Proton-pumping rhodopsins promote the growth and survival of phytoplankton in a highly variable ocean

Abstract

Proton-pumping rhodopsins (PPRs) utilize sunlight to produce cellular energy. They are widely distributed in marine phytoplankton and were recently shown to occur in the vacuolar membrane of a marine diatom, making the vacuole a second light transducing organelle. Of course, the first, the chloroplast, is where photosynthesis occurs. However, the two light-driven sources of cellular energy are quite different and, in many ways, complement one another. Photosynthesis works best at low to intermediate light intensities, and is inhibited at high light, while PPR is predicted to work best at high light intensities. And photosynthetic rates decrease with decreasing temperature and are subject to iron limitation, while PPR photochemistry is not directly limited by iron, and is unaffected by temperature. Thus, the two phototrophic systems are favored under different sets of conditions. Placing PPR in the vacuole may benefit this complementary situation where one or the other phototrophic process is favored depending on the environmental conditions. And here, the presence of PPR in the vacuole may be especially beneficial for growth and survival as that organelle often acts as a storage site for cellular energy in the form of the phosphate anhydride bonds of polyphosphates. We hypothesize that this complementary behavior, along with the ability to store excess energy produced by PPR in the vacuole as high energy polyphosphates, represents an important survival strategy in the ocean, where light, iron levels, and temperature vary widely on a variety of spatial and temporal scales.