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Chapter 11 : Global Responses of Bacteria to Oxygen Deprivation

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Abstract:

This chapter highlights some of the advances on both the molecular mechanisms of oxygen (O) sensing and the biological responses to O limitation. In the first part of the chapter, the major regulators that control expression of anaerobic respiratory pathways are described, with focus on the well studied examples from K-12. Many facultative bacteria have anaerobic lifestyles that depend on pathways not found in enteric bacteria. A section reviews the master regulators of these anaerobic lifestyles, describing how their activity responds to O deprivation, highlighting commonalities and differences to the responses described for enterobacteria, and placing them into a metabolic context of the systems they control. A recurring theme in the review is that multiple transcription factors collaborate in a given organism to control gene expression in response to changes in O. In , decreased expression of the genes encoding aerobic respiratory functions under anaerobic growth conditions is largely mediated by the aerobic respiration control (Arc) A and ArcB two-component system. Regulation of anaerobic respiration in the γ-proteobacterium has attracted great interest because of the broad diversity of electron acceptors (>14) that these bacteria can respire, including metal oxides. The use of cofactors such as flavins, heme, and [Fe-S] clusters generally sense O directly, using chemistry reflecting their well-described roles in biological reactions.

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11

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Gene Expression and Regulation
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Bacterial Proteins
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Gene Expression
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Cellular Processes
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Anaerobic Respiration
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Figures

Image of Figure 1.
Figure 1.

Distribution of genes regulated by FNR in K-12. The percentage of genes belonging to relevant functional groups, whose expression changed in response to FNR as determined in the genome-wide transcription studies of Kang et al. ( ), are indicated.

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11
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Image of Figure 2.
Figure 2.

Cellular levels of FNR are calibrated to efficiently respond to O Regulation of FNR activity and synthesis under anaerobic (top panel) and aerobic (bottom panel) growth conditions (Mettert et al., ). The Isc pathway inserts [Fe-S] clusters into FNR under both aerobic and anaerobic conditions but the active [4Fe-4S]-FNR form accumulates only under anaerobic conditions because of the O instability of the [4Fe-4S] cluster. O promotes the degradation of the [4Fe-4S] cluster to the [2Fe-2S] cluster and superoxide promotes the loss of the [2Fe-2S] cluster to apoFNR. In addition, negative autoregulation of transcription occurs under anaerobic conditions, whereas a portion of FNR is degraded via the ClpXP protease under aerobic conditions.

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11
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Image of Figure 3.
Figure 3.

Regulation of ArcB by quinones. During aerobic respiration in , electrons flow from donors to produce reduced ubiquinone (UQH), which is then used to reduce O to HO via cytochrome oxidase (C.O.), generating a higher ratio of UQ to UQH. As previously proposed (Malpica et al., ), the excess UQ under aerobic conditions oxidizes the cytosolic thiols of ArcB Cys 180 and 241 to form intermolecular disulfide bonds, inactivating the ArcB kinase activity, which uses its cytosolic domain for a His-Asp-His phosphorelay. The model also predicts that, in the absence of an electron acceptor, UQ levels are too low to maintain this disulfide bond in dimeric ArcB. The question mark denotes that it is not known how the disulfide bond is reduced back to the thiol state. This figure is adapted from Malpica et al. ( ).

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11
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Tables

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Table 1.

Global transcriptional regulators of bacterial responses to O deprivation

Citation: Kiley P, Donohue T. 2011. Global Responses of Bacteria to Oxygen Deprivation, p 175-189. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch11

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