York, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224440

Souhrn

Even when successfully surviving an infection, a host often fails to eliminate a pathogen completely and may sustain substantial pathogen burden for the remainder of its life. Using systemic bacterial infection in Drosophila melanogaster, we characterize chronic infection by three bacterial species from different genera - Providencia rettgeri, Serratia marcescens, and Enterococcus faecalis–following inoculation with a range of doses. To assess the consequences of these chronic infections, we determined the expression of antimicrobial peptide genes, survival of secondary infection, and starvation resistance after one week of infection. While higher infectious doses unsurprisingly lead to higher risk of death, they also result in higher chronic bacterial loads among the survivors for all three infections. All three chronic infections caused significantly elevated expression of antimicrobial peptide genes at one week post-infection and provided generalized protection again secondary bacterial infection. Only P. rettgeri infection significantly influenced resistance to starvation, with persistently infected flies dying more quickly under starvation conditions relative to controls. These results suggest that there is potentially a generalized mechanism of protection against secondary infection, but that other impacts on host physiology may depend on the specific pathogen. We propose that chronic infections in D. melanogaster could be a valuable tool for studying tolerance of infection, including impacts on host physiology and behavior.

Klíčová slova:

Bacterial diseases – Drosophila melanogaster – Enterococcus faecalis – Enterococcus infections – Gene expression – Pathogens – Serratia marcescens – Serratia infections


Zdroje

1. Howick VM, Lazzaro BP. Genotype and diet shape resistance and tolerance across distinct phases of bacterial infection. BMC Evol Biol. 2014;14: 56. doi: 10.1186/1471-2148-14-56 24655914

2. Chambers MC, Jacobson E, Khalil S, Lazzaro BP. Thorax injury lowers resistance to infection in Drosophila melanogaster. Infect Immun. 2014;82: 4380–4389. doi: 10.1128/IAI.02415-14 25092914

3. Clemmons AW, Lindsay SA, Wasserman SA. An effector peptide family required for Drosophila Toll-mediated immunity. PLOS Pathog. 2015;11: e1004876. doi: 10.1371/journal.ppat.1004876 25915418

4. Kutzer MAM, Armitage SAO. The effect of diet and time after bacterial infection on fecundity, resistance, and tolerance in Drosophila melanogaster. Ecol Evol. 2016;6: 4229–4242. doi: 10.1002/ece3.2185 27386071

5. Duneau D, Ferdy J-B, Revah J, Kondolf H, Ortiz GA, Lazzaro BP, et al. Stochastic variation in the initial phase of bacterial infection predicts the probability of survival in D. melanogaster. eLife. 2017;6: e28298. doi: 10.7554/eLife.28298 29022878

6. Galac MR, Lazzaro BP. Comparative pathology of bacteria in the genus Providencia to a natural host, Drosophila melanogaster. Microbes Infect. 2011;13: 673–683. doi: 10.1016/j.micinf.2011.02.005 21354324

7. Nehme NT, Quintin J, Cho JH, Lee J, Lafarge M-C, Kocks C, et al. Relative roles of the cellular and humoral responses in the Drosophila host defense against three Gram-positive bacterial infections. PLOS ONE. 2011;6: e14743. doi: 10.1371/journal.pone.0014743 21390224

8. Teixeira N, Varahan S, Gorman MJ, Palmer KL, Zaidman-Remy A, Yokohata R, et al. Drosophila host model reveals new Enterococcus faecalis quorum-sensing associated virulence factors. PLoS ONE. 2013;8. doi: 10.1371/journal.pone.0064740 23734216

9. Troha K, Im JH, Revah J, Lazzaro BP, Buchon N. Comparative transcriptomics reveals CrebA as a novel regulator of infection tolerance in D. melanogaster. PLOS Pathog. 2018;14: e1006847. doi: 10.1371/journal.ppat.1006847 29394281

10. Duneau DF, Kondolf HC, Im JH, Ortiz GA, Chow C, Fox MA, et al. The Toll pathway underlies host sexual dimorphism in resistance to both Gram-negative and Gram-positive bacteria in mated Drosophila. BMC Biol. 2017;15. doi: 10.1186/s12915-017-0466-3 29268741

11. Lemaitre B, Reichhart J-M, Hoffmann JA. Drosophila host defense: Differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci. 1997;94: 14614–14619. doi: 10.1073/pnas.94.26.14614 9405661

12. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 2002;21: 2568–2579. doi: 10.1093/emboj/21.11.2568 12032070

13. Takehana A, Katsuyama T, Yano T, Oshima Y, Takada H, Aigaki T, et al. Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-LE, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in Drosophila larvae. Proc Natl Acad Sci. 2002;99: 13705–13710. doi: 10.1073/pnas.212301199 12359879

14. Leulier F, Parquet C, Pili-Floury S, Ryu J-H, Caroff M, Lee W-J, et al. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol. 2003;4: 478. doi: 10.1038/ni922 12692550

15. Kaneko T, Goldman WE, Mellroth P, Steiner H, Fukase K, Kusumoto S, et al. Monomeric and polymeric Gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity. 2004;20: 637–649. doi: 10.1016/s1074-7613(04)00104-9 15142531

16. Royet J, Dziarski R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol. 2007;5: 264–277. doi: 10.1038/nrmicro1620 17363965

17. Buchon N, Silverman N, Cherry S. Immunity in Drosophila melanogaster—from microbial recognition to whole-organism physiology. Nat Rev Immunol. 2014;14: 796–810. doi: 10.1038/nri3763 25421701

18. Vaz F, Kounatidis I, Covas G, Parton RM, Harkiolaki M, Davis I, et al. Accessibility to peptidoglycan is important for the recognition of Gram-positive bacteria in Drosophila. Cell Rep. 2019;27: 2480–2492.e6. doi: 10.1016/j.celrep.2019.04.103 31116990

19. Tate AT, Graham AL. Dissecting the contributions of time and microbe density to variation in immune gene expression. Proc R Soc B Biol Sci. 2017;284. doi: 10.1098/rspb.2017.0727 28747473

20. Erler S, Popp M, Lattorff HMG. Dynamics of immune system gene expression upon bacterial challenge and wounding in a social insect (Bombus terrestris). PLOS ONE. 2011;6: e18126. doi: 10.1371/journal.pone.0018126 21479237

21. Louie A, Song KH, Hotson A, Thomas Tate A, Schneider DS. How many parameters does it take to describe disease tolerance? PLoS Biol. 2016;14. doi: 10.1371/journal.pbio.1002435 27088212

22. Haine ER, Moret Y, Siva-Jothy MT, Rolff J. Antimicrobial defense and persistent infection in insects. Science. 2008;322: 1257–1259. doi: 10.1126/science.1165265 19023083

23. Makarova O, Rodriguez-Rojas A, Eravci M, Weise C, Dobson A, Johnston P, et al. Antimicrobial defence and persistent infection in insects revisited. Philos Trans R Soc B Biol Sci. 2016;371. doi: 10.1098/rstb.2015.0296 27160598

24. Pham LN, Dionne MS, Shirasu-Hiza M, Schneider DS. A specific primed immune response in Drosophila is dependent on phagocytes. PLOS Pathog. 2007;3: e26. doi: 10.1371/journal.ppat.0030026 17352533

25. Christofi T, Apidianakis Y. Drosophila immune priming against Pseudomonas aeruginosa is short-lasting and depends on cellular and humoral immunity. F1000Research. 2013;2. doi: 10.12688/f1000research.2-76.v1 24358857

26. Milutinović B, Kurtz J. Immune memory in invertebrates. Semin Immunol. 2016;28: 328–342. doi: 10.1016/j.smim.2016.05.004 27402055

27. Cooper D, Eleftherianos I. Memory and specificity in the insect immune system: current perspectives and future challenges. Front Immunol. 2017;8. doi: 10.3389/fimmu.2017.00539 28536580

28. Tzou P, Ohresser S, Ferrandon D, Capovilla M, Reichhart J-M, Lemaitre B, et al. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity. 2000;13: 737–748. doi: 10.1016/s1074-7613(00)00072-8 11114385

29. Juneja P, Lazzaro BP. Providencia sneebia sp. nov. and Providencia burhodogranariea sp. nov., isolated from wild Drosophila melanogaster. Int J Syst Evol Microbiol. 2009;59: 1108–1111. doi: 10.1099/ijs.0.000117-0 19406801

30. Lazzaro BP, Sceurman BK, Clark AG. Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science. 2004;303: 1873–1876. doi: 10.1126/science.1092447 15031506

31. Khalil S, Jacobson E, Chambers MC, Lazzaro BP. Systemic bacterial infection and immune defense phenotypes in Drosophila melanogaster. J Vis Exp. 2015 [cited 28 Feb 2016]. doi: 10.3791/52613 25992475

32. Schwenke RA, Lazzaro BP. Juvenile hormone suppresses resistance to infection in mated female Drosophila melanogaster. Curr Biol. 2017;27: 596–601. doi: 10.1016/j.cub.2017.01.004 28190728

33. Pfaffl MW. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 2001;29: e45. doi: 10.1093/nar/29.9.e45 11328886

34. Dionne MS, Ghori N, Schneider DS. Drosophila melanogaster is a genetically tractable model host for Mycobacterium marinum. Infect Immun. 2003;71: 3540–3550. doi: 10.1128/IAI.71.6.3540-3550.2003 12761139

35. Mansfield BE, Dionne MS, Schneider DS, Freitag NE. Exploration of host-pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell Microbiol. 2003;5: 901–911. 14641175

36. Hotson AG, Schneider DS. Drosophila melanogaster natural variation affects growth dynamics of infecting Listeria monocytogenes. G3 GenesGenomesGenetics. 2015;5: 2593–2600. doi: 10.1534/g3.115.022558 26438294

37. Gupta V, Vale PF. Nonlinear disease tolerance curves reveal distinct components of host responses to viral infection. R Soc Open Sci. 2017;4. doi: 10.1098/rsos.170342 28791163

38. Myllymäki H, Valanne S, Rämet M. The Drosophila Imd Signaling Pathway. J Immunol. 2014;192: 3455–3462. doi: 10.4049/jimmunol.1303309 24706930

39. Hanson MA, Dostálová A, Ceroni C, Poidevin M, Kondo S, Lemaitre B. Synergy and remarkable specificity of antimicrobial peptides in vivo using a systematic knockout approach. MacPherson AJ, Garrett WS, Hornef M, Hooper LV, editors. eLife. 2019;8: e44341. doi: 10.7554/eLife.44341 30803481

40. Unckless RL, Howick VM, Lazzaro BP. Convergent balancing selection on an antimicrobial peptide in Drosophila. Curr Biol. 2016;26: 257–262. doi: 10.1016/j.cub.2015.11.063 26776733

41. Dimarcq J-L, Hoffmann D, Meister M, Bulet P, Lanot R, Reichhart J-M, et al. Characterization and transcriptional profiles of a Drosophila gene encoding an insect defensin. Eur J Biochem. 1994;221: 201–209. doi: 10.1111/j.1432-1033.1994.tb18730.x 8168509

42. Fehlbaum P, Bulet P, Michaut L, Lagueux M, Broekaert WF, Hetru C, et al. Insect immunity. Septic injury of Drosophila induces the synthesis of a potent antifungal peptide with sequence homology to plant antifungal peptides. J Biol Chem. 1994;269: 33159–33163. 7806546

43. Levashina EA, Ohresser S, Bulet P, Reichhart JM, Hetru C, Hoffmann JA. Metchnikowin, a novel immune-inducible proline-rich peptide from Drosophila with antibacterial and antifungal properties. Eur J Biochem. 1995;233: 694–700. doi: 10.1111/j.1432-1033.1995.694_2.x 7588819

44. Wang L-N, Yu B, Han G-Q, Chen D-W. Molecular cloning, expression in Escherichia coli of Attacin A gene from Drosophila and detection of biological activity. Mol Biol Rep. 2010;37: 2463–2469. doi: 10.1007/s11033-009-9758-1 19711194

45. Chippindale AK, Chu TJF, Rose MR. Complex trade-offs and the evolution of starvation resistance in Drosophila melanogaster. Evolution. 1996;50: 753–766. doi: 10.1111/j.1558-5646.1996.tb03885.x 28568920

46. Dionne MS, Schneider DS. Models of infectious diseases in the fruit fly Drosophila melanogaster. Dis Model Mech. 2008;1: 43–49. doi: 10.1242/dmm.000307 19048052

47. Engström Y. Induction and regulation of antimicrobial peptides in Drosophila. Dev Comp Immunol. 1999;23: 345–358. doi: 10.1016/s0145-305x(99)00016-6 10426427

48. Stenbak CR, Ryu J-H, Leulier F, Pili-Floury S, Parquet C, Hervé M, et al. Peptidoglycan molecular requirements allowing detection by the Drosophila Immune Deficiency Pathway. J Immunol. 2004;173: 7339–7348. doi: 10.4049/jimmunol.173.12.7339 15585858

49. Hedengren-Olcott M, Olcott MC, Mooney DT, Ekengren S, Geller BL, Taylor BJ. Differential activation of the NF-κB-like factors Relish and Dif in Drosophila melanogaster by fungi and Gram-positive bacteria. J Biol Chem. 2004;279: 21121–21127. doi: 10.1074/jbc.M313856200 14985331

50. Eleftherianos I, Marokhazi J, Millichap PJ, Hodgkinson AJ, Sriboonlert A, ffrench-Constant RH, et al. Prior infection of Manduca sexta with non-pathogenic Escherichia coli elicits immunity to pathogenic Photorhabdus luminescens: Roles of immune-related proteins shown by RNA interference. Insect Biochem Mol Biol. 2006;36: 517–525. doi: 10.1016/j.ibmb.2006.04.001 16731347

51. Roth O, Sadd BM, Schmid-Hempel P, Kurtz J. Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum. Proc R Soc B Biol Sci. 2009;276: 145–151. doi: 10.1098/rspb.2008.1157 18796392

52. Sadd BM, Schmid-Hempel P. Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol. 2006;16: 1206–1210. doi: 10.1016/j.cub.2006.04.047 16782011

53. Chambers MC, Song KH, Schneider DS. Listeria monocytogenes infection causes metabolic shifts in Drosophila melanogaster. PLoS ONE. 2012;7: e50679. doi: 10.1371/journal.pone.0050679 23272066

54. Dionne MS, Pham LN, Shirasu-Hiza M, Schneider DS. Akt and foxo Dysregulation Contribute to Infection-Induced Wasting in Drosophila. Curr Biol. 2006;16: 1977–1985. doi: 10.1016/j.cub.2006.08.052 17055976

55. Paredes JC, Herren JK, Schüpfer F, Lemaitre B. The role of lipid competition for endosymbiont-mediated protection against parasitoid wasps in Drosophila. mBio. 2016;7: e01006–16. doi: 10.1128/mBio.01006-16 27406568

56. Buchanan JL, Meiklejohn CD, Montooth KL. Energetic stress and infection generate immunity-fecundity tradeoffs in Drosophila. bioRxiv. 2018; 318568. doi: 10.1101/318568


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