Abstract

During aerobic respiratory growth, Bacillus cereus is exposed to continuously reactive oxidant, produced by partially reduced forms of molecular oxygen, known as reactive oxygen species (ROS). The sulfur-containing amino acid, methionine (Met), is particularly susceptible to ROS. The major oxidation products, methionine sulfoxides, can be readily repaired by methionine sulfoxide reductases, which reduce methionine sulfoxides [Met(O)] back to methionine. Here, we show that methionine sulfoxide reductase AB (MsrAB) regulates the Met(O) content of both the cellular proteome and exoproteome of B. cereus in a growth phase-dependent manner. Disruption of msrAB leads to metabolism changes resulting in enhanced export of Met(O) proteins at the late exponential growth phase and enhanced degradation of exoproteins. This suggests that B. cereus can modulate its capacity and specificity for protein export/secretion through the growth phase-dependent expression of msrAB. Our results also show that cytoplasmic MsrAB recycles Met residues in enterotoxins, which are major virulence factors in B. cereus.

Highlights

  • Reactive oxygen species (ROS) are by-products of aerobic metabolism, and respiration is considered to be the major intracellular source of ROS production in bacteria (Brynildsen et al, 2013; Imlay, 2013)

  • It has been shown that Met-S-(O) reductase (MsrA) reduces both oxidized proteins and low molecular weight Met(O)-containing compounds with a similar catalytic efficiency, whereas MsrB is specialized for the reduction of Met(O) in proteins

  • Four different types of organization have been reported for msrA and msrB: (i) msrA and msrB genes are two separate transcription units, (ii) msrA and msrB cistrons are organized as an operon, (iii) msrA and msrB cistrons form a single open reading frame (ORF) to produce a two domain protein, and (iv) trx, msrA, and msrB cistrons form a single ORF to produce a three domain protein (Drazic and Winter, 2014)

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Summary

INTRODUCTION

Reactive oxygen species (ROS) are by-products of aerobic metabolism, and respiration is considered to be the major intracellular source of ROS production in bacteria (Brynildsen et al, 2013; Imlay, 2013). It has been shown that MsrA reduces both oxidized proteins and low molecular weight Met(O)-containing compounds with a similar catalytic efficiency, whereas MsrB is specialized for the reduction of Met(O) in proteins. Both Msr types preferentially repair unfolded proteins (Tarrago et al, 2012). B. cereus is a Gram-positive, motile human pathogen that is well-equipped to survive in various environments such as those encountered in soil, food and the human gastrointestinal tract (Stenfors Arnesen et al, 2008) These bacteria can grow in the presence or absence of oxygen (Rosenfeld et al, 2005; Duport et al, 2006). Our results provide evidence that Met residues in exoproteins, especially enterotoxins, and their recycling by MsrAB, can serve as an antioxidant system that could trap ROS and maintain redox homeostasis in cells

MATERIALS AND METHODS
Analytical Procedures and Growth Parameters
RESULTS
DISCUSSION
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