Multifaceted defense against antagonistic microbes in developing offspring of the parasitoid wasp Ampulex compressa (Hymenoptera, Ampulicidae)

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Weiss, Katharina ^a   Parzefall, Christopher ^a   Herzner, Gudrun ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; MELLEIN; MICROMOLIDE; UNCLASSIFIED DRUG;

AMPULEX COMPRESSA; ARTICLE; ASPERGILLUS SYDOWII; CARCASS; COCKROACH; COCOON; CONTROLLED STUDY; ENVIRONMENTAL SANITATION; FOOD CONTAMINATION; FUMIGATION; GROWTH INHIBITION; HYMENOPTERA; IMAGO; INSECT DEVELOPMENT; LARVA; MASS FRAGMENTOGRAPHY; METARHIZIUM; METARHIZIUM BRUNNEUM; MICROBIAL IMMUNITY; NONHUMAN; PHYSICAL CHEMISTRY; PROTECTION; SERRATIA MARCESCENS; ANIMAL; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; WASP;

ANIMALS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; WASPS;

EID: 84902322571     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098784     Document Type: Article

References (83)

1. Herzner G, Schlecht A, Dollhofer V, Parzefall C, Harrar K, et al. (2013) Larvae of the parasitoid wasp Ampulex compressa sanitize their host, the American cockroach, with a blend of antimicrobials. P Natl Acad Sci U S A 110: 1369-1374.
2. Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, et al. (2013) Ants disinfect fungus-exposed brood by oral uptake and spread fo their poison. Curr Biol 23: 76-82.
3. Tragust S, Ugelvig LV, Chapuisat M, Heinze J, Cremer S (2013) Pupal cocoons affect sanitary brood care and limit fungal infections in ant colonies. BMC Evol Biol 13: 225.
4. Vilcinskas A, Mukherjee K, Vogel H (2013) Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. P Royal Soc B: Biol Sci 280: 20122113.
5. Rozen DE, Engelmoer DJP, Smiseth PT (2008) Antimicrobial strategies in burying beetles breeding on carrion. P Natl Acad Sci 105: 17890-17895.
6. Gross J, Eben A, Müller I, Wensing A (2010) A well protected intruder: The effective antimicrobial defence of the invasive ladybird Harmonia axyridis. J Chem Ecol 36: 1180-1188.
7. Gross J, Schumacher K, Schmidtberg H, Vilcinskas A (2008) Protected by fumigants: beetle perfumes in antimicrobial defense. J Chem Ecol 34: 179-188.
8. Herzner G, Strohm E (2007) Fighting fungi with physics: food wrapping by a solitary wasp prevents water condensation. Curr Biol 17: R46-R47. (Pubitemid 46107824)
9. Kaltenpoth M, Goettler W, Herzner G, Strohm E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15: 475-479. (Pubitemid 40323536)
10. Rosengaus RB, Mead K, Du Comb WS, Benson RW, Godoy VG (2013) Nest sanitation through defecation: antifungal properties of wood cockroach feces. Naturwissenschaften 100: 1051-1059.
11. Schmidtberg H, Röhrich C, Vogel H, Vilcinskas A (2013) A switch from constitutive chemical defence to inducible innate immune responses in the invasive ladybird Harmonia axyridis. Biol Letters 9: 20130006.
12. Bulmer MS, Bachelet I, Raman R, Rosengaus RB, Sasisekharan R (2009) Targeting an antimicrobial effector function in insect immunity as a pest control strategy. P Natl Acad Sci U S A 106: 12652-12657.
13. Hamilton C, Lay F, Bulmer MS (2011) Subterranean termite prophylactic secretions and external antifungal defenses. J Ins Physiol 57: 1259-1266.
14. Rolff J, Reynolds SE (2009) Insect Infection and Immunity. Evolution, Ecology and Mechanisms. Oxford: Oxford University Press.
15. Beckage NE, editor (2008) Insect immunology. San Diego, USA: Academic Press.
16. Reber A, Purcell J, Buechel SD, Buri P, Chapuisat M (2011) The expression and impact of antifungal grooming in ants. J Evol Biol 24: 954-964.
17. Griffiths HM, Hughes WOH (2010) Hitchhiking and the removal of microbial contaminants by the leaf-cutting ant Atta colombica. Ecol Entomol 35: 529-537.
18. Batra S, Bohart GE (1969) Alkali bees: response of adults to pathogenic fungi in brood cells. Science 165: 607-608.
19. Chouvenc T, Efstathion CA, Elliott ML, Su N-Y (2013) Extended disease resistance emerging from the faecal nest of a subterranean termite. P Royal Soc B: Biol Sci 280: 20131885.
20. Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, et al. (2008) Bacterial protection of beetle-fungus mutualism. Science 322: 63-63.
21. Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: 701-704. (Pubitemid 29197647)
22. Röhrich CR, Ngwa CJ, Wiesner J, Schmidtberg H, Degenkolb T, et al. (2012) Harmonine, a defence compound from the harlequin ladybird, inhibits mycobacterial growth and demonstrates multi-stage antimalarial activity. Biol Letters 8: 308-311.
23. Yek SH, Nash DR, Jensen AB, Boomsma JJ (2012) Regulation and specificity of antifungal metapleural gland secretion in leaf-cutting ants. P Roy Soc B: Biol Sci 279: 4215-4222.
24. Gasch T, Schott M, Wehrenfennig C, Düring R-A, Vilcinskas A (2013) Multifunctional weaponry: The chemical defenses of earwigs. J Ins Physiol 59: 1186-1193.
25. Kroiss J, Kaltenpoth M, Schneider B, Schwinger MG, Hertweck C, et al. (2010) Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol 6: 261-263.
26. Koehler S, Doubský J, Kaltenpoth M (2013) Dynamics of symbiont-mediated antibiotic production reveal efficient long-term protection for beewolf offspring. Front Zool 10: 3.
27. Keasar T, Sheffer N, Glusman G, Libersat F (2006) Host-handling behavior: An innate component of foraging behavior in the parasitoid wasp Ampulex compressa. Ethology 112: 699-706. (Pubitemid 43882156)
28. Libersat F (2003) Wasp uses venom cocktail to manipulate the behavior of its cockraoch prey. J Comp Physiol A 189: 497-508.
29. Williams FX (1942) Ampulex compressa (Fabr.), a cockroach hunting wasp introduced from New Caledonia into Hawaii. P Hawaii Entomol Soc 11: 221-233.
30. Heitmans WRB (1990) Which information is used to assess host size and sex of the progeny? Experiments with a solitary aculeate ectoparasitoid of cockroaches. Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society 1: 13-18.
31. Fakoorziba M, Eghbal F, Hassanzadeh J, Moemenbellah-Fard M (2010) Cockroaches (Periplaneta americana and Blattella germanica) as potential vectors of the pathogenic bacteria found in nosocomial infections. Ann Trop Med Parasit 104: 521-528.
32. Prado AM, Gir E, Pereira MS, Reis C, Pimenta FC (2006) Profile of antimicrobial resistance of bacteria isolated from cockroaches (Periplaneta americana) in a Brazilian health care institution. Braz J Infect Dis 10: 26-32. (Pubitemid 43881090)
33. Pai H-H, Chen W-C, Peng C-F (2004) Cockroaches as potential vectors of nosocomial infections. Infect Cont Hosp Ep 25: 979-984. (Pubitemid 39551221)
34. Pai H-H, Chen W-C, Peng C-F (2005) Isolation of bacteria with antibiotic resistance from household cockroaches (Periplaneta americana and Blattella germanica). Acta Trop 93: 259-265. (Pubitemid 40348829)
35. Chaichanawongsaroj N, Vanichayatanarak K, Pipatkullachat T, Polrojpanya M, Somkiatcharoen S (2004) Isolation of gram-negative bacteria from cockroaches trapped from urban environment. SE Asian J Trop Med 35: 681-684. (Pubitemid 39486441)
36. Baumholtz MA, Parish LC, Witkowski JA, Nutting WB (1997) The medical importance of cockroaches. Int J Dermatol 36: 90-96. (Pubitemid 27144222)
37. Trienens M, Keller NP, Rohlfs M (2010) Fruit, flies and filamentous fungi-experimental analysis of animal-microbe competition using Drosophila melanogaster and Aspergillus mould as a model system. OIKOS 119: 1765-1775.
38. Janzen D (1977) Why fruits rot, seeds mold, and meat spoils. Am Nat 111: 691- 713.
39. Ma C, Case RJ, Wang Y, Zhang HJ, Tan GT, et al. (2005) Anti-tuberculosis constituents from the stem bark of Micromelum hirsutum. Planta Med 71: 261-267. (Pubitemid 40476784)
40. Dai JR, Carté BK, Sidebottom PJ, Yew ALS, Ng SB, et al. (2001) Circumdatin G, a new alkaloid from the fungus Aspergillus ochraceus. J Nat Prod 64: 125-126. (Pubitemid 32107797)
41. Krohn K, Bahramsari R, Flörke U, Ludewig K, Kliche-Spory C, et al. (1997) Dihydroisocoumarins from fungi: Isolation, structure elucidation, circular dichroism and biological activity. Phytochemistry 45: 313-320. (Pubitemid 27180901)
42. Höller U, König GM, Wright AD (1999) Three new metabolites from marine-derived fungi of the genera Coniothyrium and Microsphaeropsis. J Nat Prod 62: 114-118. (Pubitemid 29071389)
43. Zhao J, Zhang Y, Wang L, Wang J, Zhang C (2012) Bioactive secondary metabolites from Nigrospora sp. LLGLM003, an endophytic fungus of the medicinal plant Moringa oleifera Lam. World J Microb and Biot 28: 2107-2112.
44. Oliveira CM, Regasini LO, Silva GH, Pfenning LH, Young MCM, et al. (2011) Dihydroisocoumarins produced by Xylaria sp. and Penicillium sp., endophytic fungi associated with Alibertia macrophylla and Piper aduncum. Phytochem Lett 4: 93-96.
45. Feng Z, Nenkep V, Yun K, Zhang D, Choi H, et al. (2010) Biotransformation of Bioactive (-)-Mellein by a Marine Isolate of Bacterium Stappia sp. J Microbiol Biotechn 20: 985-987.
46. El-Mehalawy AA, Abd-Allah NA, Mohammed RM, Abu-Shady MR (2005) Actinomycetes antagonizing plant and human pathogenic fungi, II. Factors affecting antifungal production and chemical characterization of the active components. Int J Agricul Biol 7: 188-196.
47. Yuan H, He R, Wan B, Wang Y, Pauli GF, et al. (2008) Modification of the side chain of micromolide, an anti-tuberculosis natural product. Bioorg Med Chem Lett 18: 5311-5315.
48. Rukachaisirikul V, Arunpanichlert J, Sukpondma Y, Phongpaichit S, Sakayaroj J (2009) Metabolites from the endophytic fungi Botryosphaeria rhodina PSU-M35 and PSU-M114. Tetrahedron 65: 10590-10595.
49. Haak U, Hölldobler B, Bestmann H, Kern F (1996) Species-specificity in trail pheromones and Dufour's gland contents of Camponotus atriceps and C. floridanus (Hymenoptera: Formicidae). Chemoecology 7: 85-93.
50. Muneer M, Qamar M, Bahnemann D (2005) Photoinduced electron transfer reaction of few selected organic systems in presence of titanium dioxide. J Mol Catal A: Chemical 234: 151-157. (Pubitemid 40612957)
51. Lemos AA, Lemos JA, Prado MA, Pimenta FC, Gir E, et al. (2006) Cockroaches as carriers of fungi of medical importance. Mycoses 49: 23-25.
52. Führer E, Willers D (1986) The anal secretion of the endoparasitic larva Pimpla turionellae : sites of production and effects. J Insect Physiol 32: 361-367.
53. Herzner G, Engl T, Strohm E (2011) Cryptic combat against competing microbes is a costly component of parental care in a digger wasp. Anim Behav 82: 321-328.
54. Cotter SC, Topham E, Price AJP, Kilner RM (2010) Fitness costs associated with mounting a social immune response. Ecol Lett 13: 1114-1123.
55. Degenkolb T, Düring RA, Vilcinskas A (2011) Secondary metabolites released by the burying beetle Nicrophorus vespilloides: chemical analyses and possible ecological functions. J Chem Ecol 37: 724-735.
56. Führer E, Rosner S, Schmied A, Wegensteiner R (2001) Studies on the significance of pathogenic fungi in the population dynamics of the lesser spruce sawfly, Pristiphora abietina Christ. (Hym., Tenthredinidae). J Applied Entomol 125: 235-242.
57. Thompson P, Hepburn H (1978) Changes in chemical and mechanical properties of honeybee (Apis mellifera adansonii L.) cuticle during development. J Comp Physiol 126: 257-262.
58. Vänninen I, Hokkanen H (1997) Efficacy of entomopathogenic fungi and nematodes against Argyresthia conjugella (Lep.: Yponomeutidae). Entomophaga 42: 377-385. (Pubitemid 127760847)
59. Gochnauer T, Boch R, Margetts V (1979) Inhibition of Ascosphaera apis by citral and geraniol. J Invertebr Pathol 34: 57-61.
60. Wang L, Dong JY, Song HC, Shen KZ, Wang LM, et al. (2008) Screening and isolation of antibacterial activities of the fermentative extracts of freshwater fungi from Yunnan Province, China. Ann Microbiol 58: 579-584.
61. Sun CM, Toia RF (1993) Biosynthetic studies on ant metabolites of mellein and 2, 4-dihydroxyacetophenone from {1, 2-13C2} Acetate. J Nat Prod 56: 953-956.
62. Schulz B, Sucker J, Aust H, Krohn K, Ludewig K, et al. (1995) Biologically active secondary metabolites of endophytic Pezicula species. Mycol Res 99: 1007-1015.
63. Hejazi A, Falkiner FR (1997) Serratia marcescens. J Med Microbiol 46: 903-912. (Pubitemid 27462659)
64. Anǧ-Küçüker M, Büyükbaba-Boral Ö, Tolun V, Törümküney D, Susever S, et al. (1999) Effect of Some Antibiotics on Pigmentation in Serratia marcescens. ZBL Bakt 289: 781-785. (Pubitemid 30097539)
65. Iranshahi M, Shahverdi AR, Mirjani R, Amin G, Shafiee A (2004) Umbelliprenin from Ferula persica roots inhibits the red pigment production in Serratia marcescens. Z Naturforsch 59c: 506-508. (Pubitemid 39098546)
66. Cardoza YJ, Klepzig KD, Raffa KF (2006) Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecol Entomol 31: 636-645. (Pubitemid 44934339)
67. Chen J, Henderson G, Grimm C, Lloyd S, Laine R (1998) Termites fumigate their nests with naphthalene. Nature 392: 558-559. (Pubitemid 28207701)
68. Chen J, Henderson G, Grimm CC, Lloyd SW, Laine RA (1998) Naphthalene in Formosan subterranean termite carton nests. J Agr Food Chem 46: 2337-2339. (Pubitemid 128491155)
69. Wiltz BA, Henderson G, Chen J (1998) Effect of naphthalene, butylated hydroxytoluene, dioctyl phthalate, and adipic dioctyl ester, chemicals found in the nests of the formosan subterranean termite (Isoptera: Rhinotermitidae) on a saprophytic Mucor sp.(Zygomycetes: Mucorales). Environ Entomol 27: 936-940. (Pubitemid 128482886)
70. Wright MS, Lax AR, Henderson G, Chen J (2000) Growth response of Metarhizium anisopliae to two Formosan subterranean termite nest volatiles, naphthalene and fenchone. Mycologia 92: 42-45.
71. Rosengaus R, Traniello J, Lefebvre M, Maxmen A (2004) Fungistatic activity of the sternal gland secretion of the dampwood termite Zootermopsis angusticollis. Insect Soc 51: 259-264. (Pubitemid 39147585)
72. Rosengaus RB, Lefebvre ML, Traniello JFA (2000) Inhibition of fungal spore germination by Nasutitermes: evidence for a possible antiseptic role of soldier defensive secretions. J Chem Ecol 26: 21-39. (Pubitemid 30091822)
73. Gross J, Schmidtberg H (2009) Glands of leaf beetle larvae - protective structures against attacking predators and pathogens. In: Jolivet P, Santiago-Blay J, Schmidt M, editors. Research on Chrysomelidae. Leiden, The Netherlands : Koninklijke Brill.pp. 177-189.
74. Suwannarach N, Kumla J, Bussaban B, Nuangmek W, Matsui K, et al. (2013) Biofumigation with the endophytic fungus Nodulisporium spp. CMU-UPE34 to control postharvest decay of citrus fruit. Crop Prot 45: 63-70.
75. Tunc S, Chollet E, Chalier P, Preziosi-Belloy L, Gontard N (2007) Combined effect of volatile antimicrobial agents on the growth of Penicillium notatum. Int J Food Microbiol 113: 263-270. (Pubitemid 46123635)
76. Herzner G, Ruther J, Goller S, Schulz S, Goettler W, et al. (2011) Structure, chemical composition and putative function of the postpharyngeal gland of the emerald cockroach wasp, Ampulex compressa (Hymenoptera, Ampulicidae). Zoology 114: 36-45.
77. Clarke K, Green R (1988) Statistical design and analysis for a 'biological effects' study. Mar Ecol - Prog Ser 46: 213-226.
78. Legendre P, Legendre L (1998) Numerical Ecology. Amsterdam: Elsevier Science B.V.
79. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Paleo Electronica 4: Art. 4: 9pp.
80. Sikorowski P, Lawrence A, Inglis G (2001) Effects of Serratia marcescens on rearing of the tobacco budworm. American Entomologist 47: 51-60. (Pubitemid 33253424)
81. Li B, Yu R, Liu B, Tang Q, Zhang G, et al. (2011) Characterization and comparison of Serratia marcescens isolated from edible cactus and from silkworm for virulence potential and chitosan susceptibility. Braz J Microbiol 42: 96-104.
82. Secil ES, Sevim A, Demirbag Z, Demir I (2012) Isolation, characterization and virulence of bacteria from Ostrinia nubilalis (Lepidoptera: Pyralidae). Biologia 67: 767-776.
83. Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101: 512-530.