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THE LACTOBACILLUS ANOMALY: TOTAL IRON ABSTINENCE EUGENE D. WEINBERG * Cells of nearly all forms of life require iron. The metal provides electron transport proteins with a wide range of redox potentials. It is an integral component of oxygen carrier proteins and of the active centers of many enzymes, including ribonucleotide reductase, essential for DNA synthesis. However, the attributes of iron that provide metabolic usefulness also render the metal dangerous to manipulate and to store [I]. Accordingly, cells have developed extensive regulatory systems to ensure both the safe acquisition of well-defined amounts of iron and the avoidance of intracellular exposure to hazardous quantities [2, 3]. An alternative approach to eliminating the considerable problems involved in handling iron would be that of dispensing with any need for the metal. Thus it is not altogether surprising that members of a group ofgram positive bacteria, Lactobacillus sp. and a few closely related forms, have evolved to achieve complete indifference to iron. This essay focusses on three aspects of their iron-free existence: awareness, mechanisms, and ecological implications. Iron-Free Existence: Awareness Forms of life that depend on iron exist in environments that are quite diverse in both content and availability of the metal. Nevertheless, their iron requirement for growth in cell cultures is consistently uniform. The minimal non-limiting iron requirement is 0.4-4.0 µ? for plant cells, animal cells, and most bacterial cells [4]. In bacterial cultures that contain this This paper is dedicated to Professor Howard Gest, in recognition ofhis distinguished career in microbiology and in the history and philosophy of science. Support for this review was provided in part by the Office of Research and the University Graduate School, Indiana University , Bloomington, Indiana. *Department of Biology and Program in Medical Sciences, Indiana University, Bloomington , IN 47405.© 1997 by The University of Chicago. All rights reserved. 0031-5982/97/4003-1020$01.00 578 Eugene D. Weinberg ¦ Total Iron Abstinence amount of iron, a growth yield of 109 cells/ml could be expected; the dry wt of the cell mass would be approximately one mgm with an iron content of one micromole. However, early studies of mineral requirements of lactobacilli indicated that this group of bacteria could grow in the presence of little or no iron [5, 6] . At that time, it was not certain if lactobacilli were unusually adept at scavenging minute amounts of environmental iron or if, remarkably, they truly could live without the metal. That lactobacilli do, indeed, practice total iron abstinence became evident in subsequent investigations. In a well designed study of Lactobacillus plantarum, Archibald observed that when grown in medium containing 0.6µ? iron, the bacteria contained only 3.6 ±1.5 atoms of the metal per cell [7]. In contrast, an iron-dependent organism, Escherichia coli, when grown in medium of the same composition, contained 1.2 ± 0.2 X 105 atoms of iron per cell. In a later study, strains of several species of lactobacilli and of closely related bacteria were found to grow well in a culture medium that had no available iron [8]. A third laboratory, in a thorough examination of 23 strains (in 19 species) of lactobacilli and related bacteria, observed that growth was identical in both iron-lacking or iron-supplemented media incubated under either aerobic or microaerophilic conditions [9]. Moreover, none of the organisms produced siderophores. Additionally, cells of the 23 strains grown in the presence of 59Fe failed to incorporate the isotope, whereas cells of iron-dependent pseudomonads acquired nearly all of the labelled metal. Paradoxically, a recent study reported that a strain each of Lactobacillus plantarum ?t?a of L. acidophilus could accumulate iron [10]. Oddly, the authors failed to suggest reasons for their singular findings, nor did they cite any of the previously published evidence that authentic lactobacilli are unable to acquire iron. Iron-Free Existence: Mechanisms Prior to the recognition that lactobacilli incorporate no iron, several studies had observed that these bacteria employ unique co-factors in various enzymes. Examples include a cobalt-cofactored ribonucleotide reductase , a manganese-cofactored DNA-dependent RNA polymerase, and a nonheme mangano-catalase [11-13]. Moreover, many strains of lactobacilli produce no catalase and most also are negative for...

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