Evolution and diversification of Group 1 [NiFe] hydrogenases. Is there a phylogenetic marker for O2-tolerance?

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Abstract

Group 1 hydrogenases are periplasmic enzymes and are thus strongly affected by the outside world the cell experiences. This exposure has brought about an extensive heterogeneity in their cofactors and redox partners. Whereas in their majority they are very O2-sensitive, several enzymes of this group have been recently reported to be O2-tolerant. Structural and biochemical studies have shown that this O2-tolerance is conferred by the presence of an unusual iron-sulfur cofactor with supernumerary cysteine ligation (6 instead of 4 Cys, hence called '6C cluster'). This atypical cluster coordination affords redox plasticity (i.e. two-redox transitions), unprecedented for this type of cofactors and likely involved in resistance to O2. Genomic screening and phylogenetic tree reconstruction revealed that 6C hydrogenases form a monophyletic clade and are unexpectedly widespread among bacteria. However, several other well-defined clades are observed, which indicate early diversification of the enzyme into different subfamilies. The various idiosyncrasies thereof are shown to comply with a very simple rule: phylogenetic grouping of hydrogenases directly correlates with their specific functions and hence biochemical characteristics. The observed variability results from gene duplication, gene shuffling and subsequent adaptation of the diversified enzymes to specific environments. An important factor for this diversification seems to have been the emergence of molecular oxygen. Hydrogenases appear to have dealt with oxidative stress in various ways, the most successful of which, however, was the innovation of the 6C-cluster conferring pronounced O2-tolerance to the parent enzymes. © 2012 Elsevier Ltd. All rights reserved.

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Pandelia, M. E., Lubitz, W., & Nitschke, W. (2012). Evolution and diversification of Group 1 [NiFe] hydrogenases. Is there a phylogenetic marker for O2-tolerance? Biochimica et Biophysica Acta - Bioenergetics, 1817(9), 1565–1575. https://doi.org/10.1016/j.bbabio.2012.04.012

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