COMMUNITY ECOLOGY All That Makes Fungus Gardens Grow The discovery of a parasitic yeast draws attention to the ways that pathogens can stabilize ant agriculture and other symbiotic networks Fifty million years ago while the earliest primates were still scurrying from tree to tree scrounging fruits and insects attine ants were growing their own food They were so adept at domesticating mushrooms that hundreds of species have descended from the original farmers all of them cultivating fungi Humans could learn a lot from the ants success Over the past 10 years researchers have come to realize that the fungus gardens thrive because of an intricate web of bacteria and fungi that includes both pests such as a newly discovered black yeast and partners including bacteria that keep pathogens in check By studying these relationships biologists hope they ll uncover lessons about the evolution of such interactions knowledge that will help humans better manage microbes in medicine and agriculture It s a system that works says John Morrissey a microbiologist at University College Cork in Ireland If you could develop a bacterial inoculant that was as successful in controlling a specific pathogen as the beneficial bacteria are for the ants you d be on to a real winner Complex network Ant agriculture runs the gamut For leafcutter ants far ming is big business 1006 They re the most notorious of the more than 230 described species of fungus gardeners forming colonies of millions of workers that can defoliate a tree or crop in mere hours The ants use the harvest to fertilize hundreds of separate fungus gardens in an elaborate subterranean compound Most attine gardens however are smallscale operations Their inconspicuous colonies are tended by as few as a dozen workers that scavenge bits of detritus to feed a spongy handful of fungus But from the most primitive gardener to the dreaded leaf cutter all attines would starve if deprived of their fungal crops When an ant queen leaves home to mate and found a new colony she must take a little mouthful of the fungus with her to start a garden Although naturalists have known since 1874 that the attine ants are fungus gardeners more than a century passed before Ph D student Cameron Currie began to chip away the microbial complexity underlying the ant fungus symbiosis While at the University of Toronto in Canada he discovered that ant gardens often contained a second fungus Escovopsis When he grew it on culture plates with different food sources Currie determined that Escovopsis is a pathogen 23 MAY 2008 VOL 320 SCIENCE Published by AAAS with a sweet tooth for only the ants cultivar What s more the pathogen s evolutionary tree had the same basic shape as those of the ants and their crop indicating that all three had coevolved since the beginning of ant agriculture Currie and colleagues reported in 2003 Science 17 January 2003 pp 325 386 Although Currie isolated Escovopsis from up to 75 of the gardens of several attine species in Panama this pathogen rarely seemed to do much damage The reason it turned out was a fourth symbiont Currie found that actinomycete bacteria housed and nourished in pits on the ants bodies produce chemicals that keep Escovopsis in check The four part garden symbiosis of ant cultivar pathogen and bacteria interrupted a scientific tradition of studying symbionts two at a time think corals and algae for example or soybeans and nitrogen fixing bacteria The discovery accelerated a transition toward thinking of interacting organisms in trios or networks not pairs When I got into this stuff it was two symbionts says Ted Schultz an entomologist at the Smithsonian National Museum of Natural History in Washington D C who has studied attine evolution for nearly 30 years I was stunned when Currie identified two more Now in a paper in this month s issue of Ecology Currie and his colleagues introduce a fifth symbiont It just continues the trend of being repeatedly surprised by how complex this system is Schultz says The first hint of the new player came when Currie now at the University of Wisconsin UW Madison cultured the actinomycete bacteria from an ant called Apterostigma In addition to white bacterial spots a black yeast often appeared on the same culture plates Ainslie Little now a postdoctoral fellow at UW Madison took a closer look at the yeast She treated worker ants in a vial coated with a selective antibiotic that would rub off on the ants and kill the yeast but not the other symbionts At first it looked like the experiment was a bust Getting rid of the yeast had no effect on the ants or their crop But when Little spritzed half the ants gardens with a solution of Escovopsis spores the yeast suddenly revealed its true colors Over 3 days ants with black yeast infections lost twice as much of their crop to Escovopsis as the yeast free ants When Little grew the actinomycetes in petri dishes with the yeast the yeast ate the bacteria demonstrating that they rob ants of an important defense against Escovopsis DNA studies showed that the black yeasts are widespread on the attine ant family tree thriving near the pits where the ants www sciencemag org CREDIT ALEX WILD 2006 Farm labor Leaf cutter ants tend their fungus garden a complex miniature ecosystem Downloaded from www sciencemag org on May 22 2008 NEWSFOCUS NEWSFOCUS No cheating allowed Currie thinks that understanding three four and five way interactions like the ones in the fungus gardens may ultimately revolutionize the way we think about the evolution of mutualism Why two parties should cooperate whether it s two species over evolutionary time or two people over the course of a day is one of science s big mysteries Science 1 July 2005 p 93 In a two player partnership cheaters should be able to get ahead by reaping benefits without paying their dues destabilizing the agreement But the ants have lived stably with two mutualists for millennia Moreover the two antagonists rarely get too far out of line Diseases and pests of humans and their crops on the other hand have evaded control measures in a matter of decades So everyone from crop scientists to basic evolutionary biologists is itching to know the secrets to both cooperation and control in the ants gardens Morrissey for example would like to incor porate benef icial microbes into human agriculture to reduce chemical input The attine system shows it is possible to set up a structured microbial community over a very long term for
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