Fungus-growing ants (Credit: Pepijn Kooij)
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Symbiont policing and mutualism maintenance

Investigating whether one or more mycoviruses suppress sexual reproduction in the fungal crops of fungus-growing ants

Project details

Project Leader: 
Funded By: 
British Ecological Society

Objectives and outputs

Background

Leaf-cutting ants have domesticated fungal crops for ca 10 million years, making them one of the most successful herbivores in the Neotropics. Their fungal symbiont is a reproductively mature mushroom-forming fungus, yet mushrooms are rarely seen. Fungal viruses (mycoviruses) are known to have “castrating” effects on human cultivated mushrooms, suggesting that ant cultivars could suffer from similar effects. 

Mutualism is a cooperation between partners that is viewed as a balance in a perpetual battle over resources. Natural selection favours mutualistic interactions that minimise cheating by one partner, including policing mechanisms that stabilise the partnership. Fungus-growing ants of the tribe Attini maintain a stable obligate mutualism with their fungal partner of the mushroom genus Leucoagaricus (Agaricales: Agaricaceae). Each generation, new ant queens bring fungus from the original colony to build their own, causing vertical transmission of the fungus. Fungal reproduction outside this transmission would be a waste of energy for the colony as whole and could introduce new genetic strains; threatening the domesticated phenotype and misaligning the reproductive interests of the ants and their fungal crops. To avoid these destabilising scenarios, the ants actively remove any fruiting body material initiated by the fungus. However, fruiting of the fungal symbiont is rare in general, suggesting the primary cause of fruiting body suppression takes place prior to mushroom formation.

Recent pilot studies, using transmission electron microscopy, have shown the presence of a mycovirus in the ant fungal crops. In other (human cultivated) mushroom forming fungi, such as Agaricus bisporus and Pleurotus ostreatus, mycoviruses have been shown to have a “castrating” effect, causing the fungi to produce malformed fruiting bodies and reduced germination of basidiospores. The mycovirus(es) in this system are potentially functioning to suppress fruit body formation, thereby policing the fungal symbiont and leading to long term maintenance of a stable mutualism.  This project aims to identify the mycovirus(es) present in the fungal crops and investigate their role in suppressing mushroom growth.

Research Questions

Q1) How many and what is/are the identities of the mycovirus(es) in ant fungal crops?

Q2) Do the mycovirus(es) suppress sexual reproductive structure formation?

Q3) How widespread is/are the mycovirus(es) in the fungus-farming ant cultivars?

Techniques used

  • Transmission electron microscopy
  • Scanning electron microscopy
  • FISH microscopy
  • High-throughput sequencing methods (MiSeq, MinION)
  • Protein sequencing
  • Mycelium/fruiting body growth essays

All work is performed at RBG Kew. Kew’s outstanding expertise in microscopy, mycology and fungal genomics are vital in reaching the research goals.

Objectives

  • To identify and classify mycoviruses in the ant fungal crops
  • To sequence the mycovirus genome and protein capsule
  • To identify the role/function of mycoviruses in the ant-fungus mutualism

Outputs

  • Mycoviral annotated genome and protein capsule sequences
  • Microscopic evidence/photography of the mycoviruses
  • Development of a method to cure the fungal symbiont and induce mushroom growth

Partners and collaborators

International

  • Centre for Social Evolution, University of Copenhagen, Denmark
  • Smithsonian Tropical Research Institute, Panama

Publications

Kooij, P.W., Aanen, D.K., Schiøtt, M. & Boomsma, J.J. (2015). Evolutionarily advanced ant farmers rear polyploid fungal crops. Journal of Evolution Biology 28: 1911–1924. doi: 10.1111/jeb.12718

Fisher, P.J., Stradling, D.J. & Pegler, D.N. (1994). Leucoagaricus basidiomata from a live nest of the leaf-cutting ant Atta cephalotes. Mycological Research 98 :884–888. doi: 10.1016/S0953-7562(09)80259-1

Yu, H.J., Lim, D.& Lee H-S. (2003). Characterization of a novel single-stranded RNA mycovirus in Pleurotus ostreatus. Virology 314: 9–15. doi: 10.1016/S0042-6822(03)00382-9

Kwon, Y.C., Jeong, D.W., Gim, S.I., et al. (2012). Curing viruses in Pleurotus ostreatus by growth on a limited nutrient medium containing cAMP and rifamycin. Journal of Virological Methods 185: 156–159. doi: 10.1016/j.jviromet.2012.06.002