23 MAY 2008 VOL 320 SCIENCE www.sciencemag.org1006CREDIT: ALEX WILD 2006NEWSFOCUSFifty million years ago, while the earliest pri-mates were still scurrying from tree to tree,scrounging fruits and insects, attine ants weregrowing their own food. They were so adeptat domesticating mushrooms that hundreds ofspecies have descended from the originalfarmers, all of them cultivating fungi.Humans could learn a lot from the ants’success. Over the past 10 years, researchershave come to realize that the fungus gardensthrive because of an intricate web of bacteriaand fungi that includes both pests, such as anewly discovered black yeast, and partners,including bacteria that keep pathogens incheck. By studying these relationships, biolo-gists hope they’ll uncover lessons about theevolution of such interactions, knowledge thatwill help humans better manage microbes inmedicine and agriculture. “It’s a system thatworks,” says John Morrissey, a microbiologistat University College Cork in Ireland. “If youcould develop a bacterial inoculant that was assuccessful in controlling a specific pathogen asthe [beneficial bacteria] are for the ants, you’dbe on to a real winner.”Complex networkAnt agriculture runs the gamut. For leaf-cutter ants, farming is big business.They’re the most notorious of the morethan 230 described species of fungus gar-deners, forming colonies of millions ofworkers that can defoliate a tree or crop inmere hours. The ants use the harvest to fer-tilize hundreds of separate fungus gardensin an elaborate subterranean compound.Most attine gardens, however, are small-scale operations: Their inconspicuouscolonies are tended by as few as a dozenworkers that scavenge bits of detritus to feeda spongy handful of fungus. But from the most primitive gardener tothe dreaded leaf-cutter, all attines wouldstarve if deprived of their fungal crops. Whenan ant queen leaves home to mate and found anew colony, she must take a little mouthful ofthe fungus with her to start a garden. Although naturalists have known since1874 that the attine ants are fungus gardeners,more than a century passed before Ph.D.student Cameron Currie began to chipaway the microbial complexity underlyingthe ant-fungus symbiosis. While at the Uni-versity of Toronto in Canada, he discoveredthat ant gardens often contained a second fun-gus, Escovopsis. When he grew it on cultureplates with different food sources, Curriedetermined that Escovopsis is a pathogenwith a sweet tooth for only the ants’ cultivar.What’s more, the pathogen’s evolutionary treehad the same basic shape as those of the antsand their crop, indicating that all three hadcoevolved since the beginning of ant agricul-ture, Currie and colleagues reported in 2003(Science, 17 January 2003, pp. 325, 386). Although Currie isolated Esco vopsis fromup to 75% of the gardens of several attinespecies in Panama, this pathogen rarelyseemed to do much damage. The reason, itturned out, was a fourth symbiont: Curriefound that actinomycete bacteria, housed andnourished in pits on the ants’ bodies, producechemicals that keep Esco vopsis in check. The four-part garden symbiosis of ant,cultivar, pathogen, and bacteria interrupted ascientific tradition of studying symbionts twoat a time—think corals and algae, for exam-ple, or soybeans and nitrogen-fixing bacteria.The discovery accelerated a transition towardthinking of interacting organisms in trios ornetworks, not pairs.“When I got into this stuff, it was two sym-bionts,” says Ted Schultz, an entomologist atthe Smithsonian National Museum of NaturalHistory in Washington, D.C., who has studiedattine evolution for nearly 30 years. “I wasstunned” when Currie identified two more.Now, in a paper in this month’s issue ofEcology, Currie and his colleagues introducea fifth symbiont. “[It] just continues the trendof being repeatedly surprised by how com-plex this system is,” Schultz says. The first hint of the new player camewhen Currie, now at the University of Wis-consin (UW), Madison, cultured the actino-mycete bacteria from an ant calledApterostigma. In addition to white bacterialspots, a black yeast often appeared on thesame culture plates. Ainslie Little, now apostdoctoral fellow at UW Madison, took acloser look at the yeast. She treated workerants in a vial coated with a selective anti-biotic that would rub off on the ants and killthe yeast but not the other symbionts. At first, it looked like the experiment wasa bust: Getting rid of the yeast had no effecton the ants or their crop. But when Littlespritzed half the ants’ gardens with a solutionof Escovopsis spores, the yeast suddenlyrevealed its true colors. Over 3 days, ants withblack yeast infections lost twice as much oftheir crop to Esco vopsis as the yeast-free ants.When Little grew the actinomycetes in petridishes with the yeast, the yeast ate the bacte-ria, demonstrating that they rob ants of animportant defense against Escovopsis. DNA studies showed that the blackyeasts are widespread on the attine ant fam-ily tree, thriving near the pits where the antsAll That Makes Fungus Gardens GrowThe discovery of a parasitic yeast draws attention to the ways that pathogens can stabilize ant agriculture and other symbiotic networksCOMMUNITY ECOLOGYFarm labor. Leaf-cutterants tend their fungusgarden, a complexminiature ecosystem.Published by AAAS on May 22, 2008 www.sciencemag.orgDownloaded fromwww.sciencemag.org SCIENCE VOL 320 23 MAY 20081007CREDITS: (ANT AND BACTERIA IMAGES) A. E. F. LITTLE AND C. R. CURRIE, ECOLOGY (2008) COPYRIGHT BY THE ECOLOGICAL SOCIETY OF AMERICA; (YEAST AND CULTIVAR) A. LITTLE; (PARASITE) E. CALDERANEWSFOCUShouse the actinomycetes. Like the cultivar,Escovopsis, and actinomycetes, the yeasthas been part of the attines’ microbial bal-ancing act since the ants first began to farm,Currie says. “It’s really exciting,” Schultz says of thefifth symbiont. And Ulrich Mueller, an inte-grative biologist at the University of Texas,Austin, agrees: It’s “interesting to whatextent the presence of [another] symbiontcan fundamentally change the interaction oftwo other symbionts.” No cheating allowed Currie thinks that understanding three-,four-, and five-way interactions like the onesin the fungus gardens may ultimately revolu-tionize the way we think about the evolutionof mutualism. Why two parties should coop-erate—whether it’s two species over evolu-tionary time or two people over the course ofa day—is one of
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