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

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Science Advances  07 Aug 2019:
Vol. 5, no. 8, eaaw8855
DOI: 10.1126/sciadv.aaw8855
  • 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.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/8/eaaw8855/DC1

    Supplementary Materials and Methods

    Fig. S1. Inorganic nutrient concentrations measured along the Mediterranean Sea and East Atlantic Ocean.

    Fig. S2. Retinal oxime reextraction test.

    Fig. S3. Concentrations of retinal oxime in Vibrio sp. AND4 extracted using hydroxylamine under different light conditions.

    Fig. S4. Retinal extraction time optimization in Vibrio sp. AND4.

    Fig. S5. Number of retinal molecules (as retinal oxime) measured in the Vibrio sp. AND4 wild-type (wt) and in the knockout mutant strain (Δprd).

    Fig. S6. Concentration of rhodopsin-bound retinal (as retinal oxime) measured in surface waters collected in January 2015 at station SPOT.

    Fig. S7. Contribution of the potential energy captured by PRs at different depths.

    Table S1. Summary of treatments used to optimize the extraction and detection of retinal, retinal oxime, and Bchl-a.

    Table S2. Transformation of retinal into retinal oxime using all-trans retinal standards.

    Table S3. Light wavelength characteristics.

    Table S4. Parameters used to calculate the light energy captured shown in Figs. 3 and 5.

    Table S5. Parameters used to calculate the cellular daily energy yield per photosystem shown in Fig. 5 and data S1.

    Data S1. Detailed sampling measurements and calculations obtained in the Mediterranean Sea and East Atlantic Ocean from 30 April to 28 May 2014.

    References (4555)

  • Supplementary Materials

    The PDF file includes:

    • Supplementary Materials and Methods
    • Fig. S1. Inorganic nutrient concentrations measured along the Mediterranean Sea and East Atlantic Ocean.
    • Fig. S2. Retinal oxime reextraction test.
    • Fig. S3. Concentrations of retinal oxime in Vibrio sp. AND4 extracted using hydroxylamine under different light conditions.
    • Fig. S4. Retinal extraction time optimization in Vibrio sp. AND4.
    • Fig. S5. Number of retinal molecules (as retinal oxime) measured in the Vibrio sp. AND4 wild-type (wt) and in the knockout mutant strain (Δprd).
    • Fig. S6. Concentration of rhodopsin-bound retinal (as retinal oxime) measured in surface waters collected in January 2015 at station SPOT.
    • Fig. S7. Contribution of the potential energy captured by PRs at different depths.
    • Table S1. Summary of treatments used to optimize the extraction and detection of retinal, retinal oxime, and Bchl-a.
    • Table S2. Transformation of retinal into retinal oxime using all-trans retinal standards.
    • Table S3. Light wavelength characteristics.
    • Table S4. Parameters used to calculate the light energy captured shown in Figs. 3 and 5.
    • Table S5. Parameters used to calculate the cellular daily energy yield per photosystem shown in Fig. 5 and data S1.
    • Legend for data S1
    • References (4555)

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    Other Supplementary Material for this manuscript includes the following:

    • Data S1 (Microsoft Excel format). Detailed sampling measurements and calculations obtained in the Mediterranean Sea and East Atlantic Ocean from 30 April to 28 May 2014.

    Files in this Data Supplement:

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