The prominent role of fungi and fungal enzymes in the ant–fungus biomass conversion symbiosis
Molecular studies have added significantly to understanding of the role of fungi and fungal enzymes in the efficient biomass conversion, which takes place in the fungus garden of leaf-cutting ants. It is now clear that the fungal symbiont expresses the full spectrum of genes for degrading cellulose and other plant cell wall polysaccharides. Since the start of the genomics era, numerous interesting studies have especially focused on evolutionary, molecular, and organismal aspects of the biological and biochemical functions of the symbiosis between leaf-cutting ants (Atta spp. and Acromyrmex spp.) and their fungal symbiont Leucoagaricus gongylophorus. Macroscopic observations of the fungus-farming ant colony inherently depict the ants as the leading part of the symbiosis (the myrmicocentric approach, overshadowing the mycocentric aspects). However, at the molecular level, it is fungal enzymes that enable the ants to access the nutrition embedded in recalcitrant plant biomass. Our hypothesis is that the evolutionary events that established fungus-farming practice were predisposed by a fascinating fungal evolution toward increasing attractiveness to ants. This resulted in the ants allowing the fungus to grow in the nests and began to supply plant materials for more fungal growth. Molecular studies also confirm that specialized fungal structures, the gongylidia, with high levels of proteins and rich blend of enzymes, are essential for symbiosis. Harvested and used as ant feed, the gongylidia are the key factor for sustaining the highly complex leaf-cutting ant colony. This microbial upgrade of fresh leaves to protein-enriched animal feed can serve as inspiration for modern biorefinery technology.
KeywordsLeucoagaricus Leaf-cutting ants Fungus garden Fungal enzymes Expressed enzyme profiles Biomass conversion
We would like to thank Jacobus J. Boomsma for his critical reading of a previous version of this manuscript and for constructive comments and suggestions and Pepijn Kooij for sharing unpublished observations and for providing colony material for photographs (Leucoagaricus gongylophorus, AC-2009-47, leg. et det. Pepijn Kooij, Gamboa, Panama). The authors further wish to thank David Nash and Henrik H. De Fine Licht, University of Copenhagen, and Ib Søndergaard for the fungus garden photographs. The authors were partially funded by the Danish Strategic Research Foundation, grant no. 2101-07-0099.
- Aylward FO, Burnum-Johnson KE, Tringe SG, Teiling C, Tremmel DM, Moeller JA, Scott JJ, Barry KW, Piehowski PD, Nicora CD (2013) Leucoagaricus gongylophorus produces diverse enzymes for the degradation of recalcitrant plant polymers in leaf-cutter ant fungus gardens. Appl Environ Microbiol 79:3770–3778PubMedCentralPubMedCrossRefGoogle Scholar
- De Siqueira CG, Bacci M, Pagnocca FC, Bueno OC, Hebling MJ (1998) Metabolism of plant polysaccharides by Leucoagaricus gongylophorus, the symbiotic fungus of the leaf-cutting ant Atta sexdens L. Appl Environ Microbiol 64:4820–4822Google Scholar
- Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martinez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Gorecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kuees U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Duenas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, John FS, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719PubMedCrossRefGoogle Scholar
- Ingold CT (1971) Fungal spores. Their liberation and dispersal. Clarendon, OxfordGoogle Scholar
- Lange L (2011) Oral presentation. In: 26th Fungal Genetics Conference, Asilomar, USAGoogle Scholar
- Möller A (1893) Die pilzgärten einiger südamerikanischer ameisen. Fischer, JenaGoogle Scholar
- Mueller UG, Schultz TR, Currie CR, Adams RM, Malloch D (2001) The origin of the attine ant–fungus mutualism. Q Rev Biol 169-197Google Scholar
- Nagamoto NS, Garcia MG, Forti LC, Verza SS, Noronha NC, Rodella RA (2011) Microscopic evidence supports the hypothesis of high cellulose degradation capacity by the symbiotic fungus of leaf-cutting ants. J Biol Res—Thessalon 16:308–312Google Scholar
- Petersen JH (2013) The kingdom of fungi. Princeton University Press, PrincetonGoogle Scholar
- Rineau F, Roth D, Shah F, Smits M, Johansson T, Canbäck B, Olsen PB, Persson P, Grell MN, Lindquist E, Grigoriev IV, Lange L, Tunlid A (2012) The ectomycorrhizal fungus Paxillus involutus converts organic matter in plant litter using a trimmed brown-rot mechanism involving Fenton chemistry. Environ Microbiol 14:1477–1487PubMedCentralPubMedCrossRefGoogle Scholar
- Vo TL, Mueller UG, Mikheyev AS (2009) Free-living fungal symbionts (Lepiotaceae) of fungus-growing ants (Attini: Formicidae). Mycologia 101:206–210Google Scholar
- Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar