Abstract
Chemical compounds are key to understand symbiotic interactions. In the leafcutter ant-microbe symbiosis a plethora of filamentous fungi continuously gain access the ant colonies through plant substrate collected by workers. Many filamentous fungi are considered transient in attine ant colonies, however, their real ecological role in this environment still remains unclear. A possible role of these microorganisms is the antagonism towards Leucoagaricus gongylophorus, the mutualistic fungus that serve as food for several leafcutter ant species. Here, we showed the antagonism of filamentous fungi isolated from different sources, and the negative impacts of their metabolites on the growth of the ant-fungal cultivar. Our results demonstrate that the chemical compounds produced by filamentous fungi can harm the mutualistic fungus of leafcutter ants.
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Akiyama K, Matsuzaki KI, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
Flórez LV, Scherlach K, Gaube P, Ross C, Sitte E, Hermes C, Rodrigues A, Hertweck C, Kaltenpoth M (2017) Antibiotic-producing symbionts dynamically transition between plant pathogenicity and insect-defensive mutualism. Nat Commun 8:15172
Seipke RF, Barke J, Brearley C, Hill L, Douglas WY, Goss RJ, Hutchings MI (2011) A single Streptomyces symbiont makes multiple antifungals to support the fungus farming ant Acromyrmex octospinosus. PLoS ONE 6:e22028
Russell JA, Sanders JG, Moreau CS (2017) Hotspots for symbiosis: function, evolution, and specificity of ant-microbe associations from trunk to tips of the ant phylogeny (Hymenoptera: Formicidae). Myrmecol News 24:43–69
Chapela IH, Rehner SA, Schultz TR, Mueller UG (1994) Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:1691–1694
Mueller UG, Scott JJ, Ishak HD, Cooper M, Rodrigues A (2010) Monoculture of leafcutter ant gardens. PLoS ONE 5:e12668
Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci USA 105:5435–5440
Cherrett JM, Peregrine DJ (1976) A review of the status of leaf-cutting ants and their control. Ann Appl Biol 84:124–128
Mueller UG, Kardish MR, Ishak HD, Wright AM, Solomon SE, Bruschi SM, Carlson AL, Bacci M Jr (2018) Phylogenetic patterns of ant–fungus associations indicate that farming strategies, not only a superior fungal cultivar, explain the ecological success of leafcutter ants. Mol Ecol 27:2414–2434
Currie CR, Mueller UG, Malloch D (1999) The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci USA 96:7998–8002
Muchovej JJ, Della Lucia TM (1990) Escovopsis, a new genus from leaf cutting ant nests to replace Phialocladus nomem invalidum. Mycotaxon 37:191–195
Dhodary B, Schilg M, Wirth R, Spiteller D (2018) Secondary metabolites from Escovopsis weberi and their role in attacking the garden fungus of leaf-cutting ants. Chem Eur J 24:4445–4452
Gerardo NM, Jacobs SR, Currie CR, Mueller UG (2006) Ancient host–pathogen associations maintained by specificity of chemotaxis and antibiosis. PLoS Biol 4:1358–1363
Marfetán JA, Romero AI, Folgarait PJ (2015) Pathogenic interaction between Escovopsis weberi and Leucoagaricus sp.: mechanisms involved and virulence levels. Fungal Ecol 17:52–61
Reynolds HT, Currie CR (2004) Pathogenicity of Escovopsis weberi: the parasite of the attine ant-microbe symbiosis directly consumes the ant-cultivated fungus. Mycologia 96:955–959
Kost C, Lakatos T, Böttcher I, Arendholz WR, Redenbach M, Wirth R (2007) Non-specific association between filamentous bacteria and fungus-growing ants. Naturwissenschaften 94:821–828
Mueller UG, Dash D, Rabeling C, Rodrigues A (2008) Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution 62:2894–2912
Little AEF, Currie CR (2007) Symbiotic complexity: discovery of a fifth symbiont in the attine ant–microbe symbiosis. Biol Lett 3:501–504
Little AEF, Currie CR (2008) Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecology 89:1216–1222
Rodrigues A, Mueller UG, Ishak HD, Bacci M Jr, Pagnocca FC (2011) Ecology of microfungal communities in gardens of fungus-growing ants (Hymenoptera: Formicidae): a year-long survey of three species of attine ants in Central Texas. FEMS Microbiol Ecol 78:244–255
Rodrigues A, Pagnocca FC, Bacci M Jr, Hebling MJA, Bueno OC, Pfenning LH (2005) Variability of non-mutualistic filamentous fungi associated with Atta sexdens rubropilosa nests. Folia Microbiol 50:421–425
Barcoto MO, Pedrosa F, Bueno OC, Rodrigues A (2017) Pathogenic nature of Syncephalastrum in Atta sexdens rubropilosa fungus gardens. Pest Manag Sci 73:999–1009
Currie CR, Stuart AE (2001) Weeding and grooming of pathogens in agriculture by ants. Proc R Soc Lond B 268:1033–1039
Fernández-Marín H, Zimmerman JK, Rehner SA, Wcislo WT (2006) Active use of the metapleural glands by ants in controlling fungal infection. Proc R Soc Lond B 273:1689–1695
Rodrigues A, Carletti CD, Bueno OC, Pagnocca FC (2008) Leaf-cutting ant faecal fluid and mandibular gland secretion: effects on microfungi spore germination. Braz J Microbiol 39:64–67
Fisher PJ, Stradling DJ, Sutton BC, Petrini LE (1996) Microfungi in the fungus gardens of the leaf-cutting ant Atta cephalotes: a preliminary study. Mycol Res 100:541–546
Rodrigues A, Passarini MRZ, Ferro M, Nagamoto NS (2014) Fungal communities in the garden chamber soils of leaf-cutting ants. J Basic Microbiol 54:1186–1196
Castrillo ML, Bich GA, Zapata PD, Villalba LL (2016) Biocontrol of Leucoagaricus gongylophorus of leaf-cutting ants with the mycoparasitic agent Trichoderma koningiopsis. Mycosphere 7:810–819
Folgarait P, Gorosito N, Poulsen M, Currie CR (2011) Preliminary in vitro insights into the use of natural fungal pathogens of leaf-cutting ants as biocontrol agents. Curr Microbiol 63:250
Nascimento MO, Almeida Sarmento R, Santos GR, Oliveira CA, Souza DJ (2017) Antagonism of Trichoderma isolates against Leucoagaricus gongylophorus (Singer) Möller. J Basic Microbiol 57:699–704
Silva A, Rodrigues A, Bacci M Jr, Pagnocca FC, Bueno ODC (2006) Susceptibility of the ant-cultivated fungus Leucoagaricus gongylophorus (Agaricales: Basidiomycota) towards microfungi. Mycopathologia 162:115–119
Varanda-Haifig SS, Albarici TR, Nunes PH, Haifig I, Vieira PC, Rodrigues A (2017) Nature of the interactions between hypocrealean fungi and the mutualistic fungus of leaf-cutter ants. Antonie Van Leeuwenhoek 110:593–605
Wicklow DT (1992) Interference competition. In: Carrol GC, Wicklow DT (eds) The fungal community: its organization and role in the ecosystem, 2nd edn. Marcel Dekker, New York, pp 265–274
Rodrigues A, Bacci M Jr, Muller UG, Ortiz A, Pagnocca FC (2008) Microfungal “weeds” in the leafcutter ant symbiosis. Microb Ecol 56:604–614
Rodrigues A, Pagnocca FC, Bueno OC, Pfenning LH, Bacci M Jr (2005) Assessment of microfungi in fungus gardens free of the leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae). Sociobiology 46:329–334
Michielse CB, Rep M (2009) Pathogen profile update: Fusarium oxysporum. Mol Plant Pathol 10:311–324
Chet I, Harman GE, Baker R (1981) Trichoderma hamatum: Its hyphal interactions with Rhizoctonia solani and Pythium spp. Microb Ecol 7:29–38
Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV (2009) Diversity, pathogenicity, and management of Verticillium species. Annu Rev Phytopathol 47:39–62
Karlsson M, Durling MB, Choi J, Kosawang C, Lackner G, Tzelepis GD, Nygren K, Dubey MK, Kamou N, Levasseur A, Zapparata A (2015) Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea. Genome Biol Evol 7:465–480
Maciá-Vicente JG, Jansson HB, Talbot NJ, Lopez-Llorca LV (2009) Real-time PCR quantification and live-cell imaging of endophytic colonization of barley (Hordeum vulgare) roots by Fusarium equiseti and Pochonia chlamydosporia. New Phytol 182:213–228
Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759
Kubicek CP et al (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:R40
Pagnocca FC, da Silva OA, Hebling-Beraldo MJ, Bueno OC, Fernandes JB, Vieira PC (1990) Toxicity of sesame extracts to the symbiotic fungus of leaf-cutting ants. Bull Entomol Res 80:349–352
Jelihovschi EG, Faria JC, Allaman IB (2014) ScottKnott: a package for performing the Scott-Knott clustering algorithm in R. Trend Mat Apl Comput 15:3–17
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Borba RD, Loeck AE, Bandeira JD, Moraes CL, Centenaro ED (2006) Growth of symbiont fungi of cutter ants of the genus Acromyrmex in means of culture with different extracts. Cienc Rural 36:725–730
Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701
Nygaard S, Hu H, Li C, Schiott M, Chen Z, Yang Z, Xie Q, Ma C, Deng Y, Dikow RB, Rabeling C (2016) Reciprocal genomic evolution in the ant-fungus agricultural symbiosis. Nat Commun 7:12233
Bae SJ, Mohanta TK, Chung JY, Ryu M, Park G, Shim S, Hong SB, Seo H, Bae DW, Bae I, Kim JJ (2016) Trichoderma metabolites as biological control agents against Phytophthora pathogens. Biol Control 92:128–138
de Lima FB, Félix C, Osório N, Alves A, Vitorino R, Domingues P, da Silva Ribeiro RT, Esteves AC (2017) Trichoderma harzianum T1A constitutively secretes proteins involved in the biological control of Guignardia citricarpa. Biol Control 106:99–109
Van Bael SA, Seid MA, Wcislo WT (2012) Endophytic fungi increase the processing rate of leaves by leaf-cutting ants (Atta). Ecol Entomol 37:318–321
Rocha SL, Evans HC, Jorge VL, Cardoso LAO, Pereira FS, Rocha FB, Barreto RW, Hart AG, Elliot SL (2017) Recognition of endophytic Trichoderma species by leaf-cutting ants and their potential in a Trojan-horse management strategy. R Soc Open Sci 4:160628
Van Bael SA, Fernández-Marín H, Valencia MC, Rojas EI, Wcislo WT, Herre EA (2009) Two fungal symbioses collide: endophytic fungi are not welcome in leaf-cutting ant gardens. Proc R Soc London B 276:2419–2426
Rocha SL, Jorge VL, Della Lucia TMC, Barreto RW, Evans HC, Elliot SL (2014) Quality control by leaf-cutting ants: evidence from communities of endophytic fungi in foraged and rejected vegetation. Arthropod Plant Interact 8:485–493
Silva A, Bacci JRM, de Siqueira CG, Bueno OC, Pagnocca FC, Hebling MJ (2003) Survival of Atta sexdens workers on different food sources. J Insect Physiol 49:307–313
Heine D, Holmes NA, Worsley SF, Santos AC, Innocent TM, Scherlach K, Patrick EH, Douglas WY, Murrell JC, Vieria PC, Boomsma JJ (2018) Chemical warfare between leafcutter ant symbionts and a co-evolved pathogen. Nat Commun 9:2208
Acknowledgement
The authors would like to thank “Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)” and “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)” for financial support: Grant # 2011/16765-0 and 478559/2011-9, respectively.
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Bizarria, R., Moia, I.C., Montoya, Q.V. et al. Soluble Compounds of Filamentous Fungi Harm the Symbiotic Fungus of Leafcutter Ants. Curr Microbiol 75, 1602–1608 (2018). https://doi.org/10.1007/s00284-018-1566-1
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DOI: https://doi.org/10.1007/s00284-018-1566-1