Chapter 34 : Sporulation Genes and Intercompartmental Regulation

Three principal stages of sporulation. At the predivisional stage, the developing cell has entered sporulation and is completing chromosome duplication but has not yet undergone asymmetric division. In the postdivisional stage, there has been an unequal division into a small cell, the forespore (or prespore), and a large cell, the mother cell. The forespore and mother cell each receive a chromosome during the postdivisional stage, and each remains in contact with the extracellular medium. Finally, in the postengulfment stage, the forespore is wholly engulfed as a free protoplast within the mother cell.

Principal targets of Spo0A∼P in the establishment of compartment-specific gene expression. The transcription factor Spo0A∼P is responsible for directing the transcription of genes involved in establishing compartment-specific transcription under the control of σF (the spoIIA operon and the spoIIE gene) and σΕ (the spoIIG operon) and of an unknown gene or genes involved in switching the site of Z-ring formation to sites near the cell poles.

Cyclic pathway governing the activation of σF. The figure shows the relationship between σF and the regulatory proteins SpoIIAA (AA), SpoIIAB (AB), and SpoIIE (E). SpoIIAA exists in two states, phosphorylated (AA-P) and unphosphorylated (AA). Likewise, SpoIIAB exists in two forms, an ATP-containing form [(ATP)AB] and an ADP-containing form [(ADP)AB]. The activation of σF is depicted as a cycle in which SpoIIAA becomes phosphorylated by reaction with the ATP-containing complex of SpoIIAB and σF [(ΑΤΡ)ΑΒ·σF] and dephosphorylated by the action of the SpoIIE phosphatase. SpoIIAA is also capable of becoming trapped in an inactive complex [(ADP)AB-AA] with the ADP-containing form of SpoIIAB [(ADP)AB]. Evidence indicates the existence of an additional, unknown regulatory step (not shown in the figure, but see text for details) acting after the dephosphorylation of SpoIIAA-P that is required for the activation of σF.

The σF factor escapes from SpoIIAB in the forespore. The σF factor is held in an inactive complex with SpoIIAB (ΑΒ·σF) in the predivisional cell and in the mother-cell chamber following division. The σF factor escapes from SpoIIAB in the forespore in a process that is accompanied by the dephosphorylation of SpoIIAA-P (AA-P) and the binding of AB to the unphosphorylated form of SpoIIAA (AA) to form the SpoIIAB-SpoIIAA complex (AB-AA). For simplicity, the presence of ATP or ADP in the SpoIIAB complexes is not shown. Also, for simplicity, SpoIIAA is only shown in its phos-phorylated state in the predivisional cell, although, as explained in the text, some dephosphorylation of SpoIIAA-P probably commences prior to asymmetric division. Dephosphorylation of SpoIIAA-P is catalyzed by the phosphatase SpoIIE (E), which localizes in bipolar Ε-rings in the predivisional cell and in the septum following division. It is not definitively known whether SpoIIE is localized on one (the forespore) or both faces of the polar septum, and the figure is not intended to favor one or the other possibility.

Intercompartmental signal transduction pathways governing the proteolytic activation of pro-σE and pro-σκ. In the pro-σE pathway, σF turns on the synthesis of the signaling protein SpoIIR, which is secreted into the space between the two cellular compartments where it directly or indirectly activates SpoIIGA (GA), an integral membrane protein that is responsible for converting pro-σE to mature σΕ. In the pro-σK pathway, σG turns on the synthesis of the signaling protein SpoIVB, which is believed to be secreted into the space between the two cellular compartments where it reverses the inhibition of the pro-σK processing enzyme SpoIVFB (IVFB) by the inhibitory proteins SpoIVFA (IVFA) and BofA. SpoIVFB, SpoIVFA, and BofA are integral membrane proteins. A fundamental difference between the pathways is that SpoIIGA is inactive in its default state and needs to be activated by SpoIIR, whereas SpoIVFB is active in its default state and is held inactive by SpoIVFA and BofA.

Crisscross regulation. The activities of the four compartment-specific sigma factors are linked in a crisscross fashion by intercompartmental signaling. Events (arrow) under the control of the transcription factors Spo0A∼P and σΗ lead to the activation of σF in the forespore. Next, an intercellular signal transduction pathway (horizontal arrow) under the control of σΕ causes the appearance of σΕ in the mother cell by proteolytic processing of the proprotein precursor pro-σE (not shown). The σΕ factor, in turn, acting by an unknown intercellular pathway (diagonal arrow), triggers the appearance σG in the forespore compartment after engulfment. Finally, an intercellular signal transduction pathway (horizontal arrow) under the control of σG causes the appearance of σκ in the mother cell by proteolytic processing of the proprotein precursor pro-σK (not shown).