All became clear when he used a microscope to examine the organs in which cicadas house their microbes. Within these round structures, Matsuura saw the cells of a foreign fungus. At first, he thought that the cicadas had picked up a fungal infection, but he found the same cells in every species that lacked Hodgkinia. These insects had clearly adopted some kind of fungus and turned it into an endosymbiont that replaced the missing bacterium.
And when Matsuura sequenced the new symbiont’s DNA, he realized that it was perhaps the last fungus that anyone would have expected. As McCutcheon later said to me, “It was a motherfucking cordyceps.”
Cordyceps fungi excel at infecting and killing insects. One particular species, Ophiocordyceps unilateralis, has become famous for its ability to turn ants into zombies. It grows through an ant’s body, creating a network of filaments that commandeers the insect’s muscles. Then it compels the ant to climb a plant stem, and clamp its jaws on the underside of a leaf. Once the ant is in position, the fungus sends a long stalk through its head, culminating in a ball full of spores that rain downward and hit the ant’s colony-mates as they go about their foraging trips. In this way, the zombie fungus can claim an entire colony. It excels at infiltrating popular culture, too: It’s the organism behind the monsters of The Last of Us and the zombies of The Girl With All the Gifts.
The fungi that Matsuura discovered in the cicadas are all close relatives of this ant-killing species—all part of the same Ophiocordyceps genus. And that, to put it bluntly, is extraordinary. Even when these fungi aren’t acting as sinister puppet-masters, they’re still acting as killer parasites. Their hosts almost always end up dead, with spore-tipped stalks erupting from their corpses.
And yet Matsuura showed that cicadas have domesticated Ophiocordyceps, turning it into an essential part of their own bodies. It’s like discovering that Darth Vader is the Jedi’s new mascot, or that the Joker has replaced Alfred as Batman’s butler.
Many beneficial microbes evolve from parasitic ancestors, and the divide between these two lifestyles is more of a continuum. “So often, we want to use black-and-white definitions to define these associations between hosts and microbes,” says Nichole Broderick from the University of Connecticut. “This study is a great reminder of the greyness of biology.”
It’s also a reminder that fungi are important. “It might be worthwhile to look at them as part of an organism’s microbiome instead of merely focusing on bacteria as is done in the majority of studies,” adds Charissa de Bekker from the University of Central Florida.
Cicadas certainly encounter a lot of fungi. They spend most of their lives underground, and are constantly surrounded by fungi that live in soil. These include several species of Ophiocordyceps that specialize in parasitizing cicadas and nothing else. Matsuura suspects that some of these fungi mutated into weaker strains, which established mild and chronic infections in the cicadas’ blood without killing them outright. These strains came to coexist with their hosts. Perhaps their presence conferred some kind of benefit, like resistance to viral infections. And perhaps they might even have saved some of the cicadas from extinction.