Abstract
Although sulfite, a by-product of the degradation of many sulfur compounds, is highly reactive and can cause damage to DNA, proteins and lipids, comparatively little is known about the regulation of sulfite-oxidizing enzyme (SOEs) expression. Here we have investigated the regulation of SOE-encoding genes in two species of α-Proteobacteria, Sinorhizobium meliloti and Starkeya novella, that degrade organo- and inorganic sulfur compounds, respectively, and contain unrelated types of SOEs that show different expression patterns. Our work revealed that in both cases, the molecular signal that triggers SOE gene expression is sulfite, and strong up-regulation depends on the presence of a sulfite-responsive, cognate Extracytoplasmic function (ECF) sigma factor, making sulfite oxidation a bacterial stress response. An additional RpoE1-like ECF sigma factor was also involved in the regulation, but was activated by different molecular signals, taurine (Sm) and tetrathionate (Sn), respectively, targeted different gene promoters, and also differed in the magnitude of the response generated. We therefore propose that RpoE1 is a secondary, species-specific regulator of SOE gene expression rather than a general, conserved regulatory circuit. Sulfite produced by major dissimilatory processes appeared to be the trigger for SOE gene expression in both species, as we were unable to find evidence for an increase of SOE activity in stationary growth phase. The basic regulation of bacterial sulfite oxidation by cognate ECF sigma factors is likely to be applicable to three groups of alpha and beta-Proteobacteria in which we identified similar SOE operon structures.
Highlights
Sulfite is a highly reactive sulfur oxyanion that occurs in both pro- and eukaryotes as a by-product of sulfur compound degradation or external exposure to sulfite (Kappler and Enemark, 2015; Kappler and Schwarz, 2016)
Sulfite oxidation is an essential process in all bacteria that degrade sulfur compounds as either carbon or energy sources, and here we have shown that despite clearly differing types of sulfur metabolism, the presence of structurally distinct sulfite-oxidizing enzymes (SOEs) and differing patterns of SOE basal regulation, the basic mechanism of SOE regulation is conserved between two different species of soil bacteria, Sm. meliloti and St. novella (Kappler and Bailey, 2005; Mcgrath et al, 2015)
In both species induction of SOE gene expression is triggered by sulfite, and depends mostly on the respective, cognate Extracytoplasmic function (ECF) sigma factor
Summary
Sulfite is a highly reactive sulfur oxyanion that occurs in both pro- and eukaryotes as a by-product of sulfur compound degradation or external exposure to sulfite (Kappler and Enemark, 2015; Kappler and Schwarz, 2016). Free sulfite can damage proteins, DNA and lipids through formation of adducts, and sulfite-oxidizing enzymes (SOEs) are found in most forms of life (Zhang et al, 2011; Kappler and Enemark, 2015; Kappler and Schwarz, 2016). While in some bacteria such as Deinococcus radiodurans SOE genes appear to be always highly expressed (D’errico et al, 2006), in many bacteria SOEs have complex regulatory patterns where upregulation usually occurs in the presence of metabolizable sulfur substrates, but activity may undergo growth phase dependent induction and show varying levels of basal expression in different bacterial strains and species (Kappler et al, 2000, 2001; Wilson and Kappler, 2009; Bastiat et al, 2012)
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