Dissimilatory Fe(III) and Mn(IV) Reduction

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Abstract

Dissimilatory Fe(III) and Mn(IV) reduction has an important influence on the geochemistry of modern environments, and Fe(III)-reducing microorganisms, most notably those in the Geobacteraceae family, can play an important role in the bioremediation of subsurface environments contaminated with organic or metal contaminants. Microorganisms with the capacity to conserve energy from Fe(III) and Mn(IV) reduction are phylogenetically dispersed throughout the Bacteria and Archaea. The ability to oxidize hydrogen with the reduction of Fe(III) is a highly conserved characteristic of hyperthermophilic microorganisms and one Fe(III)-reducing Archaea grows at the highest temperature yet recorded for any organism. Fe(III)- and Mn(IV)-reducing microorganisms have the ability to oxidize a wide variety of organic compounds, often completely to carbon dioxide. Typical alternative electron acceptors for Fe(III) reducers include oxygen, nitrate, U(VI) and electrodes. Unlike other commonly considered electron acceptors, Fe(III) and Mn(IV) oxides, the most prevalent form of Fe(III) and Mn(IV) in most environments, are insoluble. Thus, Fe(III)- and Mn(IV)-reducing microorganisms face the dilemma of how to transfer electrons derived from central metabolism onto an insoluble, extracellular electron acceptor. Although microbiological and geochemical evidence suggests that Fe(III) reduction may have been the first form of microbial respiration, the capacity for Fe(III) reduction appears to have evolved several times as phylogenetically distinct Fe(III) reducers have different mechanisms for Fe(III) reduction. Geobacter species, which are representative of the family of Fe(III) reducers that predominate in a wide diversity of sedimentary environments, require direct contact with Fe(III) oxides in order to reduce them. In contrast, Shewanella and Geothrix species produce chelators that solubilize Fe(III) and release electron-shuttling compounds that transfer electrons from the cell surface to the surface of Fe(III) oxides not in direct contact with the cells. Electron transfer from the inner membrane to the outer membrane in Geobacter and Shewanella species appears to involve an electron transport chain of inner-membrane, periplasmic, and outer-membrane c-type cytochromes, but the cytochromes involved in these processes in the two organisms are different. In addition, Geobacter species specifically express flagella and pili during growth on Fe(III) and Mn(IV) oxides and are chemotactic to Fe(II) and Mn(II), which may lead Geobacter species to the oxides under anoxic conditions. The physiological characteristics of Geobacter species appear to explain why they have consistently been found to be the predominant Fe(III)- and Mn(IV)-reducing microorganisms in a variety of sedimentary environments. In comparison with other respiratory processes, the study of Fe(III) and Mn(IV) reduction is in its infancy, but genome-enabled approaches are rapidly advancing our understanding of this environmentally significant physiology.

Section snippets

INTRODUCTION

Dissimilatory Fe(III) and Mn(IV) reduction refers to the process in which microorganisms reduce Fe(III) or Mn(IV) for purposes other than assimilation of iron or manganese. The ability of microorganisms to reduce Fe(III) or Mn(IV) has been known since early in the 20th century (Harder, 1919; Allison and Scarseth, 1942). However, the capacity for some microbes to conserve energy to support growth via the oxidation of hydrogen (Balashova and Zavarzin, 1980) or organic compounds (Lovley et al.,

Pristine Sediments, Soils, and Subsurface Environments

One of the primary reasons for investigating the physiology of any organism is to better understand its influence on the environments in which it is found and to gain insight into what environmental factors control its growth and activity. Microbial Fe(III) and Mn(IV) reduction are important processes in a diversity of anoxic environments in which organic matter and/or hydrogen as well as Fe(III) and Mn(IV) are available. For example, Fe(III) and Mn(IV) reduction are responsible for the

Microorganisms that Do Not Conserve Energy to Support Growth from Fe(III) Reduction

A wide phylogenetic diversity of microorganisms is known to reduce Fe(III) and Mn(IV) in a dissimilatory manner. Many of these microorganisms reduce Fe(III) as a minor side reaction in their metabolism but do not appear to conserve energy to support growth from this electron transfer (Lovley, 1987, 1991). Extensive lists of such microorganisms are available in previous reviews (Lovley, 1987, 2000b). Many of the initial concepts of the physiology of dissimilatory Fe(III) reduction, such as the

PHYSIOLOGICAL DIVERSITY

There are significant differences in the metabolic capabilities of dissimilatory Fe(III) reducers, which are important to consider in relating the physiology of these organisms to their function in the environment and in predicting the activity of Fe(III) reducers under various environmental conditions.

MECHANISMS FOR Fe(III) AND Mn(IV) REDUCTION

Unlike commonly considered electron acceptors such as oxygen, nitrate, sulfate, or carbon dioxide, Fe(III) and Mn(IV) are highly insoluble in most environments at circumneutral pH. Soluble electron acceptors can diffuse into cells in order to be reduced whereas Fe(III) and Mn(IV) reducers face the challenge of how to transfer electrons onto an insoluble, extracellular, electron acceptor. This is also a challenge for investigators of this process as working with insoluble electron acceptors

CONCLUSIONS

The current understanding of the physiology of dissimilatory Fe(III)- and Mn(IV)-reducing microorganisms suggests that some of these organisms are well adapted for survival and growth in a diversity of environments in which organic matter and/or hydrogen are available as electron donors where Fe(III) or Mn(IV) is present. In addition to playing an important role in the natural cycle of carbon and metals, Fe(III)- and Mn(IV)-reducing microorganisms appear to be useful tools for the

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