Microbial rhodopsins are major contributors to the solar energy captured in the sea

Abstract

All known phototrophic metabolisms on Earth rely on one of three categories of energy-converting pigments: chlorophyll-a (rarely -d), bacteriochlorophyll-a (rarely -b), and retinal, which is the chromophore in rhodopsins. While the significance of chlorophylls in solar energy capture has been studied for decades, the contribution of retinal-based phototrophy to this process remains largely unexplored. We report the first vertical distributions of the three energy-converting pigments measured along a contrasting nutrient gradient through the Mediterranean Sea and the Atlantic Ocean. The highest rhodopsin concentrations were observed above the deep chlorophyll-a maxima, and their geographical distribution tended to be inversely related to that of chlorophyll-a. We further show that proton-pumping proteorhodopsins potentially absorb as much light energy as chlorophyll-a-based phototrophy and that this energy is sufficient to sustain bacterial basal metabolism. This suggests that proteorhodopsins are a major energy-transducing mechanism to harvest solar energy in the surface ocean.

Fig. 1. Sectional distributions of pigment concentrations measured along the Mediterranean Sea and in the Eastern Atlantic Ocean.

(A) Map of sampling stations. (B) Distribution of retinal in rhodopsins. (C) Chlorophyll-a (Chl-a). (D) Bacteriochlorophyll-a (Bcl-a). The black circles indicate the depths of sampling.

Fig. 2. Depth profiles of pigment concentrations (rhodopsin retinal, Bchl-a, and Chl-a) measured at the different basins of the Mediterranean Sea and Eastern Atlantic Ocean.

Stations 2, 4, and 9 are representative of oligotrophic regions of the Eastern Mediterranean; stations 17, 20, and 23 were sampled in the coastal-influenced Western Mediterranean; and station 28 was sampled in the Eastern Atlantic Ocean.

Fig. 3. Geographical distribution of the depth-integrated light energy captured by PR, Chl-a photosystem (PS–Chl-a), and AAP–Bchl-a at the different sampling regions of the Mediterranean Sea and Eastern Atlantic Ocean within the photic zone (0 to 200 m).

A photocycle of 10 ms was used for the PR calculations, as DNA sequence, spectral tuning, and kinetics data (6, 44) show that most PRs from surface temperate waters have fast photocycles typical of H⁺ pumps. To account for any retinal signal originating from heliorhodopsin, which could represent ~20% of all rhodopsins in the photic zone (10), 80% of the quantified retinal signal was used in these calculations. Solid lines denote estimates using all PAR (400 to 700 nm). Those represent the maximum energy estimates, which assume that also accessory pigments can access all wavelengths (PAR; 400 to 700 nm). Conservative energy calculations using specific wavelengths for blue-absorbing (490 nm) and green-absorbing (530 nm) PR are shown in dashed lines.

Fig. 4. Rhodopsin cellular quotas (molecules cell⁻¹) measured in the picoplankton collected in the different basins of the Mediterranean Sea and in the Eastern Atlantic Ocean compared with prior studies.

^aSamples measured in this study: Eastern Mediterranean (stations 2 to 12), Western Mediterranean (stations 13 to 24), and Atlantic Ocean (stations 25 to 29) and Vibrio sp. AND4; ^bmetaproteomics estimates from (16); laser flash photolysis measurements: ^cSAR11 bacterium Candidatus Pelagibacter ubique HTCC1062 (17), ^dSAR86 bacteria (15), and ^eHalobacterium salinarum (38). The line within the boxplot is the median, the dot is the mean, and the boundary of the boxes indicates the 25th and 75th percentiles. Error bars to the left and to the right of the box indicate the 10th and 90th percentiles.

Fig. 5. Light energy captured per cell by PR, Bchl-a (AAP–Bchl-a), and Chl-a (PS–Chl-a) in the Mediterranean Sea and Eastern Atlantic Ocean.

These calculations assumed hyperbolic response to light, that 75% of the total heterotrophic bacteria contain PR genes and 2.5% contain Bchl-a (see Supplementary Materials and Methods and table S5). To account for any retinal signal originating from heliorhodopsin, which could represent ~20% of all rhodopsins in the photic zone (10), 80% of the quantified retinal signal was used in these calculations. Chl-a–containing cells were estimated as the addition of the Prochlorococcus, Synechococcus, and picoeukaryote counts measured with flow cytometry. As reference, the gray horizontal band denotes the estimated energy range necessary to maintain basal metabolism or survival in heterotrophic bacteria (16). Dotted boxes denote estimates using all PAR (400 to 700 nm). Conservative calculations using only specific wavelengths for blue-absorbing (490 nm) and green-absorbing (530 nm) PR are shown as blue and green boxes.