Bacterial Symbionts of Farming Ants

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Black yeast prey on Pseudonocardia

Adding to the complexity of leaf-cutting ant communities, actinobacteria were discovered to have their own specialized fungal predators—a black yeast called Phialophora, which grows on and around the crypts housing the ants’ antibiotic-producing bacteria. When the black yeast was put together with actinobacteria in a petri dish, Phialophora ate the bacteria, thereby robbing the ants of an important anti-Escovopsis defense. However, parasitism in this multipartite system is not considered a detrimental thing; it helps to keep the cooperators honest. For example, making antifungal agents is expensive, and selfish actinobacteria would be tempted to reproduce more and protect the ants less without the black yeast around. Thus, with the yeast, antibiotic production is also in the best interest of the threatened bacteria. Moreover, the black yeast undoubtedly adds value to the relationship because, like the cultivar, Escovopsis, and actinomycetes, the yeast has probably been part of the leaf-cutting ants’ microbial balancing act since they first began farming about 50 million years ago.

Cordyceps infection of ants

Ants spend a great deal of time foraging about in the soil, and it should come as no surprise that they, as well as their fungal food gardens, are vulnerable to infection with pathogenic fungi. Principal among these are Cordyceps, which comprise at least 400 species and infect a wide range of insects and spiders in addition to ants. Ant queens are at particular risk of parasitic infections during the colony-founding stage because of the many energetic demands that must be met simultaneously. In addition, although it appears that vigorous general defenses against food crop fungi indirectly protect the ants from a range of parasitic fungi, an ant-associated genus of Cordyceps, called Ophiocordyceps stilbelliformis, has been found parasitizing leaf-cutter ants in Panama. Fortunately for farming ants, this is a rare event because Cordyceps are a particularly nasty group of fungi that keep the infected ants alive just long enough to distance themselves from the nest and then become spore-making factories.

Fig. 3 Untimely death of an ant queen: Acromyrmex octospinosus queen from Panama with two Ophiocordyceps stilbelliformis stroma erupting from between the head and pronotum. Also note the fungus growing out the ends of her legs. (Courtesy of David P. Hughes, Harvard University)

Attine ant-microbe evolution

The ancestors of fungus-growing ants probably transitioned from hunter-gatherers of arthropod prey, nectar, and plant juices to the farming life fortuitously, by taming the wild fungi growing on the walls of their nests in leaf litter or from a system of myrmecochory (spore or seed dispersal by ants) where specialized fungi used the ants for their own dispersal. Ants routinely ingest fungal spores and hyphal material and such infrabuccal contents are eventually expelled as pellets on nest middens (refuse dumps) and elsewhere, providing the fungi with a way of dispersing their spores and hyphae. Thus, the fungi were probably not passive symbionts that happened to come under ant control, but rather played a proactive role in the ant evolution from hunter-gatherer to fungus farmer. Recent work using culture-independent genomic sequencing technologies is lending further weight to the long-standing scientific consensus that the ant-actinomycete association evolved for mutual benefit rather than as a coevolutionary arms race between antibiotic-producing Pseudonocardia and Escovopsis parasites. However, these new technologies must be used properly, statistically valid conclusions must be drawn, and wild as well as laboratory ant colonies must be tested in these endeavors. Importantly, the new tools and new data will attract further investigations by the growing community of researchers fascinated by the attine tribe of sophisticated farming ants.

See also: Antibiotic; Bacteria; Chemical ecology; Ecological communities; Ecology; Food web; Fungal ecology; Fungi; Hymenoptera; Mutualism; Social insects; Soil ecology; Trophic ecology

Bibliography

l C. R. Currie et al., Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants, Science, 311:81–83, 2006 DOI:10.1126/science.1119744
l C. R. Currie et al., Fungus-growing ants use antibiotic-producing bacteria to control garden parasites, Nature, 398:701–704, 1999 DOI:10.1038/19519
l O. Dong-Chan et al., Dentigerumycin: A bacterial mediator of an ant-fungus symbiosis, Nat. Chem. Biol., 5:391–393, 2009 DOI:10.1038/nchembio.159
l D. P. Hughes et al., Novel fungal disease in complex leaf-cutting ant societies, Ecol. Entomol., 34:214–220, 2009 DOI:10.1111/j.1365-2311.2008.01066.x
l G. Yim, H. Huimi Wang, and J. Davies, Antibiotics as signalling molecules, Philos. T. Roy. Soc. B., 362:1195–1200, 2007 DOI:10.1098/rstb.2007.2044

Additional Readings

l J. J. Boomsma and D. K. Aanen, Rethinking crop-disease management in fungus-growing ants, Proc. Natl. Acad. Sci. USA, 106(42):17611–17612, 2009 DOI:10.1073/pnas.0910004106
l H. Fernández-Marín et al., Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants, P. R. Soc. B., 276:2263–2269, 2009 DOI:10.1098/rspb.2009.0184
l M. Poulsen and C. R. Currie, Symbiont interactions in a tripartite mutualism: Exploring the presence and impact of antagonism between two fungus-growing ant mutualists, PLoS ONE, 5(1):1–13, 2010
DOI:10.1371/journal.pone.0008748
l H. T. Reynolds and C. R. Currie, Pathogenicity of Escovopsis weberi: The parasite of the attine ant-microbe symbiosis directly consumes the ant-cultivated fungus, Mycologia, 96(5):955–959, 2004 DOI:10.2307/3762079

Marcia Stone, “Bacterial symbionts of farming ants,” in 2011 McGraw-Hill Yearbook of Science & Technology, McGraw-Hill, New York, 2011.

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