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De novo transcriptomics reveal distinct phototransduction signaling components in the retina and skin of a color-changing vertebrate, the hogfish (Lachnolaimus maximus)

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Abstract

Across diverse taxa, an increasing number of photoreceptive systems are being discovered in tissues outside of the eye, such as in the skin. Dermal photoreception is believed to serve a variety of functions, including rapid color change via specialized cells called chromatophores. In vitro studies of this system among color-changing fish have suggested the use of a phototransduction signaling cascade that fundamentally differs from that of the retina. Thus, the goal of this study was to identify phototransduction genes and compare their expression in the retina and skin of a color-changing fish, the hogfish Lachnolaimus maximus. De novo transcriptomics revealed the expression of genes that may underlie distinct, yet complete phototransduction cascades in L. maximus retina and skin. In contrast to the five visual opsin genes and cGMP-dependent phototransduction components expressed in the retina of L. maximus, only a single short-wavelength sensitive opsin (SWS1) and putative cAMP-dependent phototransduction components were expressed in the skin. These data suggest a separate evolutionary history of phototransduction in the retina and skin of certain vertebrates and, for the first time, indicate an expression repertoire of genes that underlie a non-retinal phototransduction pathway in the skin of a color-changing fish.

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Abbreviations

CNS:

Central nervous system

COGs:

Cluster of orthologous groups of proteins

GO:

Gene ontology

GPCR:

G-protein-coupled receptor

ORF:

Open-reading frame

PDE:

Phosphodiesterase

TPM:

Transcripts per million reads

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Acknowledgements

We would like to acknowledge Duke University’s Shared Cluster Resource and Duke Biology’s Charles W. Hargitt Research Fellowship, which were essential to the success of the presented work. We also thank Dr. Nicholas Marra and his colleagues for sharing their Lachnolaimus maximus cardiac transcriptome, as well as Dean Kimberly for consenting the use of his photography in our paper. Finally, we thank Benjamin R. Wheeler for his insight and logistical support that contributed to the success of this project, and Dr. Daniel Speiser, Katie Thomas, and Eleanor Caves for their insight and comments on the earlier versions of the manuscript.

Funding

This study was funded by Charles W. Hargitt Fellowship provided by Duke University.

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Authors and Affiliations

  1. Biology Department, Duke University, Durham, NC, 27708, USA

    Lorian E. Schweikert, Robert R. Fitak & Sönke Johnsen

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  1. Lorian E. Schweikert
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  2. Robert R. Fitak
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  3. Sönke Johnsen
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Correspondence to Lorian E. Schweikert.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of Duke University’s Institutional Animal Care and Use Committee (protocol registry number A233-16-10).

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Supplemental Fig. 1

Top blast-hit abundance by species yielded from BLASTx analyses of the Lachnolaimus maximus transcriptome (PDF 129 KB)

Supplemental Fig. 2

Tissue-level comparison of Lachnolaimus maximus transcriptome annotation. Venn diagrams indicate the number of unique genes and unique gene ontology (GO) terms assigned to retinal and skin tissues (a). GO term distribution for the Biological Processes category (level 2) is compared for both tissues (b) (PDF 98 KB)

Supplemental Fig. 3

Tissue-level comparison of Lachnolaimus maximus GO term transcriptome annotation. Second level GO term distribution for the Molecular Function category (a) and Cellular Component category (b) are shown (PDF 91 KB)

Supplemental Table 1

Comprehensive information table of every contig from the assembly of the hogfish (Lachnolaimus maximus) transcriptome. Mapping statistics are given for contigs combined from the retina and skin (i.e., “All”) as well as for each individual tissue: TPM = transcripts per million mapped reads, FPKM = fragments per kilobase transcript length per million fragments mapped, IsoPct = percent expression of an isoform for a given gene, ORF = open-reading frame (CSV 117609 KB)

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Schweikert, L.E., Fitak, R.R. & Johnsen, S. De novo transcriptomics reveal distinct phototransduction signaling components in the retina and skin of a color-changing vertebrate, the hogfish (Lachnolaimus maximus). J Comp Physiol A 204, 475–485 (2018). https://doi.org/10.1007/s00359-018-1254-4

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