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Electric Eel Genome Illuminates Convergent Evolution of Electric Organs

NEW YORK (GenomeWeb) – Although fish like electric eels and electric rays are separated by millions of years of evolution, a comparative analysis of their genomes and the genomes of other electric fish indicates they've relied on similar genes and pathways to evolve their ability to generate a jolt, researchers led by Michael Sussman from the University of Wisconsin reported today in Science.

Electric organs have evolved half a dozen times, arising from the conversion of muscle cells to electrocytes. These cells are larger than muscle cells and lack or have dysfunctional versions of the contractile machinery typical of muscle cells, but they can generate higher voltages than muscle cells.

Electrocytes have an enervated surface enriched for cation-specific ion channels, while the opposite, folded-in membrane includes sodium pumps. This asymmetry of the cells, the researchers said, allows them to be stacked "like batteries in a series in a flashlight."

"The surprising result of our study is that electric fish seem to use the same 'genetic toolbox' to build their electric organ," first author Jason Gallant, an assistant professor of zoology at Michigan State University, said in a statement.

Fish use these organs for a combination of defense, predation, navigation, and communication. Electric eels, the researchers pointed out, can generate an electric field of up to 600 volts, several times that of a household outlet.

Sussman, Gallant, and their colleagues generated a draft assembly of the electric eel, Electrophorus electricus, genome as well as short-read mRNA sequences from the eels' three electric organs — main, Sachs', and Hunter's — and its kidney, brain, spinal cord, heart, and skeletal muscle.

Using those mRNA sequences, the researchers developed more than 29,000 gene models representing about 22,000 protein-coding genes. Some 211 genes, they found, were upregulated only in electric organs, while 186 were downregulated in them, as compared to skeletal and heart muscles.

The researchers also sequenced and assembled transcriptomes from electric organs and skeletal muscles of two other Gymnotiformes from South America —Sternopygus macrurus and Eigenmannia virescens — as well as from the more distantly related mormyroid Brienomyrus brachyistius from Africa and the electric catfish Malapterurus electricus.

Across these volt-producing lineages, a number of transcription factors, the researchers said, are differentially expressed in electric organs versus muscles. For instance, Six2a, which targets ARE promoter elements in Na+/K+ adenosine triphosphatases, is upregulated, while other transcription factors like myogenin and six4b, which are involved in muscle differentiation, are downregulated.

Other differentially upregulated genes hinted at how the fish can generate and conduct their shocks in one direction through their bodies and into the water.

Two collagen genes — col6a6, which is associated with muscle fibers, and col141a1, which is more widely expressed — are upregulated in the electric organs. Collagen, the researchers noted, is deposited in the extracellular domain of the basal lamina and is maintained by membrane-spanning molecules that are also attached to the cytoskeleton. Two of those membrane-spanning molecules are also upregulated in electric organs, suggesting to the researchers that these features are involved in maintaining the unidirectional conduction of the electrical jolt.

Unsurprisingly, a number of transporters and voltage-dependent ion channels, along with their regulators, were also highly expressed in electric organs, the researchers found.

One, though, the atap1a2a gene, which encodes the alpha subunit of the sodium pump, the researchers said, resembled the isoform expressed in the transverse tubules of muscle and in the villi of the invaginated side of the electric eel electroctye. This, they added, indicates that the uninnervated side of the electrocyte could be derived from the T-tubule membrane.

As the electric organs of the various shock-producing fish also lost the excitation-contraction pathway of muscle cells, the researchers found that sarcomeric and sarcoplasmic reticulum-related genes were downregulated, though to varying degrees.

Mormyroids, they noted, still have sarcomere-like structures, though they are disrupted. Still, the gene encoding the L-type calcium channel of T-tubules that is associated with excitation-contraction coupling in muscles is downregulated in all the lineages.

"We hypothesize that the early evolution of the EO included the downregulation of this suite of genes, disabling contraction," Sussman, Gallant, and their colleagues wrote in their paper.

Additionally they suspected that the larger size of electrocytes as compared to muscle fibers might be due to changes in insulin-like growth factor signaling pathway genes. IGF signaling, they noted, is linked to increased body size and developmental rate, and can work in a tissue-specific fashion.

In the fish, genes like igfII, pik3r3b, and a net37-like gene, which are involved in IGF signaling are upregulated in electrocytes, while a negative downregulator of the pathway was itself downregulated.

"[T]he observed changes in expression in these key IGF signaling pathway genes suggest a conserved pathway among electrocytes that contributes to their increased size," the researchers added.

All together, this indicated that common regulatory and transcriptional pathways were targeted in the convergent evolution of electric organs.

"By learning how nature does this, we may be able to manipulate the process with muscle in other organisms," Sussman said in a statement, "and, in the near future, perhaps use the tools of synthetic biology to create electrocytes for generating electrical power in bionic devices within the human body or for uses we have not thought of yet."

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