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Adv Microb Physiol. 2011;58:141-73. doi: 10.1016/B978-0-12-381043-4.00004-0.

Singlet oxygen stress in microorganisms.

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1
Institut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Giessen, Giessen, Germany.

Abstract

Singlet oxygen is the primary agent of photooxidative stress in microorganisms. In photosynthetic microorganisms, sensitized generation by pigments of the photosystems is the main source of singlet oxygen and, in nonphotosynthetic microorganisms, cellular cofactors such as flavins, rhodopsins, quinones, and porphyrins serve as photosensitizer. Singlet oxygen rapidly reacts with a wide range of cellular macromolecules including proteins, lipids, DNA, and RNA, and thereby further reactive substances including organic peroxides and sulfoxides are formed. Microorganisms that face high light intensities or exhibit potent photosensitizers have evolved specific mechanisms to prevent photooxidative stress. These mechanisms include the use of quenchers, such as carotenoids, which interact either with excited photosensitizer molecules or singlet oxygen itself to prevent damage of cellular molecules. Scavengers like glutathione react with singlet oxygen. Despite those protection mechanisms, damage by reactions with singlet oxygen on cellular macromolecules disturbs cellular functions. Microorganisms that regularly face photooxidative stress have evolved specific systems to sense singlet oxygen and tightly control the removal of singlet oxygen reaction products. Responses to photooxidative stress have been investigated in a range of photosynthetic and nonphotosynthetic microorganisms. However, detailed knowledge on the regulation of this response has only been obtained for the phototrophic alpha-proteobacterium Rhodobacter sphaeroides. In this organism and in related proteobacteria, the extracytoplasmic function (ECF) sigma factor RpoE is released from the cognate antisigma factor ChrR in the presence of singlet oxygen and triggers the expression of genes providing protection against photooxidative stress. Recent experiments show that singlet oxygen acts as a signal, which is sensed by yet unknown components and leads to proteolysis of ChrR. RpoE induces expression of a second alternative sigma factor, RpoH(II), which controls a large set of genes that partially overlaps with the heat-shock response controlled by RpoH(I). In addition to the transcriptional control of gene regulation by alternative sigma factors, a set of noncoding small RNAs (sRNAs) appear to affect the synthesis of several proteins involved in the response to photooxidative stress. The interaction of mRNA targets with those sRNAs is usually mediated by the RNA chaperone Hfq. Deletion of the gene encoding Hfq leads to a singlet oxygen-sensitive phenotype, which underlines the control of gene regulation on the posttranscriptional level by sRNAs in R. sphaeroides. Hence, a complex network of different regulatory components controls the defense against photooxidative stress in anoxygenic photosynthetic bacteria.

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