Sternopygus macrurus electric organ transcriptome and cell size exhibit insensitivity to short-term electrical inactivity

Abstract

Electrical activity is an important regulator of cellular function and gene expression in electrically excitable cell types. In the weakly electric teleost fish Sternopygus macrurus, electrocytes, i.e., the current-producing cells of the electric organ, derive from a striated muscle lineage. Mature electrocytes are larger than muscle fibers, do not contain sarcomeres, and are driven continuously at frequencies higher than those exerted on muscle cells. Previous work showed that the removal of electrical activity by spinal cord transection (ST) for two and five weeks led to an upregulation of some sarcomeric proteins and a decrease in electrocyte size. To test whether changes in gene transcription preceded these phenotypic changes, we determined the sensitivity of electrocyte gene expression to electrical inactivity periods of two and five days after ST. Whole tissue gene expression profiles using deep RNA sequencing showed minimal alterations in the levels of myogenic transcription factor and sarcomeric transcripts after either ST period. Moreover, while analysis of differentially expressed genes showed a transient upregulation of genes associated with proteolytic mechanisms at two days and an increase in mRNA levels of cytoskeletal genes at five days after electrical silencing, electrocyte size was not affected. Electrical inactivity also resulted in the downregulation of genes that were classified into enriched clusters associated with functions of axon migration and synapse structure. Overall, these data demonstrate that unlike tissues in the myogenic lineage in other vertebrate species, regulation of gene transcription and cell size in the muscle-like electrocytes of S. macrurus is highly insensitive to short-term electrical inactivity. Moreover, together with data obtained from control and long-term ST studies, the present data suggest that neural input might influence post-transcriptional processes to affect the mature electrocyte phenotype.

Development of the electric organ in embryos and larvae of the knifefish, Brachyhypopomus gauderio

“…Such analyses of adult mEO from several electric fish species have already been reported ( Gallant et al., 2014 ). More recently, Guth et al. (2016) reported transcriptome analysis of regenerating tail showing stage specific gene expression during the developmental process of regenerating mEO.…”

“…The species has already been extensively used for electrophysiological studies (e.g. Stoddard and Salazar, 2011 ; Matsushita et al., 2013 ) and for transcriptomics ( Gallant et al., 2014 ; Guth et al., 2016 ). Previous studies have shown that the mEO in the B. gauderio develops at the ventral side of the tail myotome in the 6 days post-fertilization (dpf) larvae ( Franchina, 1997 ).…”

A conserved phenylalanine motif among Teleost fish provides insight for improving electromagnetic perception

“…Today, the Teleostei are the largest group of fish on the planet, containing approximately 95% of all living fish species, exhibiting incredible biodiversity and inhabiting waters across the globe (25). The Teleostei are currently being studied for numerous unique attributes including electrical abilities (26)(27)(28), mouthbrooding (29), brackish tolerance (30), cold tolerance (31,32), among others, and now including magnetoreception. The tree was generated using TimeTree (23).…”

A conserved phenylalanine motif among teleost fish provides insight for improving electromagnetic perception

“…Today, the Teleostei are the largest group of fish on the planet, containing approximately 95% of all living fish species, exhibiting incredible biodiversity and inhabiting waters across the globe [25]. The Teleostei are currently being studied for numerous unique attributes including electrical abilities [26][27][28], mouthbrooding [29], brackish tolerance [30] and cold tolerance [31,32], among others, and now including magnetoreception.…”