Electron flow and biofilms
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ectron flow in biological systems We begin this discussion of biofilms with a simple axiom: “Electrons must flow.” While there are a few notable exceptions to this statement, it remains a general rule of life that electron flow must occur in order for chemo-osmotic gradients to be established and adenosine triphosphate synthesized as the energy in such gradients is harvested.1,2 Such is true for the mitochondria in virtually all eukaryotic cells (e.g., fungi, animal cells, and plant cells), as well as for both domains of prokaryotic cells, the bacteria, and the archaea, which lack a nucleus or organelles such as mitochondria. When electron flow stops, most eukaryotes rapidly die, while many bacteria and archaea can be more robust but eventually suffer a similar fate. This seemingly simple tenet has a major implication for microbial ecology: if redox energy is available in a natural system, and if the natural rate of electron flow is not too rapid, then it is a niche that will probably be exploited by a redox-active microbe. Eukaryotic cells are, as a rule, capable of utilizing only oxygen as an electron acceptor and only organic carbon as an electron donor, while prokaryotic cells (the bacteria and archaea) are often able to utilize other electron donors (e.g., inorganic molecules such as hydrogen) and/or other electron acceptors (e.g., inorganic molecules such as sulfates and nitrates). The range of electron donors available to living microbial systems is shown
in Figure 1. Such a view of life’s reactions3 allows one to see the energy available for the creation of membrane gradients and relate the metabolic opportunities to environmental chemistry and geology. However, it is a misconception that bacteria and archaea are metabolically diverse as individual species. In fact, in order to accomplish what they do, they often become very highly specialized (e.g., methanotrophs often are restricted to growth on methane or methanol). Thus, it is the community of prokaryotes that is diverse, populated by individual, specialist species that are working together. For many years, it was accepted that electron acceptors had to be soluble, whether they are inorganics such as oxygen, nitrate, sulfate, or carbon dioxide, or organics such as dimethyl sulfoxide (DMSO), trimethylamine N-oxide (TMAO), or fumarate. These electron acceptors are very well documented in the literature, and reduction is commonly done on the inner membrane, where specific enzymes are found that catalyze substrate reduction.4 Of notable exception were the solid metal oxides such as Fe(III) oxides and Mn(IV) oxides, a variety of which exist in abundance in various environments. As shown in Figure 1, both Fe(III) and Mn(IV) have good potentials, with Fe(III) yielding more energy than sulfate, and Mn(IV) yielding energy at approximately the level of nitrate. Yet the biological reduction of these compounds as electron acceptors
Kenneth H. Nealson, University of Southern California, Los Angeles, CA 90089-0740, USA; [email protected] Steven E. Finkel, University of Sout
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