Dissimilatory metal reduction: from early life to bioremediation

Abstract

I t is well known that metals, and iron in particular, are key components of proteins involved in transferring electrons to terminal acceptors such as oxygen and sulfate. However, it has only recently been recognized that metals can serve as terminal electron acceptors to support the anaerobic growth of microorganisms. Here again, iron is the most important metal, reflecting the considerable abundance of insoluble Fe(III) oxides in the Earth's crust, but other metals and metalloids such as manganese, uranium, chromium, technetium, cobalt, selenium, and arsenic can also serve as electron acceptors. Microbial reduction of Fe(III) and the oxidized forms of other metals influences not only the biogeochemical cycles of these metals, but also the fate of organic matter and nutrients in a variety of environments. The use of metals as terminal electron acceptors is called "dissimilatory metal reduction," distinguishing it from the reduction of metals associated with metal uptake into cells. A phylogenetically diverse group of bacteria (Fig. 1) and archaea are known to conserve energy to support growth by oxidizing hydrogen or organic compounds with the reduction of Fe(III), and novel Fe(III)-reducing microorganisms are continually being discovered. However, not all dissimilatory metal reduction is linked to energy conservation. For example, our studies demonstrate that sulfate-reducing and methanogenic microorganisms oxidize hydrogen with the reduction of Fe(III). Although these microorganisms do not appear capable of growing with Fe(III) serving as the sole terminal electron acceptor, they may preferentially reduce Fe(III) over sulfate or carbon dioxide. Dissimilatory metal reduction is relevant to many issues, ranging from the beginnings of life on Earth to environmental remediation, but the study ofthis process is in its infancy. Of all of the major forms of anaerobic respiration, it has received the least attention. However, this field seems poised to develop rapidly, particularly as the Department of Energy and the National Science Foundation are now supporting numerous research groups that are investigating both geochemical and biochemical aspects of dissimilatory metal reduction.

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