Dynamics of symbiont-mediated antibiotic production reveal efficient long-term protection for beewolf offspring

Frontiers in Zoology

Volumn 10, Issue 1, 2013, Pages

  Koehler, Sabrina ^a   Doubský, Jan ^a,b   Kaltenpoth, Martin ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b API Synthesis Department   (Czech Republic)

Author keywords

Antibiotic; Crabronidae; Defensive symbiosis; Hymenoptera; Protective mutualism; Streptochlorin synthesis; Streptomyces

Indexed keywords

BACTERIA (MICROORGANISMS); CRABRONIDAE; FUNGI; HEXAPODA; HYMENOPTERA; PHILANTHUS TRIANGULUM; SPHECIDAE; STREPTOMYCES;

EID: 84873040990     PISSN: None     EISSN: 17429994     Source Type: Journal    
DOI: 10.1186/1742-9994-10-3     Document Type: Article

References (93)

1. Rantala MJ, Roff DA. An analysis of trade-offs in immune function, body size and development time in the mediterranean field cricket, Gryllus bimaculatus. Funct Ecol 2005, 19(2):323-330.
2. Vainio L, Hakkarainen H, Rantala MJ, Sorvari J. Individual variation in immune function in the ant Formica exsecta; effects of the nest, body size and sex. Evol Ecol 2004, 18(1):75-84.
3. Soler JJ, de Neve L, Perez-Contreras T, Soler M, Sorci G. Trade-off between immunocompetence and growth in magpies: an experimental study. Proc Biol Sci 2003, 270(1512):241-248. 10.1098/rspb.2002.2217, 1691245, 12614572.
4. Schmid-Hempel P. Variation in immune defence as a question of evolutionary ecology. Proc Biol Sci 2003, 270(1513):357-366. 10.1098/rspb.2002.2265, 1691258, 12639314.
5. Herzner G, Strohm E. Fighting fungi with physics: food wrapping by a solitary wasp prevents water condensation. Curr Biol 2007, 17(2):R46-R47. 10.1016/j.cub.2006.11.060, 17240324.
6. Janzen DH. Why fruits rot, seeds mold, and meat spoils. Am Nat 1977, 111(980):691-713.
7. Strohm E, Linsenmair KE. Females of the European beewolf preserve their honeybee prey against competing fungi. Ecol Entomol 2001, 26(2):198-203.
8. Degenkolb T, During RA, Vilcinskas A. Secondary metabolites released by the burying beetle Nicrophorus vespilloides: chemical analyses and possible ecological functions. J Chem Ecol 2011, 37(7):724-735. 10.1007/s10886-011-9978-4, 21667150.
9. Bot ANM, Ortius-Lechner D, Finster K, Maile R, Boomsma JJ. Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insectes Soc 2002, 49(4):363-370.
10. Batra SWT. Behavior of some social and solitary halictine bees within their nests: a comparative study (Hymenoptera: Halicitidae). J Kans Entomol Soc 1968, 41:120-133.
11. Reber A, Purcell J, Buechel SD, Buri P, Chapuisat M. The expression and impact of antifungal grooming in ants. J Evol Biol 2011, 24(5):954-964. 10.1111/j.1420-9101.2011.02230.x, 21306465.
12. Fefferman NH, Traniello JFA, Rosengaus RB, Calleri DV. Disease prevention and resistance in social insects: modeling the survival consequences of immunity, hygienic behavior, and colony organization. Behav Ecol Sociobiol 2007, 61(4):565-577.
13. Hughes WOH, Eilenberg J, Boomsma JJ. Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc Biol Sci 2002, 269(1502):1811-1819. 10.1098/rspb.2002.2113, 1691100, 12350269.
14. Cremer S, Armitage SAO, Schmid-Hempel P. Social immunity. Curr Biol 2007, 17(16):R693-R702. 10.1016/j.cub.2007.06.008, 17714663.
15. Hamilton C, Lejeune BT, Rosengaus RB. Trophallaxis and prophylaxis: social immunity in the carpenter ant Camponotus pennsylvanicus. Biol Lett 2011, 7(1):89-92. 10.1098/rsbl.2010.0466, 3030872, 20591850.
16. Schmid-Hempel P. Parasites in social insects 1998, Princeton: Princeton University Press.
17. Konrad M, Vyleta ML, Theis FJ, Stock M, Tragust S, Klatt M, Drescher V, Marr C, Ugelvig LV, Cremer S. Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS Biol 2012, 10(4):e1001300. 10.1371/journal.pbio.1001300, 3317912, 22509134.
18. Ugelvig LV, Cremer S. Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr Biol 2007, 17(22):1967-1971. 10.1016/j.cub.2007.10.029, 17980590.
19. Field J, Brace S. Pre-social benefits of extended parental care. Nature 2004, 428(6983):650-652. 10.1038/nature02427, 15071594.
20. Kaltenpoth M, Gottler W, Herzner G, Strohm E. Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 2005, 15(5):475-479. 10.1016/j.cub.2004.12.084, 15753044.
21. Kellner RLL. Molecular identification of an endosymbiotic bacterium associated with pederin biosynthesis in Paederus sabaeus (Coleoptera: Staphylinidae). Insect Biochem Mol Biol 2002, 32(4):389-395. 10.1016/S0965-1748(01)00115-1, 11886773.
22. Cane JH, Gerdin S, Wife G. Mandibular gland secretions of solitary bees (Hymenoptera, Apoidea) - potential for nest cell desinfection. J Kans Entomol Soc 1983, 56(2):199-204.
23. Rozen DE, Engelmoer DJP, Smiseth PT. Antimicrobial strategies in burying beetles breeding on carrion. Proc Natl Acad Sci USA 2008, 105(46):17890-17895. 10.1073/pnas.0805403105, 2584725, 19001269.
24. Marchini D, Marri L, Rosetto M, Manetti AGO, Dallai R. Presence of antibacterial peptides on the laid egg chorion of the medfly Ceratitis capitata. Biochem Biophys Res Commun 1997, 240(3):657-663. 10.1006/bbrc.1997.7694, 9398621.
25. Cotter SC, Kilner RM. Sexual division of antibacterial resource defence in breeding burying beetles, Nicrophorus vespilloides. J Anim Ecol 2010, 79(1):35-43. 10.1111/j.1365-2656.2009.01593.x, 19627394.
26. Burse A, Frick S, Discher S, Tolzin-Banasch K, Kirsch R, Strauss A, Kunert M, Boland W. Always being well prepared for defense: the production of deterrents by juvenile Chrysomelina beetles (Chrysomelidae). Phytochemistry 2009, 70(15-16):1899-1909.
27. Discher S, Burse A, Tolzin-Banasch K, Heinemann SH, Pasteels JM, Boland W. A versatile transport network for sequestering and excreting plant glycosides in leaf beetles provides an evolutionary flexible defense strategy. Chem Bio Chem 2009, 10(13):2223-2229. 10.1002/cbic.200900226, 19623597.
28. Feld BK, Pasteels JM, Boland W. Phaedon cochleariae and Gastrophysa viridula (Coleoptera: Chrysomelidae) produce defensive iridoid monoterpenes de novo and are able to sequester glycosidically bound terpenoid precursors. Chemoecology 2001, 11(4):191-198.
29. Mattoso TC, Moreira DD, Samuels RI. Symbiotic bacteria on the cuticle of the leaf-cutting ant Acromyrmex subterraneus subterraneus protect workers from attack by entomopathogenic fungi. Biol Lett 2011, 8(3):461-464.
30. Currie CR, Mueller UG, Malloch D. The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci USA 1999, 96(14):7998-8002. 10.1073/pnas.96.14.7998, 22176, 10393936.
31. Brownlie JC, Johnson KN. Symbiont-mediated protection in insect hosts. Trends Microbiol 2009, 17(8):348-354. 10.1016/j.tim.2009.05.005, 19660955.
32. Oliver KM, Russell JA, Moran NA, Hunter MS. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 2003, 100(4):1803-1807. 10.1073/pnas.0335320100, 149914, 12563031.
33. Scott JJ, Oh DC, Yuceer MC, Klepzig KD, Clardy J, Currie CR. Bacterial protection of beetle-fungus mutualism. Science 2008, 322(5898):63. 10.1126/science.1160423, 2761720, 18832638.
34. Koch H, Schmid-Hempel P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci USA 2011, 108(48):19288-19292. 10.1073/pnas.1110474108, 3228419, 22084077.
35. Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 2004, 49:71-92. 10.1146/annurev.ento.49.061802.123416, 14651457.
36. Forsgren E, Olofsson TC, Vásquez A, Fries I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 2009, 41(1):99-108.
37. Evans JD, Lopez DL. Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). J Econ Entomol 2004, 97(3):752-756. 10.1603/0022-0493(2004)097[0752:BPIAIR]2.0.CO;2, 15279248.
38. de Souza DJ, Bezier A, Depoix D, Drezen J-M, Lenoir A. Blochmannia endosymbionts improve colony growth and immune defence in the ant Camponotus fellah. BMC Microbiol 2009, 9:29. 10.1186/1471-2180-9-29, 2660346, 19200360.
39. Oh D-C, Scott JJ, Currie CR, Clardy J. Mycangimycin, a polyene peroxide from a mutualist Streptomyces sp. Org Lett 2009, 11(3):633-636. 10.1021/ol802709x, 2640424,2640424, 19125624.
40. Kroiss J, Kaltenpoth M, Schneider B, Schwinger MG, Hertweck C, Maddula RK, Strohm E, Svatos A. Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol 2010, 6(4):261-263. 10.1038/nchembio.331, 20190763.
41. Currie CR, Scott JA, Summerbell RC, Malloch D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 1999, 398(6729):701-704.
42. Kaltenpoth M. Actinobacteria as mutualists: general healthcare for insects?. Trends Microbiol 2009, 17(12):529-535. 10.1016/j.tim.2009.09.006, 19853457.
43. Seipke RF, Kaltenpoth M, Hutchings MI. Streptomyces as symbionts: an emerging and widespread theme?. FEMS Microbiol Rev 2012, 36(4):862-876. 10.1111/j.1574-6976.2011.00313.x, 22091965.
44. Watve MG, Tickoo R, Jog MM, Bhole BD. How many antibiotics are produced by the genus Streptomyces?. Arch Microbiol 2001, 176(5):386-390. 10.1007/s002030100345, 11702082.
45. Solecka J, Zajko J, Postek M, Rajnisz A. Biologically active secondary metabolites from actinomycetes. Cent Eur J Biol 2012, 7(3):373-390.
46. Berdy J. Recent advances in and prospects of antibiotic research. Process Biochem 1980, 15(7):28-35.
47. Dufour N, Rao RP. Secondary metabolites and other small molecules as intercellular pathogenic signals. FEMS Microbiol Lett 2011, 314(1):10-17. 10.1111/j.1574-6968.2010.02154.x, 21114519.
48. Linares JF, Gustafsson I, Baquero F, Martinez JL. Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci USA 2006, 103(51):19484-19489. 10.1073/pnas.0608949103, 1682013, 17148599.
49. Yim G, Wang HH, Davies J. Antibiotics as signalling molecules. Philos T Roy Soc B 2007, 362(1483):1195-1200.
50. Haeder S, Wirth R, Herz H, Spiteller D. Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc Natl Acad Sci USA 2009, 106(12):4742-4746. 10.1073/pnas.0812082106, 2660719, 19270078.
51. Cafaro MJ, Poulsen M, Little AE, Price SL, Gerardo NM, Wong B, Stuart AE, Larget B, Abbot P, Currie CR. Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria. Proc Biol Sci 2011, 278(1713):1814-1822. 10.1098/rspb.2010.2118, 3097832, 21106596.
52. Poulsen M, Currie CR. Symbiont interactions in a tripartite mutualism: exploring the presence and impact of antagonism between two fungus-growing ant mutualists. PLoS One 2010, 5(1):e8748. 10.1371/journal.pone.0008748, 2806923, 20090958.
53. Poulsen M, Cafaro MJ, Erhardt DP, Little AEF, Gerardo NM, Tebbets B, Klein BS, Currie CR. Variation in Pseudonocardia antibiotic defence helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants. Environ Microbiol Rep 2010, 2(4):534-540. 3418327, 22896766.
54. Kaltenpoth M, Yildirim E, Guerbuez MF, Herzner G, Strohm E. Refining the roots of the beewolf-Streptomyces symbiosis: antennal symbionts in the rare genus Philanthinus (Hymenoptera, Crabronidae). Appl Environ Microbiol 2012, 78(3):822-827. 10.1128/AEM.06809-11, 3264120, 22113914.
55. Kaltenpoth M, Schmitt T, Polidori C, Koedam D, Strohm E. Symbiotic streptomycetes in antennal glands of the south American digger wasp genus Trachypus (Hymenoptera, Crabronidae). Physiol Entomol 2010, 35(2):196-200.
56. Goettler W, Kaltenpoth M, Herzner G, Strohm E. Morphology and ultrastructure of a bacteria cultivation organ: the antennal glands of female european beewolves, Philanthus triangulum (hymenoptera, crabronidae). Arthropod Struct Dev 2007, 36(1):1-9. 10.1016/j.asd.2006.08.003, 18089083.
57. Strohm E, Linsenmair KE. Leaving the cradle: how beewolves (Philanthus triangulum F.) obtain the necessary spatial information for emergence. Zoology 1995, 98:137-146.
58. Kaltenpoth M, Goettler W, Koehler S, Strohm E. Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission. Evol Ecol 2010, 24(2):463-477.
59. Chater KF, Biro S, Lee KJ, Palmer T, Schrempf H. The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 2010, 34(2):171-198. 10.1111/j.1574-6976.2009.00206.x, 20088961.
60. Kitani S, Miyamoto KT, Takamatsu S, Herawati E, Iguchi H, Nishitomi K, Uchida M, Nagamitsu T, Omura S, Ikeda H. Avenolide, a Streptomyces hormone controlling antibiotic production in Streptomyces avermitilis. Proc Natl Acad Sci USA 2011, 108(39):16410-16415. 10.1073/pnas.1113908108, 3182739, 21930904.
61. Dharmaraj S. Marine Streptomyces as a novel source of bioactive substances. World J Microbiol Biotechnol 2010, 26(12):2123-2139.
62. Berdy J. New ways to obtain antibiotics. Chin J Antibiot 1984, 7:272-290.
63. Champness WC, Chater KF. Regulation and integration of antibiotic production and morphological differentiation in Streptomyces spp. Regulation of bacterial differentiation 1994, 61-93. Washington, DC: American Society for Microbiology, Piggot P, Moran CP, Youngman P.
64. Miyadoh S. Research on antibiotic screening in Japan over the last decade: a producing microorganisms approach. Actinomycetologica 1993, 7:100-106.
65. Hopwood DA. Streptomyces in nature and medicine: the antibiotic makers 2007, New York: Oxford University Press.
66. Chater KF. A morphological and genetic mapping study of white colony mutants of Streptomyces coelicolor. J Gen Microbiol 1972, 72(AUG):9-28.
67. Ryding NJ, Bibb MJ, Molle V, Findlay KC, Chater KF, Buttner MJ. New sporulation loci in Streptomyces coelicolor A3(2). J Bacteriol 1999, 181(17):5419-5425. 94051, 10464216.
68. Willemse J, Mommaas AM, van Wezel GP. Constitutive expression of ftsZ overrides the whi developmental genes to initiate sporulation of Streptomyces coelicolor. Antonie van Leeuwenhoek 2012, 101(3):619-632. 10.1007/s10482-011-9678-7, 3278627, 22113698.
69. Flärdh K, Leibovitz E, Buttner MJ, Chater KF. Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Mol Microbiol 2000, 38(4):737-749. 10.1046/j.1365-2958.2000.02177.x, 11115109.
70. Vazquez-Ramos JM, Mandelstam J. Inhibition of sporulation by DNA gyrase inhibitors. J Gen Microbiol 1981, 127:11-17.
71. Goss WA, Deitz WH, Cook TM. Mechanism of action of nalidixic acid on escherichia coli - inhibition of deoxyribonucleic acid synthesis. J Bacteriol 1965, 89(4):1068-1074. 277597, 14276097.
72. Staudenbauer WL. Replication of Escherichia coli DNA in vitro: inhibition by oxolinic acid. Eur J Biochem 1976, 62(3):491-497. 10.1111/j.1432-1033.1976.tb10183.x, 770163.
73. Smith DH, Davis BD. Mode of action of novobiocin in Escherichia coli. J Bacteriol 1967, 93(1):71-79. 314970, 5335903.
74. van Wezel GP, McDowall KJ. The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat Prod Rep 2011, 28(7):1311-1333. 10.1039/c1np00003a, 21611665.
75. Huang CH, Renew JE, Pinkston K, Sedlak DL. Occurrence and fate of antibiotic compounds in municipal wastewater and animal waste. Proc Water Environ Fed 2001, 686-697.
76. Jefferys EG. The stability of antibiotics in soils. J Gen Microbiol 1952, 7(3-4):295-312.
77. Kuehne M, Ihnen D, Moeller G, Agthe O. Stability of tetracycline in water and liquid manure. J Vet Med A 2000, 47(6):379-384.
78. Golet EM, Strehler A, Alder AC, Giger W. Determination of fluoroquinolone antibacterial agents in sewage sludge and sludge-treated soil using accelerated solvent extraction followed by solid-phase extraction. Anal Chem 2002, 74(21):5455-5462. 10.1021/ac025762m, 12433073.
79. Giger W, Alder AC, Golet EM, Kohler HPE, McArdell CS, Molnar E, Siegrist H, Suter MJF. Occurrence and fate of antibiotics as trace contaminants in wastewaters, sewage sludges, and surface waters. Chimia 2003, 57(9):485-491.
80. Kreuzig R, Holtge S. Investigations on the fate of sulfadiazine in manured soil: laboratory experiments and test plot studies. Environ Toxicol Chem 2005, 24(4):771-776. 10.1897/03-582R.1, 15839548.
81. Schmidt B, Ebert J, Lamshoeft M, Thiede B, Schumacher-Buffel R, Ji R, Corvini PFX, Schaeffer A. Fate in soil of C-14-sulfadiazine residues contained in the manure of young pigs treated with a veterinary antibiotic. J Environ Sci Health B 2008, 43(1):8-20. 10.1080/03601230701734824, 18161568.
82. Oroshnik W, Mebane AD. The polyene antifungal antibiotics. Fort Chem Org Nat 1963, 21:17-79.
83. Raab WP. Natamycin (pimaricin), its properties and possibilities in medicine 1972, Stuttgart: Georg Thieme Verlag.
84. Bonner DP, Mechlinski W, Schaffner CP. Stability studies with amphotericin B and amphotericin B methyl ester. J Antibiot 1975, 28:132-135. 10.7164/antibiotics.28.132, 234414.
85. Mouton JW. Combination therapy as a tool to prevent emergence of bacterial resistance. Infection 1999, 27:S24-S28.
86. Challis GL, Hopwood DA. Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA 2003, 100:14555-14561. 10.1073/pnas.1934677100, 304118, 12970466.
87. Field J. The evolution of progressive provisioning. Behav Ecol 2005, 16(4):770-778.
88. Strohm E, Herzner G, Kaltenpoth M, Boland W, Schreier P, Geiselhardt S, Peschke K, Schmitt T. The chemistry of the postpharyngeal gland of female European beewolves. J Chem Ecol 2008, 34(5):575-583. 10.1007/s10886-008-9447-x, 2373416, 18415061.
89. Herzner G, Schmitt T, Peschke K, Hilpert A, Strohm E. Food wrapping with the postpharyngeal gland secretion by females of the European beewolf Philanthus triangulum. J Chem Ecol 2007, 33(4):849-859. 10.1007/s10886-007-9263-8, 17334918.
90. Liu Q, Yao F, Chooi YH, Kang Q, Xu W, Li Y, Shao Y, Shi Y, Deng Z, Tang Y. Elucidation of piericidin A1 biosynthetic locus revealed a thioesterase-dependent mechanism of alpha-pyridone ring formation. Chem Biol 2012, 19(2):243-253. 10.1016/j.chembiol.2011.12.018, 22365607.
91. Lee C, Lee SY, Shin SG, Hwang S. Real-time PCR determination of rRNA gene copy number: absolute and relative quantification assays with Escherichia coli. Appl Microbiol Biotechnol 2008, 78(2):371-376. 10.1007/s00253-007-1300-6, 18074129.
92. Lee C, Kim J, Shin SG, Hwang S. Absolute and relative qPCR quantification of plasmid copy number in Escherichia coli. J Biotechnol 2006, 123(3):273-280. 10.1016/j.jbiotec.2005.11.014, 16388869.
93. Aitchison J. The statistical analysis of compositional data 1986, London: Chapman and Hall.