Rhodopsin gene expression regulated by the light dark cycle, light spectrum and light intensity in the dinoflagellate Prorocentrum

Abstract

The proton pump rhodopsin is widely found in marine bacteria and archaea, where it functions to capture light energy and convert it to ATP. While found in several lineages of dinoflagellates, this gene has not been studied in Prorocentrales species and whether it functionally tunes to light spectra and intensities as in bacteria remains unclear. Here we identified and characterized this gene in the bloom-forming Prorocentrum donghaiense. It is a 7-helix transmembrane polypeptide containing conserved domains and critical amino acid residues of PPR. This gene is phylogenetically affiliated to the xanthorhodopsin clade, but seems to have a distinct evolutionary origin. Quantitative reverse transcription PCR showed that in regular cultures, the transcript abundance of the gene exhibited a clear diel pattern, high abundance in the light period and low in the dark. The same diel pattern was observed for protein abundance with a Western blot using specific antiserum. The rhythm was dampened when the cultures were shifted to continuous dark or light condition, suggesting that this gene is not under circadian clock control. Rhodopsin transcript and protein abundances varied with light intensity, both being highest at a moderate illumination level. Furthermore, the expression of this gene responded to different light spectra, with slightly higher transcript abundance under green than blue light, and lowest abundance under red light. Transformed Escherichia coli over-expressing this rhodopsin gene also exhibited an absorption maximum in the blue–green region with slightly higher absorption in the green. These rhodopsin-promoting light conditions are similar to the relatively turbid marine habitat where the species forms blooms, suggesting that this gene may function to compensate for the light-limited photosynthesis in the dim environment.

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

“…The proton-pump type rhodopsins can create a proton gradient to drive synthesis of ATPase, in lieu of photosynthesis 47,48 . An earlier gene-expression analysis of the bloomforming Prorocentrum donghaiense 49 revealed that proton-pump rhodopsins may compensate for photosynthesis under light-deprived conditions. These rhodopsins were also found to be highly expressed in diatoms under iron-deficient conditions 50 .…”

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

“…The authors speculated that proton-pumping rhodopsins could contribute to the acidification of feeding vacuoles in phagotrophic dinoflagellates. Subsequent analyses in the photosynthetic dinoflagellate Prorocentrum donghaiens CCMAXU-364 showed that xanthorhodopsin gene expression is regulated by light and influenced by the light spectrum and intensity (153). Recent work on O. marina CCMP1795 showed that light induces rhodopsin expression and promotes survival under starvation (79), supposedly by providing energy for maintenance of basic cell integrity.…”

Proton‐pumping rhodopsins are abundantly expressed by microbial eukaryotes in a high‐Arctic fjord

“…All known eukaryotic xanthorhodopsins exhibit the DLE motif that characterizes maximum absorption in the green spectrum, as demonstrated for the Prorocentrum donghaiense xanthorhodopsin (Shi et al ., ). Members of the eukaryotic proteorhodopsin clade, conversely, seem to be tuned to blue light (Fig.…”

“…The ecological function of proton-pumping rhodopsins remains elusive, but includes stimulation of growth (Gomez-Consarnau et al, 2007), enhanced starvation survival (Gomez-Consarnau et al, 2010) and inorganic carbon fixation (Palovaara et al, 2014) in certain bacteria (reviewed in Pinhassi et al, 2016). In marine eukaryotes, proton-pumping rhodopsins have been suggested to provide cellular energy to photoautotrophs under iron (Marchetti et al, 2015) or light (Shi et al, 2015) limitation.…”