Flow of light energy in benthic photosynthetic microbial mats

Abstract

This work presents, the first balanced light energy budget for a benthic microbial mat ecosystem, and shows how the budget and the spatial distribution of the local photosynthetic efficiencies within the euphotic zone depend on the absorbed irradiance (Jabs). It demonstrates the factors affecting variations in light utilization efficiency and invistigates sptial heterogeniety in photosynthetic efficiency between samples collected from distant geographical locations. Our approach employs microscale measurements of the rates of heat dissipation, gross photosynthesis and light absorption in the system, and a model describing light propagation and conversion in a scattering-absorbing medium. The energy budget was dominated by heat dissipation on the expense of photosynthesis: at light limiting conditions, 95.5% of the absorbed light energy dissipated as heat and 4.5% was channeled into photosynthesis. This energy disproportionation was light dependant. At light limiting conditions the maximum photosynthetic effciency was measured, and decreased with increasing inciedent light intensity. Maximum photosynthetic efficiencies varied with depth in the euphotic zone. Due to steep light gradients, photosynthetic efficiencies varied differently with increasing irradiances at different depths in the euphotic zone; e.g., at Jabs > 700 micro mol photon m-2 s-1, they reached around 10% of the maximum values at depths 0 - 0.3 mm and progressively increased towards 100% below 0.3 mm.. The mats, originating from distant geographical locations, differed with respect to the structure and composition of the phototrophic community, thickness of the photosynthetically active zone and pigment concentrations in this zone, but not with respect to the areal photosynthetic activity at light saturation. In all mats, the efficiency of light energy conservation by photosynthesis increased with decreasing light intensity, reaching maximum at light limiting conditions. The maximum photosynthetic efficiency varied among the studied mats between 4.5 - 16.2%, and was positively correlated with the rate of light attenuation and the average concentration of photo-pigments in the euphotic zone of the mat. For all mats, the maximum photosynthetic efficiencies were much lower than those estimated for an ideal system that absorbs the same fraction of incident light as the mats, for which the theoretical maximum is 27.7%. The photosynthetic microbial mats were more efficient in conserving the light energy at light limiting conditions when their euphotic zone was thinner and more densely populated by photosynthetic cells, and the efficiency was significantly lowered due to light absorption by photosynthetically inactive components of the mat ecosystem. We applied hyperspectral and PAM imaging to study small- and large-scale variability in pigment distribution, maximum quantum yield of PSII (Ymax) and light adaptation of cyanobacterial mats from distant geographical locations. The maximum quantum yield and light acclimation intensity exhibited pronounced vertical and horizontal heterogeneity on a sub-millimetre scale. They generally decreased in a correlated manner with depth in the mat, with gradients that varied greatly within as well as between samples. Average values of the Ymax, light acclimation intensity and pigment absorbance varied between samples, but grouped in significantly different clusters according to the geographical origin. This was similar to the grouping of the mats based on their microbial community structure derived from ARISA fingerprinting profiles. The present study provides the base for addressing in much more detail the photobiology of densely populated photosynthetic systems with intense absorption and scattering. Furthermore, our analysis has promising applications in other areas of photosynthesis research such as plant biology and biotechnology.