Trans-generational Immune Priming Protects the Eggs Only against Gram-Positive Bacteria in the Mealworm Beetle

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In some insects, the immunological experience of mothers is transferred to their otherwise naïve offspring, protecting them against infection. Such a maternal effect has likely evolved from selective pressure imposed by the persistence of some microbial pathogens in the environment between insect generations. If microbes are not transmitted vertically from mother to the offspring, only those able to survive in the external environment have the highest probability to infect the offspring. Therefore, early levels of immune protection transferred by mothers to their offspring might be specific of these microbes. In this study, we found that enhanced levels of antimicrobial activity in the eggs of immune challenged females of the mealworm beetle, Tenebrio molitor, were only active against Gram-positive bacteria, whatever the microorganism used for the maternal challenge. Furthermore, immune challenged females with fungi rarely transferred antimicrobial activity to their eggs. The analysis of the proteins conferring antibacterial activity in the eggs of bacterially immune-challenged mothers revealed the presence of tenecin 1, an antibacterial peptide active against Gram-positive bacteria only. These results suggest that maternal transfer of antimicrobial activity in the eggs in T. molitor might have evolved from the persistence of Gram-positive bacterial pathogens between insect generations.

Vyšlo v časopise: Trans-generational Immune Priming Protects the Eggs Only against Gram-Positive Bacteria in the Mealworm Beetle. PLoS Pathog 11(10): e32767. doi:10.1371/journal.ppat.1005178
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005178

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Zdroje

1. Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13 : 403–407. 21238360

2. Boulinier T, Staszewski V (2007) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23 : 282–288.

3. Grindstaff JL, Brodie ED, Ketterson ED (2003) Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc Biol Sci 270 : 2309–2319. 14667346

4. Hasselquist D, Nilsson JA (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos Trans R Soc Lond B Biol Sci 364 : 51–60. doi: 10.1098/rstb.2008.0137 18926976

5. Schmid-Hempel P (2005) Natural insect host-parasite systems show immune priming and specificity: puzzles to be solved. BioEssays 27 : 1026–1034. 16163710

6. Huang CC, Song YL (1999) Maternal transmission of immunity to white spot syndrome associated virus (WSSV) in shrimp (Penaeus monodon). Dev Comp Immunol 23 : 545–552. 10579383

7. Little TJ, O'Connor B, Colegrave N, Watt K., Read AF (2003) Maternal Transfer of Strain-Specific Immunity in an Invertebrate. Curr Biol 13 : 489–492. 12646131

8. Sadd BM, Kelinlogel Y, Schmid-Hempel R, Schmid-Hempel P (2005) Trans-generational immune priming in a social insect. Biol Lett 1 : 386–388. 17148213

9. Moret Y (2006) "Trans-generational immune priming": specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc R Soc B 273 : 1399–1405. 16777729

10. Sadd BM, Schmid-Hempel P (2007) Facultative but persistent trans-generational immunity via the mother's eggs in bumblebees. Curr Biol 17: R1046–1047. 18088585

11. Freitak D, Heckel DG, Vogel H (2009) Dietary-dependent trans-generational immune priming in an insect herbivore. Proc R Soc B 276 : 2617–2624. doi: 10.1098/rspb.2009.0323 19369263

12. Sadd BM, Schmid-Hempel P (2009) A distinct infection cost associated with trans-generational priming of antibacterial immunity in bumble-bees. Biol Lett 5 : 798–801. doi: 10.1098/rsbl.2009.0458 19605389

13. Roth O, Joop G, Eggert H, Hilbert J, Daniel J, Schmid-Hempel P, Kurtz J (2010) Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. J Anim Ecol 79 : 403–413. doi: 10.1111/j.1365-2656.2009.01617.x 19840170

14. Tidbury HJ, Pedersen AB, Boots M (2010) Within and transgenerational immune priming in an insect to a DNA virus. Proc Biol Sci 278 : 871–876. doi: 10.1098/rspb.2010.1517 20861049

15. Zanchi C, Troussard J-P, Martinaud G, Moreau J, Moret Y (2011) Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect. J Anim Ecol 80 : 1174–1183. doi: 10.1111/j.1365-2656.2011.01872.x 21644979

16. Moreau J, Martinaud G, Troussard J-P, Zanchi C, Moret Y (2012) Trans-generational immune priming is constrained by the maternal immune response in an insect. Oikos 121 : 1828–1832.

17. Zanchi C, Troussard JP, Moreau J, Moret Y (2012) Relationship between maternal transfer of immunity and mother fecundity in an insect. Proc R Soc B 279 : 3223–3230. doi: 10.1098/rspb.2012.0493 22535782

18. Trauer U, Hilker M (2013) Parental legacy in insects: variation of transgenerational immune priming during offspring development. PLoS One 8: e63392. doi: 10.1371/journal.pone.0063392 23700423

19. López JH, Schuehly W, Craisheim K, Riessberger-Gallé U (2014) Trans-generational immune priming in honeybees. Proc R Soc B 281 : 20140454. doi: 10.1098/rspb.2014.0454 24789904

20. Natori S, Shiraishi H, Hori S, Kobayashi A (1999) The roles of Sarcophaga defense molecules in immunity and metamorphosis. Dev Comp Immunol 23 : 317–328. 10426425

21. Meylaers K, Freitak D, Schoofs L (2007) Immunocompetence of Galleria. mellonella: sex -⁠ and stage-specific differences and the physiological cost of mounting an immune response during metamorphosis. J Insect Physiol 53 : 146–156. 17198709

22. Eleftherianos I, Baldwin H, ffrench-Constant RH, Reynolds SE (2008) Developmental modulation of immunity: changes within the feeding period of the fifth larval stage in the defence reactions of Manduca sexta to infection by Photorhabdus. J Insect Physiol 54 : 309–318. 18001766

23. Laughton AM, Boots M, Siva-Jothy MT (2011) The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge. J Insect physiol 57 : 1023–1032. doi: 10.1016/j.jinsphys.2011.04.020 21570403

24. Bulet P, Stocklin R (2005) Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept Lett 12 : 3–11. 15638797

25. Gorman MJ, Kankanala P, Kanost MR (2004) Bacterial challenge stimulates innate immune responses in extra-embryonic tissues of tobacco hornworm eggs. Insect Mol Biol 13 : 19–24. 14728663

26. Jacobs CGC, van der Zee M (2013) Immune competence in insect eggs depends on the extraembryonic serosa. Dev Comp Immunol 41 : 263–269. doi: 10.1016/j.dci.2013.05.017 23732406

27. Haine ER, Pollitt LC, Moret Y, Siva-Jothy MT, Rolff J (2008) Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor). J Insect Physiol 54 : 1090–1097. doi: 10.1016/j.jinsphys.2008.04.013 18513740

28. Tingvall T, Roos E, Engstrom Y (2001) The GATA factor Serpent is required for the onset of the humoral immune response in Drosophila embryos. Proc Natl Acad Sci U S A 98 : 3884–3888. 11274409

29. Freitak D, Schmidtberg H, Dickel F, Lochnit G, Vogel H, Vilcinskas A (2014) The maternal transfer of bacteria can mediate trans-generational immune priming in insects. Virulence 5 : 547–554. doi: 10.4161/viru.28367 24603099

30. Moret Y, Schmid-Hempel P (2000) Survival for immunity: The price of immune system activation for bumblebee workers. Science 290 : 1166–1168. 11073456

31. Lee KH, Hong SY, Oh JE, Kwon MY, Yoon JH, Lee JH, Lees BL, Moon HM (1998) Identification and characterization of the antimicrobial peptide corresponding to C-terminal beta-sheet domain of tenecin 1, an antibacterial protein of larvae of Tenebrio molitor. Biochem J 334 : 99–105. 9693108

32. Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36 : 407–477. 4568761

33. Broderick NA, Lemaitre B (2009) Recognition and response to microbial infection in Drosophila. In: Rolff J, Reynolds S, editors. Insect Infection and Immunity: Evolution, Ecology, and Mechanisms. Oxford: Oxford University Press. pp. 13–33.

34. Lehrer RI, Rosenman M, Harwig SSSL, Jackson R, Eisenhauer P (1991) Ultrasensitive assays for endogenous antimicrobial polypeptides. J Immunol Meth 137 : 167–173.

35. Schagger H, Vonjagow G (1987) Tricine Sodium Dodecyl-Sulfate polyacrylamide-gel electrophoresis for the separation of proteins in the range from 1-KDa to 100-KDa. Anal Biochem 166 : 368–379. 2449095

36. Fraune S, Augustin R, Anton-Erxleben F, Wittlieb J, Gelhaus C, Klimovich VB, Samoilovich MP, Bosch TC (2011) In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides. Proc Natl Acad Sci U S A 107 : 18067–18072.

37. Zhang S, Wang Z, Wang H (2013) Maternal immunity in fish. Dev Comp Immunol 39 : 72–78. doi: 10.1016/j.dci.2012.02.009 22387589

38. Baron OL, van West P, Industri B, Ponchet M, Dubreuil G, Gourbal B, Reichhart J-M, Coustau C (2013) Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections. PLoS Pathog 9: e1003792. doi: 10.1371/journal.ppat.1003792 24367257

39. Yu Y, Park JW, Kwon HM, Hwang HO, Jang IH, Masuda A, Kurokawa K, Nakayama H, Lee WJ, Dohmae N, et al. (2010) Diversity of innate immune recognition mechanism for bacterial polymeric meso-diaminopimelic acid-type peptidoglycan in insects. J Biol Chem 285 : 32937–32945. doi: 10.1074/jbc.M110.144014 20702416

40. Ferrari J, Vavre F (2011) Bacterial symbionts in insects or the story of communities affecting communities. Phil Trans R Soc B 366 : 1389–1400. doi: 10.1098/rstb.2010.0226 21444313

41. Lord JC, Hartzer KL, Kambhampati S (2012) A nuptially transmitted ichthyosporean symbiont of Tenebrio molitor (Coleoptera: Tenebrionidae). J Eukaryot Microbiol 59 : 246–250. doi: 10.1111/j.1550-7408.2012.00617.x 22510059

42. Lord JC (2009) Beauvaria bassiana infection of eggs of stored-product beetles. Entomol Res 39 : 155–157.

43. Jacobs CGC, Wang Y, Vogel H, Vilcinskas A, van der Zee M, Rozen DE (2014) Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides. BMC Evol Biol 14 : 208. doi: 10.1186/s12862-014-0208-x 25260512

44. Du Rand N, Laing MD (2011) Determination of insecticidal toxicity of three species of entomopathogenic spore-forming bacterial isolates against Tenebrio molitor L. (Coleoptera: Tenebrionidae) Afr J Microbiol Res 5 : 2222–2228.

45. Jurat-Fuentes JL, Jackson T. Bacterial Entomopathogens. In: Kaya H, Vera F, editors. Insect Pathology, 2nd Edition, Elsevier, 2012.

46. Meyling NV, Pell JK (2006) Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecol Entomol 31 : 162–171.

47. Dyballa N, Metzger S (2009) Fast and sensitive colloidal coomassie G-250 staining for proteins in polyacrylamide gels. J Vis Exp (30).

48. Cummings G, Finch S (2005) Inference by the eye: How to read pictures of your data. Am Psychol 60 : 170–180. 15740449

49. R Development Core Team (2011) R: A language and environment for statistical computing. Vienna, Austria, R foundation for statistical computing.

50. Bates D, Maechler M (2010) lme4: linear mixed-effects models using S4 classes. In R package version 10–6 http://CRANR-projectorg/package=lme4.

51. Dubuffet A, Zanchi C, Boutet G, Moreau J, Moret Y (2015) Data from: Trans-Generational Immune Priming Protect the Eggs only against Gram-positive Bacteria in the Mealworm Beetle. Dryad Digital Repository.