2,765
Views
12
CrossRef citations to date
0
Altmetric
Mini Review

Chemical warfare

Leaf-cutting ants defend themselves and their gardens against parasite attack by deploying antibiotic secreting bacteria

, &
Article: e23095 | Received 01 Dec 2012, Accepted 03 Dec 2012, Published online: 01 Mar 2013

References

  • Oliveira MA, Araújo MS, Marinho CGS, Ribeiro MMRR, Della Lucia TMC. Manejo de formigas-cortadeiras. In: (Della Lucia TMC ed.) Formigas cortadeiras: da bioecologia ao manejo. 1. ed. Viçosa: Editora UFV 2011; 420p.
  • Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR. The evolution of agriculture in insects. Annu Rev Ecol Evol Syst 2005; 36:563 - 95; http://dx.doi.org/10.1146/annurev.ecolsys.36.102003.152626
  • Hölldobler B, Wilson EO. The ants. 1990; 1st ed. Cambridge: Harvard University Press.
  • Littledyke M, Cherrett JM. Direct ingestion of plant sap from cut leaves by the leaf-cutting ants Atta cephalotes and Acromyrmex octospinosus (Hymenoptera: Formicidae). Bull Entomol Res 1978; 68:263 - 71; http://dx.doi.org/10.1017/S0007485300007343
  • Quinlan RJ, Cherrett JM. The role of the fungus in the diet of the leaf-cutting ant Atta cephalotes.. Ecol Entomol 1979; 4:151 - 60; http://dx.doi.org/10.1111/j.1365-2311.1979.tb00570.x
  • Silva A, Bacci M Jr., Gomes de Siqueira C, Correa Bueno O, Pagnocca FC, Aparecida Hebling MJ. Survival of Atta sexdens workers on different food sources. J Insect Physiol 2003; 49:307 - 13; http://dx.doi.org/10.1016/S0022-1910(03)00004-0; PMID: 12769984
  • Morelos-Juárez C, Walker TN, Lopes JFS, Hughes WOH. Ant farmers practice proactive personal hygiene to protect their fungus crop. Curr Biol 2010; 20:R553 - 4; http://dx.doi.org/10.1016/j.cub.2010.04.047; PMID: 20619804
  • Bot ANM, Ortius-Lechner D, Finster K, Maile R, Boomsma JJ. Variable sensitivity of fungi andbacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insectes Soc 2002; 49:363 - 70; http://dx.doi.org/10.1007/PL00012660
  • Currie CR, Scott JA, Summerbell RC, Malloch D. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 1999; 398:701 - 4; http://dx.doi.org/10.1038/19519
  • Mattoso TC, Moreira DDO, Samuels RI. Symbiotic bacteria on the cuticle of the leaf-cutting ant Acromyrmex subterraneus subterraneus protect workers from attack by entomopathogenic fungi. Biol Lett 2012; 8:461 - 4; http://dx.doi.org/10.1098/rsbl.2011.0963; PMID: 22130174
  • Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI. Ocurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol Lett 2004; 239:319 - 23; http://dx.doi.org/10.1016/j.femsle.2004.09.005; PMID: 15476982
  • Currie CR. A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol 2001; 55:357 - 80; http://dx.doi.org/10.1146/annurev.micro.55.1.357; PMID: 11544360
  • Mueller UG. Symbiont recruitment versus ant-symbiont co-evolution in the attine ant-microbe symbiosis. Curr Opin Microbiol 2012; 15:269 - 77; http://dx.doi.org/10.1016/j.mib.2012.03.001; PMID: 22445196
  • Cafaro MJ, Currie CR. Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants. Can J Microbiol 2005; 51:441 - 6; http://dx.doi.org/10.1139/w05-023; PMID: 16121221
  • Currie CR, Poulsen M, Mendenhall J, Boomsma JJ, Billen J. Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 2006; 311:81 - 3; http://dx.doi.org/10.1126/science.1119744; PMID: 16400148
  • Kost C, Lakatos T, Böttcher I, Arendholz WR, Redenbach M, Wirth R. Non-specific association between filamentous bacteria and fungus-growing ants. Naturwissenschaften 2007; 94:821 - 8; http://dx.doi.org/10.1007/s00114-007-0262-y; PMID: 17541536
  • Sen R, Ishak HD, Estrada D, Dowd SE, Hong E, Mueller UG. Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci U S A 2009; 106:17805 - 10; http://dx.doi.org/10.1073/pnas.0904827106; PMID: 19805175
  • Charnley AK. Entomopathogenic fungi and their role in pest control. In: Wicklow D.T., Soderstrom M., (eds) The mycota IV - environmental and microbial relationships. Berlim Heidelberg: Springer-Verlag 1997; p. 185-201.
  • Santos AV, de Oliveira BL, Samuels RI. Selection of entomopathogenic fungi for use in combination with sub-lethal doses of imidacloprid: perspectives for the control of the leaf-cutting ant Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae). Mycopathologia 2007; 163:233 - 40; http://dx.doi.org/10.1007/s11046-007-9009-8; PMID: 17404893
  • Wilson EO. The Insect Societies. 1. ed. Cambridge: Harvard University 1971; 548p.
  • Hughes WOH, Eilenberg J, Boomsma JJ. Trade-offs in group living: transmission and disease resistance in leafcutting ants. Proc R Soc Lond B 2002; 269: 1811-19.
  • Currie CR, Stuart AE. Weeding and grooming of pathogens in agriculture by ants. Proc Biol Sci 2001; 268:1033 - 9; http://dx.doi.org/10.1098/rspb.2001.1605; PMID: 11375087
  • Little AEF, Murakami T, Mueller UG, Currie CR. Defending against parasites: fungus-growing ants combine specialized behaviours and microbial symbionts to protect their fungus gardens. Biol Lett 2006; 2:12 - 6; http://dx.doi.org/10.1098/rsbl.2005.0371; PMID: 17148313
  • Galvanho JP, Carrera MP, Moreira DDO, Erthal M Jr., Silva CP, Samuels RI. Imidacloprid Inhibits Behavioral Defenses of the Leaf-Cutting Ant Acromyrmex subterraneus subterraneus (Hymenoptera:Formicidae). J Insect Behav 2012; In press http://dx.doi.org/10.1007/s10905-012-9328-6
  • Currie CR, Stuart AE. Weeding and grooming of pathogens in agriculture by ants. Proc Biol Sci 2001; 268:1033 - 9; http://dx.doi.org/10.1098/rspb.2001.1605; PMID: 11375087
  • Hart AG, Ratnieks FLW. Waste management in the leaf-cutting ant Atta colombica.. Behav Ecol 2002; 13:224 - 31; http://dx.doi.org/10.1093/beheco/13.2.224
  • Ballari S, Farji-Brener A, Tadey M. Waste management in the leaf-cutting ant Acromyrmex lobicornis: division of labour, aggressive behaviour, and location of external refuse dumps. J Insect Behav 2007; 20:87 - 98; http://dx.doi.org/10.1007/s10905-006-9065-9
  • Brown MJ, Bot AN, Hart AG. Mortality rates and division of labor in the leaf-cutting ant, Atta colombica.. J Insect Sci 2006; 6:1 - 8; http://dx.doi.org/10.1673/2006_06_18.1; PMID: 19537995
  • Knapp JJ, Jackson CW, Howse PE, Vilela EF. Mandibular gland secretions of leaf-cutting ants: role in defense against alien fungi. XII Congress of the International Union for the Study of Social Insects 1994; Paris: p. 109.
  • Marsaro AL Jr., Della Lucia TMC, Barbosa LCA, Maffia LA, Morandi MAB. Efeito de secreções da glândula mandibular de Atta sexdens rubropilosa Forel (Hymenoptera: Formicidae) sobre a germinação de conídios de Botrytis cinerea Pers. Fr. Neotrop Entomol 2001; 30:403 - 6; http://dx.doi.org/10.1590/S1519-566X2001000300010
  • Mendonça AdeL, da Silva CE, de Mesquita FL, Campos RdaS, Do Nascimento RR, Ximenes ECPA, et al. Antimicrobial activities of components of the glandular secretions of leaf cutting ants of the genus Atta.. Antonie Van Leeuwenhoek 2009; 95:295 - 303; http://dx.doi.org/10.1007/s10482-009-9312-0; PMID: 19214771
  • 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; 49:363 - 70; http://dx.doi.org/10.1007/PL00012660
  • Fernández-Marín H, Zimmerman JK, Rehner SA, Wcislo WT. Active use of the metapleural glands by ants in controlling fungal infection. Proc Biol Sci 2006; 273:1689 - 95; http://dx.doi.org/10.1098/rspb.2006.3492; PMID: 16769642
  • Fernández-Marín H, Zimmerman JK, Nash DR, Boomsma JJ, Wcislo WT. Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proc Biol Sci 2009; 276:2263 - 9; http://dx.doi.org/10.1098/rspb.2009.0184; PMID: 19324734
  • Poulsen M, Bot ANM, Nielsen MG, Boomsma JJ. Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants. Behav Ecol Sociobiol 2002; 52:151 - 7; http://dx.doi.org/10.1007/s00265-002-0489-8
  • Poulsen M, Bot ANM, Currie CR, Boomsma JJ. Mutualistic bacteria and a possible trade-off between alternative defense mechanisms in Acromyrmex leaf-cutting ants. Insectes Soc 2002; 49:15 - 9; http://dx.doi.org/10.1007/s00040-002-8271-5
  • Poulsen M, Bot ANM, Boomsma JJ. The effect of metapleural gland secretion on the growth of a mutualistic bacterium on the cuticle of leaf-cutting ants. Naturwissenschaften 2003; 90:406 - 9; http://dx.doi.org/10.1007/s00114-003-0450-3; PMID: 14504783
  • Mueller UG, Dash D, Rabeling C, Rodrigues A. Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution 2008; 62:2894 - 912; http://dx.doi.org/10.1111/j.1558-5646.2008.00501.x; PMID: 18752608
  • Poulsen M, Bot ANM, Currie CR, Nielsen MG, Boomsma JJ. Within-colony transmission and the cost of a mutualistic bacterium in the leaf-cutting ant Acromyrmex octospinosus.. Funct Ecol 2003; 17:260 - 9; http://dx.doi.org/10.1046/j.1365-2435.2003.00726.x
  • Currie CR, Bot ANM, Boomsma JJ. Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites. Oikos 2003; 101:91 - 102; http://dx.doi.org/10.1034/j.1600-0706.2003.12036.x
  • Boomsma JJ, Aanen DK. Rethinking crop-disease management in fungus-growing ants. Proc Natl Acad Sci U S A 2009; 106:17611 - 2; http://dx.doi.org/10.1073/pnas.0910004106; PMID: 19826091
  • Poulsen M, Cafaro M, Boomsma JJ, Currie CR. Specificity of the mutualistic association between actinomycete bacteria and two sympatric species of Acromyrmex leaf-cutting ants. Mol Ecol 2005; 14:3597 - 604; http://dx.doi.org/10.1111/j.1365-294X.2005.02695.x; PMID: 16156826
  • Poulsen M, Erhardt DP, Molinaro DJ, Lin TL, Currie CR. Antagonistic bacterial interactions help shape host-symbiont dynamics within the fungus-growing ant-microbe mutualism. PLoS One 2007; 2:e960; http://dx.doi.org/10.1371/journal.pone.0000960; PMID: 17896000
  • Zhang MM, Poulsen M, Currie CR. Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants. ISME J 2007; 1:313 - 20; PMID: 18043642
  • 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 U S A 2009; 106:4742 - 6; http://dx.doi.org/10.1073/pnas.0812082106; PMID: 19270078
  • Oh D-C, Scott JJ, Poulsen MZ, Currie CR, Clardy J. Discovery of new secondary metabolites mediating insect-microorganism symbioses. Planta Med 2008; 74:906 - 06; http://dx.doi.org/10.1055/s-0028-1083882
  • Oh D-C, Poulsen M, Currie CR, Clardy J. Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis. Nat Chem Biol 2009; 5:391 - 3; http://dx.doi.org/10.1038/nchembio.159; PMID: 19330011
  • Ribeiro SB. Caracterização de espécies bacterianas encontradas em ninhos de Atta sexdens L. e isolamento de Streptomyces de formigas da tribo Attini. PhD Thesis Rio Claro SP, 2000 Universidade Estadual Paulista.
  • Rodrigues AR, Cable RN, Mueller UG, Bacci M Jr., Pagnocca FC. Antagonistic interactions between garden yeasts and microfungal garden pathogens of leaf-cutting ants. Antonie Van Leeuwenhoek 2009; 96:331 - 42; http://dx.doi.org/10.1007/s10482-009-9350-7; PMID: 19449210
  • Zucchi TD, Guidolin AS, Cônsoli FL. Isolation and characterization of actinobacteria ectosymbionts from Acromyrmex subterraneus brunneus (Hymenoptera, Formicidae). Microbiol Res 2011; 166:68 - 76; http://dx.doi.org/10.1016/j.micres.2010.01.009; PMID: 20171857
  • Parke JL, Gurian-Sherman D. Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu Rev Phytopathol 2001; 39:225 - 58; http://dx.doi.org/10.1146/annurev.phyto.39.1.225; PMID: 11701865
  • Coenye T, Vandamme P. Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 2003; 5:719 - 29; http://dx.doi.org/10.1046/j.1462-2920.2003.00471.x; PMID: 12919407
  • Lim YH, Suh JW, Kim S, Hyun BC, Kim CS, Lee CH. Cepacidine A, a novel antifungal antibiotic produced by Pseudomonas cepacia. II. Physico-chemical properties and structure elucidation. J Antibiot (Tokyo) 1994; 47:1406 - 16; http://dx.doi.org/10.7164/antibiotics.47.1406; PMID: 7531194
  • Parke JL, Rand RE, Joy AE, King EB. Biological control of Pythium damping-off and Aphanomyces root rot of peas by application of Pseudomonas cepacia or P. fluorescens to seed. Plant Dis 1991; 75:987 - 92; http://dx.doi.org/10.1094/PD-75-0987
  • Bergstrom CT, Lo M, Lipsitch M. Ecological theory suggests that antimicrobial cycling will not reduce antimicrobial resistance in hospitals. Proc Natl Acad Sci U S A 2004; 101:13285 - 90; http://dx.doi.org/10.1073/pnas.0402298101; PMID: 15308772
  • Rodríguez A, Bacci M Jr., Mueller UG, Ortiz A, Pagnocca FC. Microfungal “Weeds” in the Leafcutter Ant Symbiosis. Microb Ecol 2008; 1:1 - 5
  • Currie CR. A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol 2001; 55:357 - 80; http://dx.doi.org/10.1146/annurev.micro.55.1.357; PMID: 11544360