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Primary and Secondary Oxidative Stress in Bacillusemi 2433 1387..1394 Provided by Wageningen University & Research Publications Environmental Microbiology (2011) 13(6), 1387–1394 doi:10.1111/j.1462-2920.2011.02433.x Minireview View metadata, citation and similar papers at core.ac.uk brought to you by CORE Primary and secondary oxidative stress in Bacillusemi_2433 1387..1394 provided by Wageningen University & Research Publications Maarten Mols*† and Tjakko Abee organism for Gram-positive bacteria and besides being a Laboratory of Food Microbiology, Wageningen major food spoilage organism, it is used in food fermen- University, Wageningen, the Netherlands. tations (Murooka and Yamshita, 2008) and as a probiotic (Sorokulova et al., 2008). Bacillus cereus is a notorious food-borne pathogen that causes two distinct types of Summary diseases: emesis and diarrhoea (Stenfors Arnesen et al., Coping with oxidative stress originating from oxidiz- 2008). Bacillus thuringiensis is widely applied as biopes- ing compounds or reactive oxygen species (ROS), ticide and it is also known to cause various human dis- associated with the exposure to agents that cause eases (Ghelardi et al., 2007). Bacillus anthracis is well environmental stresses, is one of the prerequisites known, because it causes the mammalian and human for an aerobic lifestyle of Bacillus spp. such as B. disease anthrax that can be present in three clinical subtilis, B. cereus and B. anthracis. This minireview forms: cutaneous, pulmonary and gastrointestinal (Kolsto highlights novel insights in the primary oxidative et al., 2009). stress response caused by oxidizing compounds Bacillus spp. may encounter oxidative agents and con- including hydrogen peroxide and the secondary oxi- ditions in a range of settings. To prevent spoilage and dative stress responses apparent upon exposure to a (re)contamination of food by Bacillus spp., food- range of agents and conditions leading to environ- processing equipment is regularly cleaned and disinfected mental stresses such as antibiotics, heat and acid. with oxidative compounds such as hydrogen peroxide and Insights in the pathways and damaging radicals sodium hypochlorite (Block, 2000). Furthermore, B. involved have been compiled based among others on anthracis encounters oxidizing compounds, including - transcriptome studies, network analyses and fluores- superoxide (O2 ), hydrogen peroxide and nitric oxide (NO), cence techniques for detection of ROS at single cell upon germination and growth inside macrophages (Mac- level. Exploitation of the current knowledge for the Micking et al., 1997; Fang, 2004; Shatalin et al., 2008). control of spoilage and pathogenic bacteria is Bacillus spp. that encounter oxidizing conditions react by discussed. inducing an oxidative stress response, including upregu- lation of catalases and thioredoxins. The response of Bacillus spp. to oxidative agents such as hydrogen perox- Introduction ide, hypochlorite, paraquat, diamide and peracetic acid is The genus Bacillus, belonging to the phylum Firmicutes, addressed in this minireview as the primary oxidative comprises a diverse group of Gram-positive and Gram- stress response. In addition, it has been noted that expo- variable bacteria. Bacillus spp. are rod-shaped aerobic sure to heat, acid and high salt concentrations, which are or facultative anaerobic organisms that can form also widely used to prevent food spoilage and contamina- endospores. Vegetative cells and spores of Bacillus spp. tion by bacteria including Bacillus spp., also cause an can be isolated from a wide range of environments (Claus oxidative stress response. This so-called secondary oxi- and Berkeley, 1986). The most well-known and best- dative stress response is activated when bacterial cells studied members of the Bacillus genus are Bacillus sub- are exposed to harsh, unfavourable conditions while the tilis, Bacillus cereus, Bacillus thuringiensis and Bacillus cells are still actively respiring. Recent studies showed the anthracis. Bacillus subtilis is widely used as model impact of secondary oxidative stresses and that it was suggested to act as a general mechanism in cellular death when bacteria are exposed to toxic agents and conditions Received 15 October, 2010; accepted 6 January, 2011. *For such as bactericidal antibiotics, heat and acid (Kohanski correspondence. E-mail [email protected]; Tel. (+31) 50 3632107; et al., 2007; Mols et al., 2009; 2010). Fax (+31) 50 3632348. †Present address: Department of Molecular Genetics, University of Groningen, Groningen Biomolecular Sciences The aim of this minireview is to provide an overview in and Biotechnology Institute, Groningen, the Netherlands. the responses of Bacillus spp. to primary and secondary © 2011 Society for Applied Microbiology and Blackwell Publishing Ltd 1388 M. Mols and T. Abee oxidative stress and to give insight in the differences upon peroxide stress while in B. cereus this was not the between these primary and secondary oxidative stress case (Ceragioli et al., 2010). responses observed in recent studies. Furthermore, the The putative functions of the induced genes suggest importance and implications for the secondary oxidative that exposure to hydrogen peroxide leads to protein and stress responses in the general stress response and DNA damage. The reaction of hydrogen peroxide with mechanisms of cellular death are discussed. thiol and methionine residues of proteins, concomitantly leading to damage, has been verified by measuring oxidation of sulfhydryl groups (Ceragioli et al., 2010). Primary oxidative stress responses Additionally, hydrogen peroxide may cause damage to proteins harbouring iron–sulfur clusters leading to The response of Bacillus spp. upon exposure to chemi- elevated levels of free iron that can bind adventitiously to cals that are oxidizing and used or studied because of proteins. Free iron also initiates the generation of highly their oxidizing chemical properties is briefly discussed reactive hydroxyl radicals (OH·) in the Fenton reaction. below. For a more detailed overview in the different oxi- Consequently, OH· oxidizes biomolecules including dative stimulons we recommend recent reviews by Zuber lipids, DNA and proteins (Imlay, 2008; Zuber, 2009). (2009), Duarte and Latour (2010), Faulkner and Helmann Damage to DNA was experimentally verified by estab- (2011) and Antelmann and Helmann (2011). lishing mutation rates in hydrogen peroxide treated and untreated B. cereus cells, showing that exposed cells demonstrated higher mutation rates (Ceragioli et al., Response of Bacillus to hydrogen peroxide 2010). In contrast, no indications were found for lipid Hydrogen peroxide is often used as a model chemical for peroxidation and staining with propidium iodide (a fluo- experiments designed to study oxidative stresses. It is rescent probe that enters cells through compromised inevitably formed as a by-product of oxidative phosphory- membranes) did not show damage to the cell mem- lation and other reactions. The antimicrobial properties of branes in the conditions tested. Even more unexpected hydrogen peroxide provide a first line of defence against was the lack of free radicals upon exposure to primary invading microbes along wound sites in plants and in oxidative stress, while these are observed after exposure mammal macrophages. Furthermore, it is used in house- to heat and acid stress. Primary oxidative stress may holds and industries as bleaching agent and antibacterial lead to OH· formation; however, the threshold needed for disinfectant. detection may not be reached in these experiments as Upon exposure of B. cereus to mild and lethal hydrogen OH· formation may be low from autolysis of hydrogen peroxide concentrations the expression of numerous peroxide (Mohan et al., 2009; Ikai et al., 2010). Further- genes was affected (Ceragioli et al., 2010), including more, differences in (threshold) levels of free radicals genes involved in the common response to general resulting from primary and secondary oxidative stresses. For example, genes involved in protein protec- responses may originate from the localized formation tion, refolding and turnover including groES, dnaK and clp and inflicted damage of for example OH· (Imlay, 2003; proteases were upregulated. The exposure to hydrogen Mohan et al., 2009). peroxide leads to the induction of oxidative stress- associated genes and mechanisms. Genes encoding Response to other oxidative agents catalases, thioredoxin reductases and peroxidases were induced to remove hydrogen peroxide from the cells or Besides hydrogen peroxide other chemicals, such as per- extracellular environment. The involvement of iron and acetic acid and sodium hypochlorite, are also used for manganese in the response of B. cereus to hydrogen their oxidative properties to clean and disinfect food- peroxide was indicated by the induction of perR and iron contacting surfaces. Exposure of B. cereus to peracetic and manganese uptake systems. Imbalance in iron acid showed similar responses as observed for hydrogen homeostasis has also been reported for B. subtilis (Zuber, peroxide (Ceragioli et al., 2010). The nature of peracetic 2009) and manganese may provide protection against acid, i.e. being a mixture of hydrogen peroxide and acetic hydrogen peroxide (Inaoka et al., 1999). The SOS acid, is perhaps the reason for the large overlap between response, which is activated when DNA is damaged, and the responses to hydrogen peroxide and peracetic acid other DNA repair and protection mechanisms were exposures. Sodium hypochlorite treatments led to the induced upon exposure to hydrogen peroxide. Bacillus induction of genes involved
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