Evaluating microbial chemical choices: the ocean chemistry basis for the competition between use of O2 or NO3 as an electron acceptor

Abstract

The traditional ocean chemical explanation for the emergence of suboxia is that once O2 levels decline to about 10 micromoles/kg then onset of NO3 reduction occurs. This piece of ocean chemical lore is well founded in observations and is typically phrased as a microbial choice and not as an obligate requirement. The argument based on O2 levels alone could also be phrased as being dependent on an equivalent amount of NO3 that would yield the same energy gain. This description is based on the availability of the electron acceptor: but the oxidation reactions are usually written out as free energy yield per mole of organic matter, thus not addressing the oxidant availability constraint invoked by ocean scientists. Here we show that the argument can be phrased simply as competing rate processes dependent on the free energy yield ratio per amount of electron acceptor obtained, and thus the [NO3]:[O2] ratio is the critical variable. The rate at which a microbe can acquire either O2 or NO3 to carry out the oxidation reactions is dependent on both the concentration in the bulk ocean, and on the diffusivity within the microbial external molecular boundary layer. From the free energy yield calculations combined with the ~25% greater diffusivity of the O2 molecule we find that the equivalent energy yield occurs at a ratio of about 3.8 NO3:O2 for a typical Redfield ratio reaction, consistent with an ocean where NO3 reduction onset occurs at about 10 μmol O2: 40 μmol NO3, and the reactions then proceed in parallel along a line of this slope until the next energy barrier is approached. Within highly localized microbial consortia intensely reducing pockets may occur in a bulk ocean containing finite low O2 levels; and the local flux of reduced species from strongly reducing shelf sediments will perturb the large scale water column relationship. But all localized reactions drive towards maximal energy gain from their immediate diffusive surroundings, thus the ocean macroscopic chemical fields quite well approximate the net efficiency and operational mode of the ensemble microbial engine.