Microbes and insects often interact in a delicate symbiosis. The microbes provide nutrients that the insects need and the insects provide a home for the microbes. In the case of the cicada-microbe interactions, the bacteria Hodgkinia provides the essential amino acids histidine and methionine. Over time, the endosymbionts, the microbes living within the host cells, become metabolically integrated with the host, and the endosymbiont genome becomes reduced, leaving few genes outside of the core processes.
But, something strange happened in the cicada Tettigades undada. The three-member symbiosis (cicada and two endosymbiont) became a four-way symbiosis. James Van Leuven and John McCutcheon from the University of Montana found this out in 2014.
Identifying the Hodgkinia genome split
At first, they were confused. McCutcheon sequenced the Hodgkinia genome from a different cicada in 2009. The three-member symbiosis the lab deciphered previously showed the cicada Diceroprocta semicincta has two bacterial endosymbionts: Candidatus Sulcia muelleri and Hodgkinia. The Hodgkinia genome was small, encoding about 140 genes.
But when Van Leuven sequenced the genomes from the cicada (Tettigades undada), he couldn’t piece together the Hodgkinia genome. The researchers could assemble the Sulcia genome, but the Hodgkinia genome kept assembling into two distinct chromosomes.
The two chromosomes have complementary patterns of gene loss and retention. In most cases, if a gene was lost in one genome, it was retained in the other. Here’s what they found:
- 136 out of the 137 protein-coding genes from the original Hodgkinia species were retained and functional.
- 72 genes were functional in both genomes.
- 68 were functional on one genome but not the other.
The next question the researchers asked was if the two Hodgkinia genomes resided in one cell or if the genomes split into two cells. They labeled different regions of the genome with fluorescently probes so that one chromosome would fluoresce yellow and the other would fluoresce in blue. They saw little overlap of the yellows and blue meaning that the two Hodgkinia genomes came from different cells.
So how did this happen? The researchers think this slowly happened when mutations that inactivate at least one gene occur in two different Hodgkinia cells residing in the same insect. These mutations can rise to a high level in the insect, and the ancestral Hodgkinia cells are purged. Over time, more and more gene inactivations like this give rise to even more distinct Hodgkinia genomes.
Hodgkinia complexity is inevitable
McCutcheon hypothesized that the long life cycles of cicadas enabled the genomes to split. The lab tested this hypothesis by examining the Hodgkinia genome in Magicicada tredecim, one of the longest-lived cicadas with a 13-year life cycle. They saw that the Hodgkinia genome fragmented into multiple circles, with some circles partitioned into discrete cells. (The team called these “circles” at the time because it was unclear if some of these were actually new genomes or plasmid-like molecules.) Later, the researchers found that the Hodgkinia genomes in all Magicicada species exist as complexes of over 20 circular molecules.
The split doesn’t seem to have any functional benefits on the symbiosis. In other words, it’s a non-adaptive (or even maladaptive) evolution. But now, the cicada must ensure that the offspring receive a full set of Hodgkinia genes. If the symbiosis becomes so complex that the offspring don’t get a full set of genes, the species get closer and closer to extinction. In 2018, the lab found out the cicadas developed a way to counteract this: cicada eggs with more complex Hodgkinia receive more Hodgkinia cells than cicada carrying less complex Hodgkinia.
“Sometimes increased complexity is inevitable,” McCutcheon says.
Further reading
Changes in Endosymbiont Complexity Drive Host-Level Compensatory Adaptations in Cicadas. mBio, 2018.
Convergent evolution of metabolic roles in bacterial co-symbionts of insects. PNAS, 2009.
