Rethinking Metabolic Assumptions and Data from High Salinity Ponds

Oren has another interesting paper out, focusing on community metabolism in hypersaline systems. The communities in the studied solar salterns consist of a primary producer, the alga Dunaliella, and halophillic prokaryotes (mostly archae, of which the majority are halobacter).

In sunny conditions the phototroph Dunaliella converts light energy to chemical forms in the system, fixing carbon and producing oxygen (oxygenic photosynthesis). The produced oxygen can be used to produce energy chemically (aerobic respiration) by Dunaliella itself (when there is insufficient light energy available) but also by halophillic prokaryotes. The halophillic prokaryotes have a way of their own to use photons, using ‘retinal’ pigments to power a proton pump and generate ATP, filling a similar role that chlorophyll does in other organisms.

The abstract reads:

We have explored the use of optical oxygen electrodes to study oxygenic photosynthesis and heterotrophic activities in crystallizer brines of the salterns in Eilat, Israel. Monitoring oxygen uptake rates in the dark enables the identification of organic substrates that are preferentially used by the community. Addition of glycerol (the osmotic solute synthesized by Dunaliella) or dihydroxyacetone (produced from glycerol by Salinibacter) enhanced respiration rates. Pyruvate, produced from glycerol or from some sugars by certain halophilic Archaea also stimulated community respiration. Fumarate had a sparing effect on respiration, possibly as many halophilic Archaea can use fumarate as a terminal electron acceptor in respiration. Calculating the photosynthetic activity of Dunaliella by monitoring oxygen concentration changes during light/dark incubations is not straightforward as light also affects respiration of some halophilic Archaea and Bacteria due to action of light-driven proton pumps. When illuminated, community respiration of brine samples in which oxygenic photosynthesis was inhibited by [the herbicide] DCMU decreased by ~40%. This effect was interpreted as the result of competition between two energy yielding systems: the bacteriorhodopsin proton pump and the respiratory chain of the prokaryotes. These findings have important implications for the interpretation of other published data on photosynthetic and respiratory activities in hypersaline environments.

So a measurement is made of the total energy needs, which can only be met using respiration when the lights are off, of a community consisting of principally Dunaliella and halophillic prokaryotes. When the lights are turned on the total respiration used to meet the same community’s energy needs, drops by about 40%. Since Dunaliella has been prevented (with DCMU) from using photosynthesis (and is thus presumably still respiring at the same rate) the drop is inferred to be coming from the prokaryotes, which seem, effectively, to opt in light to produce some portion of the energy they need from their retinal proton pumps, thereby reducing their respiration requirement.

A couple of other excerpts summarize the implications

The fact that light excitation of retinal-based proton pumps may cause a significant decrease in respiration of the (photo)heterotrophs that dominate the prokaryotic community in the system now requires a critical re-evaluation of all older data on primary productivity in salt lakes and saltern ponds […], as respiration of the prokaryotic heterotrophic component of the community may be strongly light-dependent.

There’s also an interesting side point made in the paper about the advantages of the characteristic low background oxygen level and high community densities for in situ activity studies in these sorts of systems.