Diel transcriptional oscillations of light-sensitive regulatory elements in open-ocean eukaryotic plankton communities

Abstract

Significance Most organisms coordinate key biological events to coincide with the day/night cycle. These diel oscillations are entrained through the activity of light-sensitive photoreceptors that allow organisms to respond rapidly to changes in light exposure. In the ocean, the plankton community must additionally contend with dramatic changes in the quantity and quality of light over depth. Here, we show that the predominantly blue-light field in the open-ocean environment may have driven expansion of blue light-sensitive regulatory elements in open-ocean eukaryotic plankton derived from secondary and tertiary endosymbiosis. The diel transcription of genes encoding light-sensitive elements indicate that photosynthetic and heterotrophic marine protists respond to and anticipate fluctuating light conditions in the dynamic marine environment. The 24-h cycle of light and darkness governs daily rhythms of complex behaviors across all domains of life. Intracellular photoreceptors sense specific wavelengths of light that can reset the internal circadian clock and/or elicit distinct phenotypic responses. In the surface ocean, microbial communities additionally modulate nonrhythmic changes in light quality and quantity as they are mixed to different depths. Here, we show that eukaryotic plankton in the North Pacific Subtropical Gyre transcribe genes encoding light-sensitive proteins that may serve as light-activated transcription factors, elicit light-driven electrical/chemical cascades, or initiate secondary messenger-signaling cascades. Overall, the protistan community relies on blue light-sensitive photoreceptors of the cryptochrome/photolyase family, and proteins containing the Light-Oxygen-Voltage (LOV) domain. The greatest diversification occurred within Haptophyta and photosynthetic stramenopiles where the LOV domain was combined with different DNA-binding domains and secondary signal-transduction motifs. Flagellated protists utilize green-light sensory rhodopsins and blue-light helmchromes, potentially underlying phototactic/photophobic and other behaviors toward specific wavelengths of light. Photoreceptors such as phytochromes appear to play minor roles in the North Pacific Subtropical Gyre. Transcript abundance of environmental light-sensitive protein-encoding genes that display diel patterns are found to primarily peak at dawn. The exceptions are the LOV-domain transcription factors with peaks in transcript abundances at different times and putative phototaxis photoreceptors transcribed throughout the day. Together, these data illustrate the diversity of light-sensitive proteins that may allow disparate groups of protists to respond to light and potentially synchronize patterns of growth, division, and mortality within the dynamic ocean environment.