Award: OCE-1335269

Sunlight drives virtually all life on the Earth?s surface, with about 50% of that light energy being transformed into organic molecules occurring in marine systems. However, prior to the year 2000, all sunlight-dependent metabolisms in the ocean were believed to be based on chlorophyll-like molecules. This traditional view of light utilization changed radically with the discovery of marine bacterial rhodopsin-like proteins (proteorhodopsins) that contain the light-sensitive pigment retinal. Since then, hundreds of articles describing proteorhodopsins? gene distribution in the world ocean have been published. These studies clearly indicate that proteorhodopsins are more abundant and widespread than we ever anticipated, with gene abundance exceeding the chlorophyll photosynthetic genes in some marine systems several-fold. Furthermore, it is now clear that proteorhodopsins are widely distributed not only in the world ocean, but also in any environment that receives sunlight. However, a major limitation of all proteorhodopsin studies is that their current quantification is not accurate, as it relies on an indirect quantification of genes or transcripts that may never be translated into proteins. The lack of a direct technique to measure marine proteorhodopsins has indubitably hindered our understanding of their truly ecological role on important biogeochemical processes including their contribution to the energetic balance of the planet. To better assess the ecological relevance of proteorhodopsins, we have developed a method to analytically quantify the pigment retinal in the proteorhodopsins. Because each proteorhodopsin contains a single retinal, the total number of retinal molecules is equivalent to the total number of proteorhodopsins. We have applied this technique to samples collected in different contrasting marine environments ranging from nutrient-enriched coastal waters to the nutrient-depleted open ocean. While most marine studies have focused on establishing the ecological importance of proteorhodopsins in the open ocean, our results show that proteorhodopsins are widespread even in coastal environments. We also show that proteorhodopsin provides a physiological advantage to the bacteria that contain it by providing enough energy to sustain cellular basal metabolism. This is an important finding that could explain how the microbial communities in large areas of the world ocean subsist when organic matter from algal blooms is not available. Therefore, the survival of heterotrophic bacteria depends greatly on solar energy when organic matter for decomposition is not accessible. Our results also show that the ubiquitous proteorhodopsin-containing bacteria are key contributors to the solar energy captured and stored in the sea. In fact, the amount of depth-integrated solar energy harvested by proteorhodopsins that could potentially be transformed into biochemical energy is even higher than the amount of energy trapped by phytoplankton containing chlorophyll-a. Our data also suggest that the role of proteorhodopsin in the world ocean may increase in the future due to the expansion of oligotrophic environments in response to climate change. Furthermore, current heat balance estimates for the surface ocean could be misleading as those estimates are only based on the energy capture by chlorophyll-a containing phytoplankton. Last Modified: 11/04/2017 Submitted by: Sergio A Sanudo-Wilhelmy