Symbiosis turns messy in 13-year cicadas

Cicadas subsist on tree sap, which doesn't provide them all the nutrients they need to live. Bacteria in their gut, including one called Hodgkinia, turns the sap into amino acids that sustain them during their unusual lives. Cicadas spend most of their lives underground before emerging in droves, singing loudly, mating for weeks and then dying off en masse. McCutcheon studied the evolution of Hodgkinia in Magicicada tredicim, a type of cicada that burrows for 13 years. He dissected the insects and removed the bacteria, then sequenced their DNA.

What he found, shortly after setting up his own lab several years ago, perplexed him so much that he thought there was a technical mistake. "I could not make heads or tails of it," McCutcheon says. "It looked so, so broken." Hodgkinia's genome was a fragmented and overlapping mess that seemed to contain many copies of its DNA with slight variations.

He set it aside for a while, until last year, when he found that in the gut of a South American cicada with a much shorter life span, Hodgkinia had split into two separate species about five million years ago. The split left the insect reliant on double the species to create the same nutrients that required only one species to make before.

When McCutcheon's lab returned to the 13-year cicada, they found many more than two splits. Pulling apart the web of genetic information revealed the bacterium's genome had increased about 10-fold from what the scientists estimate its ancestor's DNA looked like. They found at least 17 new chromosomes or genomes, but estimate that the cicada may rely on as many as 50 to survive.

"We think Hodgkinia has a very high mutation rate," McCutcheon says. "It makes a lot of mistakes every replication cycle."

In cicadas with longer lives, those mistakes might be piling up during idle years spent underground, leading to broken genes in different cell types. McCutcheon's lab is now studying how a growing symbiont might make life difficult for cicadas. McCutcheon compares the problem with trying to care for many children -- several species of Hodgkinia -- in addition to its other symbiont, a bacterium called Sulcia.

"We can actually see a little bit of evidence for that in our data, where the tissue volume the cicada puts toward one of its children, Sulcia, is getting smaller, because of the increasing space it must devote to its growing gaggle of Hodgkinia. It's trying to accommodate all these different cell types," he says.

From a broader perspective, understanding how symbioses evolve over time could help scientists learn more about organelles such as mitochondria, which humans and all other animals depend on.

"The greater context of this is something that people in Integrated Microbial Biodiversity and CIFAR have been thinking about for a long time," McCutcheon says.

They've been studying questions such as why some organelle genomes look very different than others, and how genetic complexity arises from evolution that isn't adaptive, or beneficial to the organism. "There is no better place in the world than CIFAR to think about these fundamental and broad themes in biology," McCutcheon says.

The paper in Proceedings of the National Academy of Sciences was published in conjunction with a Sackler Colloquium co-sponsored by CIFAR and the US National Academy of Sciences, entitled "Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of Organelles."