Photoheterotrophy in marine prokaryotes

A review of: Zubkov, M. V. (2009) Photoheterotrophy in marine prokaryotes. J. Plankton Res. 31: 933-938

Knowledge of light- utilizing prokaryotes has increased rapidly driven by the growing interest of the scientific community to understand the microbial use of solar energy. The intention of the author is to propose new avenues of enquiry. This is achieved by examining how solar radiation is exploited in the photic zone by investigating the different metabolic strategies used by marine microbes.

Over half of the prokaryotes found in our oceans populate the thin surface layer known as the ‘photic’ layer. These organisms have adapted to develop mechanisms which absorb and exploit solar energy as a way to increase their metabolism. Recently, the attention of the scientific community has largely been on aspects of oxygenic photosynthesis because of its global biological and geological significance in the generation of oxygen and carbon reduction. However, as evidence of alternative metabolic methods which contribute to the survival of microbial communities emerges, the author advocates that a shift in the attention of the scientific community may be of interest.

Photoheterotrophy is a common strategy adopted by marine prokaryotes. Photoheterotrophic acquisition of organic molecules containing nitrogen by cyanobacteria is suggested to be energetically beneficial to an individual when compared with de novo synthesis of the same molecules. Photoheterotrophic organisms are suggested to be better adapted to variable light conditions and dark periods by storing some light energy as chemical bonds or by switching to heterotrophy.

The author suggests that the role of photosynthesis in phototrophic organisms assumed in previous research is too narrow because other aspects of utilising light have been overlooked. Both principal types of light harvesting (rhodopsin-based and chlorophyll-based) produce energy via a photon induced electrochemical potential gradient. This can be used for photophosphorylation which is preserved as ATP. This ATP can be utilised in various metabolic processes, one of which is photosynthetic carbon reduction. Bacteriorhodopsin/proteorhodopsin based light absorption is discussed as an alternative to chlorophyll-based light harvesting. This method of utilising light is noted to be a relatively small evolutionary step and once acquired; proteorhodopsins could have ecological benefits for the organisms that possess them. These advantages are still to be experimentally shown in marine prokaryotes but can be identified in eukaryotes such as the alga, Acetabularia.

Oxygenic phototrophs rely on photophosphorylation to maintain photosynthetic carbon reduction, regulation of dark photoreactions, and elementary cell metabolism when nutrients are limited. However innovative photoheterotrophic strategies have been identified where ATP synthesis can be avoided and a proton –motive force is generated which can directly drive cell energetics, cell motility and importation of molecules in to a cell without producing oxygen. Photoheterotrophic strategies such as this could potentially give an organism an ecological advantage. The author implies that the heterotrophic strategies of marine prokaryotes, like cyanobacteria, could be as refined. Nevertheless, further investigation is needed.
The author advocates that photoheterotrophic prokaryotes may be able to regulate their uptake and use of solar energy. This is determined by the energetic demands of the metabolic processes of a cell. However further experimental evidence is needed.

The unknown complexity of oceanic photoheterotrophic prokaryotes could potentially influence carbon flow, and thus the application of current biogeochemical models. Energy could be channelled directly into cell metabolism, growth and nutrient acquisition by avoiding CO2 fixation because of a large, but unquantified, amount of solar energy being harvested by photoheterotrophic organisms. Due to this, element-based models may not be adequate. Models surrounding energy and protein flow are suggested as an alternative.