Abstract
We investigated the radiative energy budgets of a heterogeneous photosynthetic coral reef sediment and a compact uniform cyanobacterial biofilm on top of coastal sediment. By combining electrochemical, thermocouple and fiber-optic microsensor measurements of O2, temperature and light, we could calculate the proportion of the absorbed light energy that was either dissipated as heat or conserved by photosynthesis. We show, across a range of different incident light regimes, that such radiative energy budgets are highly dominated by heat dissipation constituting up to 99.5% of the absorbed light energy. Highest photosynthetic energy conservation efficiency was found in the coral sediment under low light conditions and amounted to 18.1% of the absorbed light energy. Additionally, the effect of light directionality, i.e., diffuse or collimated light, on energy conversion efficiency was tested on the two surface-associated systems. The effects of light directionality on the radiative energy budgets of these phototrophic communities were not unanimous but, resulted in local spatial differences in heat-transfer, gross photosynthesis, and light distribution. The light acclimation index, Ek, i.e., the irradiance at the onset of saturation of photosynthesis, was >2 times higher in the coral sediment compared to the biofilm and changed the pattern of photosynthetic energy conservation under light-limiting conditions. At moderate to high incident irradiances, the photosynthetic conservation of absorbed energy was highest in collimated light; a tendency that changed in the biofilm under sub-saturating incident irradiances, where higher photosynthetic efficiencies were observed under diffuse light. The aim was to investigate how the physical structure and light propagation affected energy budgets and light utilization efficiencies in loosely organized vs. compact phototrophic sediment under diffuse and collimated light. Our results suggest that the optical properties and the structural organization of phytoelements are important traits affecting the photosynthetic efficiency of biofilms and sediments.
Highlights
Photosynthetic sediments and biofilms are characterized by pronounced vertical stratification of the microbial environment as a result of steep light gradients, high metabolic activity and limitations of heat and solute transport by diffusion (Kühl et al, 1996; Kühl and Fenchel, 2000; Al-Najjar et al, 2012)
When light energy absorption exceeds the capacity for light utilization, excess energy is channeled into heat production via non-photochemical quenching (NPQ) processes to avoid degradation of pigments and other cell constituents e.g., by reactive singlet oxygen produced by the de-excitation of triplet state chlorophyll (3Chl∗) (Müller et al, 2001)
We found that a higher fraction of the absorbed light energy was conserved by photosynthesis in the heterogenous loosely organized coral sediment, while the radiative energy budgets of both sediment types were highly dominated by dissipation of heat
Summary
Photosynthetic sediments and biofilms are characterized by pronounced vertical stratification of the microbial environment as a result of steep light gradients, high metabolic activity and limitations of heat and solute transport by diffusion (Kühl et al, 1996; Kühl and Fenchel, 2000; Al-Najjar et al, 2012). The radiative energy balance in such phototrophic microbial communities is affected by the incident radiative energy from the sun, of which a fraction is backscattered and not absorbed, while absorbed light energy is either photochemically conserved via photosynthesis or dissipated as heat via radiative energy transfer and non-photochemical quenching (NPQ; Al-Najjar et al, 2010; Brodersen et al, 2014). A sub-saturating flux of photons will limit the rate of photosynthesis, as the available light is insufficient to support the maximal potential rate of the light reactions. As the photon flux increases, photosynthesis saturates, whereby O2 becomes a competitive inhibitor on the binding-site of CO2 to Ribulose1,5-bisphosphate carboxylase oxygenase (Rubisco; Falkowski and Raven, 2007). When light energy absorption exceeds the capacity for light utilization, excess energy is channeled into heat production via NPQ processes to avoid degradation of pigments and other cell constituents e.g., by reactive singlet oxygen produced by the de-excitation of triplet state chlorophyll (3Chl∗) (Müller et al, 2001)
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