Skip to main content
Log in

Selective isolation of dematiaceous fungi from the workers of Atta laevigata (Formicidae: Attini)

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

Leaf-cutting ants (Formicidae: Attini) are considered pests in agriculture for their impact in human crops, as they utilize leaf fragments to raise their fungal mutualist (Agaricales: Lepiotaceae). Basically, the basidiomycetous fungus is cultivated to supply food to adult workers and broads; in return, the ants protect it against natural enemies. However, recent studies have claimed that other microorganisms are associated to ant nests where a wide range of interactions may take place. To investigate the occurrence of dematiaceous fungi on the cuticle of Atta laevigata ants, 30 workers were sampled from an adult nest located in the surroundings of the Center for the Studies of Social Insects, UNESP-Rio Claro, SP, Brazil. The use of selective techniques to avoid high-sporulation fungi has been recommended and was tested in this study. To favor the isolation of the desired fungi, heads and cuticle scrapings of ant bodies were inoculated on Mycosel agar and incubated for 3 weeks at 35°C. Morphological and molecular methods were used to identify the filamentous fungi recovered. From 56 isolates, 19 were hyaline filamentous species, and among the remaining 37, some are mentioned as phyto-associated fungi like Alternaria arborescens, Bipolaris sorokiniana, Bipolaris eleusines, Bipolaris zeae, Curvularia trifolii, and Paraphaeosphaeria michotii. These species are reported from A. laevigata bodies for the first time. None of the isolation trials revealed the presence of the parasite Escovopsis or entomopathogenic fungi. The possible spread of the fungi in nature by the ants is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Blatrix R, Bouamer S, Morand S, Selosse M-A (2009) Ant-plant mutualisms should be viewed as symbiotic communities. Plant Signal Behav 4(6):554–556

    Article  PubMed  Google Scholar 

  • Craven SE, Dix MW, Michaels GE (1970) Attini fungus gardens contains yeasts. Science 169:184–186

    Article  PubMed  CAS  Google Scholar 

  • Crous PW, Verkley GJM, Groenewald JZ, Samson RA (2009) Fungal biodiversity. CBS KNAW Fungal Biodiversity Centre. CBS Laboratory Manual Series, Utrecht, p 269

    Google Scholar 

  • Currie CR (2001) A community of ants, fungi and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol 55:357–380

    Article  PubMed  CAS  Google Scholar 

  • Currie CR, Scott JA, Summerbell RC, Malloch D (1999a) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398(6729):701–704

    Article  CAS  Google Scholar 

  • Currie CR, Muller UG, Malloch D (1999b) The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci 96:7998–8002

    Article  PubMed  CAS  Google Scholar 

  • Currie CR, Bot ANM, Boomsma JJ (2003) Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites. Oikos 10:91–102

    Article  Google Scholar 

  • Defossez E, Selosse M-A, Dubois MP, Mondolot L, Faccio A, Djieto-Lordon C, McKey D, Blatrix R (2009) Ant-plants and fungi: a new threeway symbiosis. New Phytol 182:942–949

    Article  PubMed  Google Scholar 

  • Domsch KH, Gams W, Anderson TH (1993) Compendium of soil fungi. Academic Press, London, p 1

    Google Scholar 

  • Dugan FM, Schubert K, Braun U (2004) Check-list of Cladosporium names. Schlechtendalia 11:1–103

    Google Scholar 

  • Ellis MB, Ellis JP (1985) Microfungi on land plants. Croom Helm Ltd Provident House, London, 818p

    Google Scholar 

  • Fischer PJ, Stradling DJ, Sutton BC, Petrini LE (1996) Microfungi in the fungus gardens of the leaf-cutting ants Atta cephalotes: a preliminary study. Mycol Res 100(5):541–546

    Article  Google Scholar 

  • Gerrits van den Ende AHG, Hoog GS (1999) Variability and molecular diagnostics of the neurotropic species Cladophialophora bantiana. Stud Mycol 43:152–162

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hoog GS (1993) Evolution of black yeasts: possible adaptation to the human host. Antonie van Leeuwenhoek 63:105–109

    Article  PubMed  Google Scholar 

  • Hoog GS, Guarro J, Gené J, Figueras MJ (2000) Atlas of clinical fungi. 2nd ed. Utrecht: Centraalbureau voor Schimmelcultures; Reus: Universitat Rovira i Virgili 374–379

  • Hoog GS, Attili-Angelis D, Rodrigues A, Pagnocca FC (2009) Chaetothyriales associated with leafcutter ants: opportunistic species. In: The 17th Congress of The International Society for Human and Animal Mycology-ISHAM 2009-Tokyo Abstracts p. 345

  • Jacobson ES (2000) Pathogenic roles for fungal melanins. Clin Microbiol Rev 13(4):708–717

    Article  PubMed  CAS  Google Scholar 

  • Little AEF, Currie CR (2007) Symbiotic complexity: discovery of a fifth symbiont in the Attine ant-microbe symbosis. Biol Lett 3(5):501–504

    Article  PubMed  Google Scholar 

  • Little AEF, Currie CR (2008) Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants. Ecol Soc Amer 89(5):1216–1222

    Google Scholar 

  • Masclaux F, Gueho E, Hoog GS, Christen R (1995) Phylogenetic relationship of human-pathogenic Cladosporium (Xylohypha) species inferred from partial LS rRNA sequences. J Med Vet Mycol 33:327–338

    Article  PubMed  CAS  Google Scholar 

  • Pagnocca FC et al (1996) Microbiological changes in the nests of leaf-cutting ants fed on sesame leaves. J Appl Entomol 120:317–320

    Article  Google Scholar 

  • Pagnocca FC et al (2008) Yeasts and filamentous fungi carried by gynes of leaf-cutting ants. Antonie van Leeuwenhoek 94(4):517–526

    Article  PubMed  Google Scholar 

  • Pagnocca FC et al (2010) Yeasts isolated from a fungus-growing ant nest, including the description of Trichosporon chiarellii sp. nov., an anamorphic basidiomycetous yeast. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.015727-0

  • Pagnocca FC et al (2011) Micro-organismos associados às formigas cortadeiras. In: Formigas Cortadeiras: da bioecologia ao manejo, Editora UFV

  • Ribeiro EL et al (2006) Cromoblastomicose: Doença presente na realidade populacional brasileira. RBAC 38(3):189–192

    Google Scholar 

  • Rodrigues A et al (2008) Microfungal weeds in the leafcutter ant symbiosis. Microb Ecol 56:614–604

    Article  Google Scholar 

  • Rosa CA et al (2003) Yeast communities associated with stingless bees. FEMS Yeast Res 4:271–275

    Article  PubMed  CAS  Google Scholar 

  • Sampaio JP et al (2001) Polyphasic taxonomy of basidiomycetous yeasts genus Rhodosporidium: Rhodosporidium kratochvilovae and related anamorphic species. Int J Syst Evol Microbiol 51:687–697

    PubMed  CAS  Google Scholar 

  • Satow MM, Attili-Angelis D, Hoog GS, Angelis DF, Vicente VA (2008) Selective factors involved in oil flotation isolation of black yeasts from the environment. Stud Mycol 61:157–163

    Article  PubMed  CAS  Google Scholar 

  • Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Nat Acad Science 105(14):5435–5440

    Article  CAS  Google Scholar 

  • Silva A, Bacci M Jr, Pagnocca FC, Bueno OC, Hebling MJA (2006) Starch metabolism in Leucoagaricus gongylophorus, the symbiotic fungus of leaf-cutting ants. Microbiol Res 161:299–303

    Article  PubMed  CAS  Google Scholar 

  • Sunjian A, Hongmei LI (2005) Behavioral plasticity in soldiers of Atta mexicana and its adaptive significance in urban environments. Notes from Underground 11 (1). http://www.blueboard.com/nfu/behavioral_plasticity.htm. Accessed 9 June 2011

  • Vicente VA et al (2008) Environmental isolation of black yeast-like fungi involved in human infection. Stud Mycol 61:137–144

    Article  PubMed  CAS  Google Scholar 

  • Weber NA (1972) The gardening ants: the Attines. American Philosophical Society, Philadelphia

    Google Scholar 

  • Wheeler MH, Bell AA (1988) Melanins and their importance in pathogenic fungi. Curr Topics Med Mycol 2:338–387

    Article  CAS  Google Scholar 

  • White TJT, Bruns SL, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, London, pp 315–322

    Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. Odair Correa Bueno, CEIS-UNESP–RC, SP for providing the ants, to FAPESP (Process, 2009/10001–9 and 50.139/4-2007) for financial support, and also to Miss Dinato (UNESP–RC) for identifying the plants around the nests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. C. Pagnocca.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guedes, F.L.A., Attili-Angelis, D. & Pagnocca, F.C. Selective isolation of dematiaceous fungi from the workers of Atta laevigata (Formicidae: Attini). Folia Microbiol 57, 21–26 (2012). https://doi.org/10.1007/s12223-011-0081-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-011-0081-6

Keywords

Navigation