Phytochromes in Diatoms: Sensing Far-Red Light in the Deep Blue Sea

In land plants, phytochromes sense red and far-red light and participate in regulation of germination, photomorphogenesis, and circadian rhythms. For aquatic plants, the light spectrum changes with depth, as water attenuates red and far-red wavelengths at increasing depth (Ragni and Ribera d’Alcala, 2004). Nevertheless, many aquatic organisms, including different lineages of algae, have phytochromes, although the functions of these phytochromes remain unclear.

Plant phytochromes convert between Pr and Pfr forms, yet recent studies have revealed marked spectral diversity of algal phytochromes, some of which can sense blue and green light (Duanmu et al., 2014). Substantial divergence of signaling output domains has also occurred in the green plant lineage (Li et al., 2015). In a new Breakthrough Report, Fortunato et al. (2016) examine phytochromes (DPHs) from the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. These DPHs showed typical conserved domain architecture with a conserved photosensory control module; however, phylogenetic comparison and biochemical analysis suggest that this domain binds biliverdin IXα, the precursor of plant and green algal phytochrome chromophores. Like plant phytochromes, DPH also photoconverts between Pr and Pfr forms. Transcript levels of P. tricornutum DPH (Pt-DPH) decrease in dark conditions but increase at the end of the light period. By contrast, HA-tagged Pt-DPH expressed under its native promoter accumulated in the dark and decreased in the light. These opposite patterns suggest regulation of DPH by light at the transcriptional and posttranscriptional levels.

Next, the authors investigated DPH function by examining changes in the P. tricornutum transcriptome in response to a shift from dark to red or far-red light, identifying genes that respond to red light, far-red light, or both. Using TALE-mediated genome editing to generate knockout mutants, the authors showed that Pt-DPH mutants lost the response to far-red light but retained a normal response to red light. Consistent with this, light-regulated kinase activity of Pt-DPH is enhanced by far-red light and inhibited by red light. These data present a paradox, since aquatic environments lack red and far-red light, except near the water’s surface.

Unlike the typical sessile plant, diatoms can be moved by currents of water to different places in the water column; for example, upwelling might bring diatoms from a deep, low-light environment to a shallower, high-light environment. Diatoms occur at different abundances at different depths (see figure, left) and experience differences in light environment with depth (see figure, center). One question about the function of DPH is whether it senses far-red light from sunlight as part of photoperiodic responses or to help the diatoms detect when they are near the surface. Modeling of red and far-red light from sources other than sunlight, such as chlorophyll autofluorescence and Raman scattering, indicates that for diatoms at more than one meter below the surface, DPH likely does not respond to the ratio of red to far-red light (see figure, right). DPH might also function in deeper water to sense light from chlorophyll autofluorescence, which may allow diatoms to sense the density of algal cells, all intriguing possibilities for future research on what the authors term the “aquatic phytochrome conundrum.”

Changes in diatom abundance and light signatures with depth. Left: The diatoms Thalassiosira rotula (yellow) and Skeletonema costatum (green) differ in abundance at different depths. Center: Filled circles indicate total irradiance E(tot), and open circles indicate irradiance from sunlight E(sl) at different depths. Right: Differences in light capture of Pr and Pfr forms of DPH. (Reprinted from Fortunato et al. [2016], Figures 5B to 5D.)