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Vibrational modes of water predict spectral niches for photosynthesis in lakes and oceans

Abstract

Stretching and bending vibrations of water molecules absorb photons of specific wavelengths, a phenomenon that constrains light energy available for aquatic photosynthesis. Previous work suggested that these absorption properties of water create a series of spectral niches but the theory was still too simplified to enable prediction of the spectral niches in real aquatic ecosystems. Here, we show with a state-of-the-art radiative transfer model that the vibrational modes of the water molecule delineate five spectral niches, in the violet, blue, green, orange and red parts of the spectrum. These five niches are effectively captured by chlorophylls and phycobilin pigments of cyanobacteria and their eukaryotic descendants. Global distributions of the spectral niches are predicted by satellite remote sensing and validated with observed large-scale distribution patterns of cyanobacterial pigment types. Our findings provide an elegant explanation for the biogeographical distributions of photosynthetic pigments across the lakes and oceans of our planet.

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Fig. 1: Absorption properties of the water molecule.
Fig. 2: Spectral niches in the underwater light spectrum created by harmonics of the vibrational modes of the water molecule.
Fig. 3: Absorption spectra of the main cyanobacterial pigments capture the spectral niches created by the harmonics of the water molecule.
Fig. 4: Global distribution of the five spectral niches.
Fig. 5: Comparison of predicted spectral niches and global distributions of cyanobacterial pigment types.

Data availability

Datasets of all spectra shown in this study (Figs. 13 and Extended Data Figs. 15) are available67 at: https://doi.org/10.6084/m9.figshare.c.5140601.v1. Remote sensing data that support the findings of this study are available from the Ocean Color Climate Change Initiative project of the European Space Agency: http://www.oceancolour.org. Relative abundance data of cyanobacterial pigment types are obtained from refs. 5,6,7,9,22 and available in Supplementary Table 2.

Code availability

R scripts used to generate Figs. 2 and 4 are available at: https://github.com/tadzi/spectral_niches_photosynthesis

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Acknowledgements

This article is dedicated to the memory of our late colleagues M. Stomp and H. C. P. Matthijs, who provided a source of inspiration for our understanding of the spectral niches for cyanobacterial photosynthesis. We thank G. Dall’Olmo and R. M. Letelier for constructive comments on previous versions of the manuscript, M. Kehoe (University of Amsterdam) for measuring underwater spectra of the North Atlantic during the STRATIPHYT II cruise, V. M. Luimstra (University of Amsterdam) for help with the cyanobacterial absorption spectra, and F. R. Pick (University of Ottawa) and L. Vörös (Hungarian Academy of Sciences) for sampling of lake stations. We thank the Tara Oceans coordinators and consortium for support, and the captains and crew of the Tara schooner for sampling of the marine stations. This research was funded by the Dutch Research Council (NWO) under grant no. ALW-GO 14-06 and a VENI-grant to M. Stomp, and also by the French Agence Nationale de la Recherche (ANR) programs CINNAMON (ANR‐17‐CE02‐0014‐01) and EFFICACY (ANR-19-CE02-0019).

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M.S. and J.H. conceived the original idea and designed the study in collaboration with H.J.v.d.W. The radiative transfer model was run by T.H. and H.J.v.d.W. Underwater light spectra were measured by M.S. and J.H. Remote sensing data were analysed by T.H., L.B. and H.J.v.d.W. Absorption spectra of cyanobacteria were measured by M.S., J.H. and L.G. Biogeographical distributions of the pigment types were collected by T.G., F.P. and L.G. for the marine stations and by M.S. and J.H. for the lake stations and Baltic Sea. T.H. made the figures. J.H. and T.H. wrote the manuscript and H.J.v.d.W., L.G., F.P., T.G., J.A. and L.B. commented on the different manuscript versions.

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Correspondence to Jef Huisman.

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Extended data

Extended Data Fig. 1 Inherent optical properties of coloured dissolved organic matter (CDOM) and non-algal particles (NAP).

a, Absorption spectrum of CDOM; scattering by CDOM is negligible. b, Absorption and scattering spectrum of NAP used in our application (see Methods for details).

Extended Data Fig. 2 Predictions of a null model in which the vibrational modes of H2O are ignored.

a, In the null model, the absorption spectrum of water (blue-grey line) is replaced by a smooth absorption spectrum (magenta line) without the subtle shoulders of the vibrational harmonics. b, Overlay of 100 underwater scalar irradiance spectra at the euphotic depth for waters with different CDOM concentrations, calculated by the null model. The null model does not predict a spectral landscape with pronounced peaks and valleys (in contrast to models that incorporate the vibrational modes of H2O; see Fig. 2 in the main text).

Extended Data Fig. 3 Absorption spectra of chromatic acclimators grown in different light colours.

a, Fluorescence excitation spectra of Synechococcus A15-62, a chromatic acclimator that adjusts its PUB:PEB ratio. The spectra show excitation wavelengths absorbed by the cells and subsequently emitted by the phycobilisomes as fluorescence at 580 nm, when the cells are grown in blue light (blue line) or green light (green line). b, Absorption spectra of Pseudanabaena CCY9509, a chromatic acclimator that adjusts its PEB:PCB ratio. The absorption spectra are shown for cells acclimated to green light (green line), orange light (orange line), and midway during chromatic acclimation after a switch from green to orange light (black line). The spectra are normalized with respect to (a) the PEB peak at ~540 nm, and (b) the Chl-a peak at 440 nm. Spectra in (a) were measured in this study using methods described in Sanfilippo et al.68, whereas spectra in (b) are from Stomp et al.31. For comparison, grey peaks and valleys in the background show simulated underwater irradiance spectra and vertical dashed lines indicate the harmonics of the water molecule.

Extended Data Fig. 4 Comparison of simulated and measured irradiance spectra, for aquatic ecosystems ranging from the clearest ocean waters to a hypertrophic lake.

a, Simulated planar irradiance spectra at the euphotic depth for a wide range of CDOM concentrations. b, Measured planar irradiance spectra at the euphotic depth in 7 different aquatic ecosystems. The spectra were obtained from (1) the South Pacific gyre (near Easter Island), (2) North Pacific gyre (station ALOHA north of Hawaii), (3) subtropical North Atlantic (Canary Islands), (4) temperate North Atlantic (west of Ireland), (5) Baltic Sea (near Gulf of Finland), (6) lake IJsselmeer (Netherlands) and (7) lake ‘t Joppe (Netherlands). Simulated irradiance spectra in (a) that qualitatively resemble measured irradiance spectra in (b) are indicated by the same colour. The irradiance spectrum of the South Pacific gyre is from Morel et al.14; all other spectra were measured in this study. Locations of the measured spectra are mapped in Fig. 5a. Vertical dashed lines indicate the harmonics of the water molecule.

Extended Data Fig. 5 Relative availability of the spectral niches depends on absorption by CDOM and NAP.

The relative availability of a spectral niche is calculated by the radiative transfer model, as the fraction of the total scalar irradiance at the euphotic depth that falls within this spectral niche (see equation 10 in the Methods). The relative availability of the spectral niches is displayed as function of absorption by dissolved and detrital matter (that is, CDOM and NAP) at 443 nm (adg(443)), which is a variable that can be retrieved by satellite remote sensing.

Extended Data Fig. 6 Relative abundances of cyanobacterial pigment types in the Great Lakes Area of North America, Central European lakes and the Baltic Sea.

a, Great Lakes Area of North America. b, Central European lakes and the Baltic Sea. Relative abundances were estimated using epifluorescence microscopy for the lake stations5,6,7 and flow cytometry for stations in the Baltic Sea7 (Supplementary Table 2). Prochlorococcus and PUB-rich Synechococcus were not found at these stations. Data from nearby stations in the Baltic Sea are aggregated in single pie charts.

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Supplementary Video 1

Interactive plot, showing scalar irradiance spectra at the euphotic depth for a wide range of CDOM and NAP concentrations.

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Holtrop, T., Huisman, J., Stomp, M. et al. Vibrational modes of water predict spectral niches for photosynthesis in lakes and oceans. Nat Ecol Evol 5, 55–66 (2021). https://doi.org/10.1038/s41559-020-01330-x

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