Larvae of the parasitoid wasp Ampulex compressa sanitize their host, the American cockroach, with a blend of antimicrobials.

Gudrun Herzner, Anja Schlecht, Veronika Dollhofer, Christopher Parzefall, Klaus Harrar, Andreas Kreuzer, Ludwig Pilsl, Joachim Ruther
Author Information
  1. Gudrun Herzner: Evolutionary Ecology Group, Institute of Zoology, University of Regensburg, 93053 Regensburg, Germany. gudrun.herzner@biologie.uni-regensburg.de

Abstract

Food resources contaminated with spoilage or pathogenic microorganisms pose severe problems to all higher organisms. Here, we describe a food-hygienic strategy of the emerald cockroach wasp Ampulex compressa. The wasp larvae develop on and inside the American cockroach Periplaneta americana, a host that can harbor various putrefactive microbes, as well as human and insect pathogens. From P. americana, we isolated the Gram-negative bacterium Serratia marcescens, which is a potent entomopathogen that can rapidly kill insect larvae. It is also known as a food contaminant and as an opportunistic human pathogen. Using behavioral observations and chemical analyses, we demonstrated that A. compressa larvae impregnate their cockroach hosts from inside with large amounts of an oral secretion containing a blend of γ-lactones and isocoumarins with (R)-(-)-mellein [(R)-(-)-3,4-diydro-8-hydroxy-3-methylisocoumarin] and micromolide [(4R,9Z)-octadec-9-en-4-olide] as dominant components. We fractionated hexane extracts of the secretion and investigated the antimicrobial properties of the fraction containing the lactones and isocoumarins, as well as of synthetic (R)-(-)-mellein and micromolide, against S. marcescens and a Gram-positive bacterium, Staphylococcus hyicus, in broth microdilution assays. The test fraction inhibited growth of both tested bacteria. The activity of the fraction against S. marcescens was explained by (R)-(-)-mellein alone, and the activity against S. hyicus was explained by the combined action of (R)-(-)-mellein and micromolide. Our data suggest that the specific combination of antimicrobials in the larval secretion provides an effective frontline defense against the unpredictable spectrum of microbes that A. compressa larvae may encounter during their development inside their cockroach hosts.

Associated Data

GENBANK | JX448402

References

  1. Int J Dermatol. 1997 Feb;36(2):90-6 [PMID: 9109002]
  2. J Gen Microbiol. 1980 Sep;120(1):173-81 [PMID: 7012273]
  3. Zoology (Jena). 2011 Feb;114(1):36-45 [PMID: 21256725]
  4. Curr Biol. 2005 Mar 8;15(5):475-9 [PMID: 15753044]
  5. Braz J Infect Dis. 2006 Feb;10(1):26-32 [PMID: 16767312]
  6. Braz J Microbiol. 2011 Jan;42(1):96-104 [PMID: 24031610]
  7. PLoS One. 2011 Feb 22;6(2):e16763 [PMID: 21364940]
  8. Mycoses. 2006 Jan;49(1):23-5 [PMID: 16367814]
  9. Proc Natl Acad Sci U S A. 2008 Nov 18;105(46):17890-5 [PMID: 19001269]
  10. J Med Microbiol. 1997 Nov;46(11):903-12 [PMID: 9368530]
  11. Infect Control Hosp Epidemiol. 2004 Nov;25(11):979-84 [PMID: 15566034]
  12. Nat Chem Biol. 2010 Apr;6(4):261-3 [PMID: 20190763]
  13. Nat Prod Rep. 2010 Jan;27(12):1737-57 [PMID: 20957283]
  14. J Chem Ecol. 2011 Jul;37(7):724-35 [PMID: 21667150]
  15. J Chem Ecol. 2001 Sep;27(9):1841-53 [PMID: 11545374]
  16. Trans R Soc Trop Med Hyg. 1989 Jan-Feb;83(1):133-5 [PMID: 2603192]
  17. Phytochemistry. 1997 May;45(2):313-20 [PMID: 9141717]
  18. Biol Lett. 2012 Apr 23;8(2):308-11 [PMID: 21937493]
  19. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005 Jun;191(6):529-34 [PMID: 15864597]
  20. J Nat Prod. 2009 Jan;72(1):8-13 [PMID: 19072711]
  21. Southeast Asian J Trop Med Public Health. 2004 Sep;35(3):681-4 [PMID: 15689087]
  22. Acta Trop. 2005 Mar;93(3):259-65 [PMID: 15716054]
  23. Phytochemistry. 2001 Nov;58(5):709-16 [PMID: 11672735]
  24. Planta Med. 2005 Mar;71(3):261-7 [PMID: 15770548]
  25. J Nat Prod. 2001 Jan;64(1):125-6 [PMID: 11170686]
  26. J Med Entomol. 1969 May;6(2):185-9 [PMID: 5807859]
  27. Ann Trop Med Parasitol. 2010 Sep;104(6):521-8 [PMID: 20863441]
  28. J Agric Food Chem. 2005 Mar 9;53(5):1678-83 [PMID: 15740058]
  29. Phytopathology. 2003 Oct;93(10):1233-9 [PMID: 18944322]
  30. J Nat Prod. 1999 Jan;62(1):114-8 [PMID: 9917295]
  31. Emerg Infect Dis. 2011 Jan;17(1):7-15 [PMID: 21192848]
  32. Org Biomol Chem. 2008 May 7;6(9):1601-4 [PMID: 18421392]
  33. J Am Chem Soc. 2011 Feb 16;133(6):1793-8 [PMID: 21166415]
  34. Curr Biol. 2007 Jan 23;17(2):R46-7 [PMID: 17240324]
  35. J Chem Ecol. 2003 Oct;29(10):2189-99 [PMID: 14682505]

MeSH Term

Animals
Anti-Infective Agents
Genes, Bacterial
Host-Parasite Interactions
Humans
Isocoumarins
Lactones
Molecular Sequence Data
Periplaneta
RNA, Bacterial
RNA, Ribosomal, 16S
Serratia marcescens
Staphylococcus hyicus
Wasps

Chemicals

Anti-Infective Agents
Isocoumarins
Lactones
RNA, Bacterial
RNA, Ribosomal, 16S

Word Cloud

Created with Highcharts 10.0.0-cockroachRcompressalarvae-melleinwaspinsidemarcescenssecretionmicromolidefractionSAmpulexAmericanamericanahostcanmicrobeswellhumaninsectbacteriumhostscontainingblendisocoumarins[hyicusactivityexplainedantimicrobialsFoodresourcescontaminatedspoilagepathogenicmicroorganismsposesevereproblemshigherorganismsdescribefood-hygienicstrategyemeralddevelopPeriplanetaharborvariousputrefactivepathogensPisolatedGram-negativeSerratiapotententomopathogenrapidlykillalsoknownfoodcontaminantopportunisticpathogenUsingbehavioralobservationschemicalanalysesdemonstratedimpregnatelargeamountsoralγ-lactones-34-diydro-8-hydroxy-3-methylisocoumarin]4R9Z-octadec-9-en-4-olide]dominantcomponentsfractionatedhexaneextractsinvestigatedantimicrobialpropertieslactonessyntheticGram-positiveStaphylococcusbrothmicrodilutionassaystestinhibitedgrowthtestedbacteriaalonecombinedactiondatasuggestspecificcombinationlarvalprovideseffectivefrontlinedefenseunpredictablespectrummayencounterdevelopmentLarvaeparasitoidsanitize

Similar Articles

Cited By