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Widespread Production of Extracellular Superoxide by Heterotrophic Bacteria

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Science  07 Jun 2013:
Vol. 340, Issue 6137, pp. 1223-1226
DOI: 10.1126/science.1237331

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Sending Out an ROS

The global imprint of biological activity in aquatic environments is often considered a consequence of enzyme-mediated redox reactions that support metabolic activity, such as reducing oxygen during respiration. But some organisms also release redox-active reactive oxygen species (ROS) into the environment—to acquire trace metals or to prevent viral infections—which can influence global processes like nutrient availability and contaminant transport. Photosynthetic organisms like phytoplankton are thought to be the primary biological source of ROS in freshwater and marine environments. However, Diaz et al. (p. 1223, published online 2 May; see the Perspective by Shaked and Rose) now show that a broad range of ecologically and phylogenetically diverse heterotrophic bacteria also produce large quantities of superoxide. Production rates vary widely across 30 common bacterial isolates but in some cases were greater than production rates of phytoplankton. Because these bacteria do not require light to grow, they may be the dominant source of ROS in dark environments like the deep ocean, terrestrial soils, or lake sediments.

Abstract

Superoxide and other reactive oxygen species (ROS) originate from several natural sources and profoundly influence numerous elemental cycles, including carbon and trace metals. In the deep ocean, the permanent absence of light precludes currently known ROS sources, yet ROS production mysteriously occurs. Here, we show that taxonomically and ecologically diverse heterotrophic bacteria from aquatic and terrestrial environments are a vast, unrecognized, and light-independent source of superoxide, and perhaps other ROS derived from superoxide. Superoxide production by a model bacterium within the ubiquitous Roseobacter clade involves an extracellular oxidoreductase that is stimulated by the reduced form of nicotinamide adenine dinucleotide (NADH), suggesting a surprising homology with eukaryotic organisms. The consequences of ROS cycling in immense aphotic zones representing key sites of nutrient regeneration and carbon export must now be considered, including potential control of carbon remineralization and metal bioavailability.

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