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A Channel Connecting the Mother Cell and Forespore During Bacterial Endospore Formation

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A Channel Connecting the Mother Cell and Forespore During Bacterial Endospore Formation A channel connecting the mother cell and forespore during bacterial endospore formation Jeffrey Meisner*†, Xin Wang*†‡, Monica Serrano§, Adriano O. Henriques§, and Charles P. Moran, Jr.*¶ *Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322; and §Instituto de Tecnologia Química e Biolo´gica, Universidade Nova de Lisboa, Avenida da Repu´blica, Apartado 127, 2781-901 Oeiras Codex, Portugal Edited by Thomas J. Silhavy, Princeton University, Princeton, NJ, and approved August 1, 2008 (received for review July 1, 2008) At an early stage during Bacillus subtilis endospore development activation of ␴G. The spoIIIA locus is expressed under the control the bacterium divides asymmetrically to produce two daughter of ␴E in the mother cell. With the exception of spoIIIAA, each cells. The smaller cell (forespore) differentiates into the endospore, of the spoIIIA genes (spoIIIAB–AH) encodes a predicted integral while the larger cell (mother cell) becomes a terminally differen- membrane protein. SpoIIIAH contains an N-terminal trans- tiated cell that nurtures the developing forespore. During devel- membrane segment (TMS) and a C-terminal extracellular do- opment the mother cell engulfs the forespore to produce a pro- main. Although SpoIIIAH is inserted randomly into the mother toplast, surrounded by two bilayer membranes, which separate it cell membrane, it is targeted to the sporulation septum, sepa- from the cytoplasm of the mother cell. The activation of ␴G, which rating the mother cell and forespore, through an interaction of drives late gene expression in the forespore, follows forespore its C-terminal domain with the forespore integral membrane engulfment and requires expression of the spoIIIA locus in the protein SpoIIQ (4, 5). SpoIIIAH and SpoIIQ colocalize along mother cell. One of the spoIIIA-encoded proteins SpoIIIAH is the engulfing membrane and form discrete foci surrounding the targeted specifically to the membrane surrounding the forespore, forespore. However, it is unclear why SpoIIIAH is necessary for through an interaction of its C-terminal extracellular domain with ␴G activity in the forespore. the C-terminal extracellular domain of the forespore membrane In this study, we identified a homologous relationship between protein SpoIIQ. We identified a homologous relationship between SpoIIIAH and the proteins that form the export channel and the C-terminal domain of SpoIIIAH and the YscJ/FliF protein family, structural scaffold of type III secretion and flagellar export members of which form multimeric rings involved in type III systems. We hypothesized that if SpoIIIAH also forms a channel, secretion systems and flagella. If SpoIIIAH forms a similar ring then its C-terminal extracellular domain may be accessible to structure, it may also form a channel between the mother cell and modification by an enzyme produced in the forespore. To test forespore membranes. To test this hypothesis we developed a this hypothesis, we developed a compartmentalized biotinylation compartmentalized biotinylation assay, which we used to show assay. Using this assay, we demonstrated that the C-terminal that the C-terminal extracellular domain of SpoIIIAH is accessible to domain of SpoIIIAH is accessible to biotin ligase produced in the enzymatic modification from the forespore cytoplasm. These and forespore. These and other results suggest that SpoIIIAH and other results lead us to suggest that SpoIIIAH forms part of a SpoIIQ may form a channel between the mother cell and channel between the forespore and mother cell that is required for forespore. the activation of ␴G. Results Bacillus subtilis ͉ flagellar protein export apparatus ͉ sporulation ͉ C-Terminal Extracellular Domain of SpoIIIAH Is Homologous to the type III secretion system YscJ/FliF Protein Family. Although no significant relationship to a protein of known function could be established using conven- tional search methods, the HHpred server (6, 7) identified a ndospore formation in the gram-positive bacterium Bacillus homologous relationship between the C-terminal extracellular subtilis involves a series of morphological changes that E domain of SpoIIIAH and the YscJ/FliF protein family (PF01514) culminate in the production of a dormant spore (reviewed in (Fig. 1A). The sequence similarity covers a 78-amino-acid stretch refs. 1–3). In response to nutrient depletion, vegetative cells with 23% identity, corresponding to the C-terminal domain of undergo an asymmetric cell division that yields two dissimilar the YscJ proteins and the central domain of the FliF proteins. progeny cells, the mother cell and forespore. Remarkably, the The members of the YscJ family are involved in type III secretion mother cell engulfs the forespore and nurtures it to maturity. of virulence factors in gram-negative bacteria (8). The structure Ultimately, the mother cell lyses, releasing the mature spore. The of a representative member, the enteropathogenic Escherichia differentiation of these two cell types is governed by two parallel coli EscJ protein, indicated that these proteins probably form programs of gene expression controlled by a cascade of alter- ring structures with a central channel that is 75Å in diameter (9). native RNA polymerase sigma (␴) factors. To synchronize the The dimensions of the 24-subunit EscJ ring were similar to those differentiation of the mother cell and forespore, the two pro- estimated by electron microscopy (10). The YscJ ring is thought grams of gene expression are coordinated through a series of intercellular signaling pathways. Following asymmetric cell di- ␴F ␴F vision, is activated in the forespore. then signals the Author contributions: J.M., X.W., A.O.H., and C.P.M. designed research; J.M., X.W., and M.S. activation of ␴E in the mother cell. Together, ␴F and ␴E control performed research; J.M. and X.W. analyzed data; and J.M., X.W., and C.P.M. wrote the expression of the genes responsible for forespore engulfment. paper. After the completion of forespore engulfment, ␴G is activated in The authors declare no conflict of interest. the forespore and signals the activation of ␴K in the mother cell. This article is a PNAS Direct Submission. G K ␴ and ␴ control expression of the genes necessary for fore- †J.M. and X.W. contributed equally to this work. spore maturation. While the intercellular signaling pathways that ‡Present address: Meningitis Laboratory, Meningitis and Vaccine Preventable Diseases trigger the activation of ␴E and ␴K in the mother cell are well Branch, CDC/NCIRD/DBD, Atlanta, GA 30333. G understood, the mechanisms that trigger the activation of ␴ in ¶To whom correspondence should be addressed. E-mail: [email protected]. the forespore are not known. This article contains supporting information online at www.pnas.org/cgi/content/full/ In addition to the completion of forespore engulfment, the 0806301105/DCSupplemental. eight-gene spoIIIA locus (spoIIIAA–AH) is also necessary for the © 2008 by The National Academy of Sciences of the USA 15100–15105 ͉ PNAS ͉ September 30, 2008 ͉ vol. 105 ͉ no. 39 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0806301105 Downloaded by guest on October 3, 2021 Fig. 1. Homology between SpoIIIAH and the YscJ/FliF protein family. HHpred alignment of SpoIIIAH and the YscJ/FliF family. (A) Identical (black boxes) and similar (gray boxes) amino acids are highlighted. Predicted secondary structure is indicated above the alignment. Cartoon representations of the type III secretion system (B), flagellar basal body (C), and SpoIIIAH channel model (D). YscJ, FliF, and SpoIIIAH are labeled and colored green. The extracellular space (ES), cell wall (CW), periplasm (P), and cytoplasm (C) of gram-negative bacteria, and mother cell (MC), intermembrane space (IMS), and forespore (FS) of bacterial endospores are indicated. to form the inner membrane channel of the type III secretion prediction, we developed a compartmentalized biotinylation system (Fig. 1B) (11). The FliF protein forms the bacterial assay, involving the biotinylation of target proteins by the E. coli flagellar protein export channel and the structural scaffold for biotin ligase, BirA, produced in either the mother cell or flagellar assembly (Fig. 1C) (12). Therefore, we hypothesized forespore (Fig. 2 A and B). BirA transfers biotin to a specific that the C-terminal extracellular domain of SpoIIIAH forms a lysine in biotin-accepting proteins (14). Biotinylated proteins can large, hollow ring with the N-terminal TMS anchored in the then be detected by Western blot with a streptavidin-horseradish mother cell membrane (Fig. 1D). The SpoIIIAH ring may be part peroxidase (HRP) conjugate (15). We tagged proteins with a 14-amino-acid biotin acceptor peptide (BAP), defined as the of a channel between the mother cell and forespore. The minimal substrate required for E. coli BirA-catalyzed biotinyla- similarity of SpoIIIAH with the YscJ/FliF protein family and the tion (16). Then we tested whether the fusion proteins were hypothesis that SpoIIIAH forms a channel were independently biotinylated in B. subtilis strains producing the E. coli BirA in proposed by Camp and Losick (13). either the mother cell or forespore, under the control of the spoIID and spoIIQ promoters, respectively (17, 18). Immunoblot Compartmentalized Biotinylation Assay. If SpoIIIAH forms part of analysis of BirA indicated that similar amounts of BirA accu- a channel between the mother cell and forespore, then the mulated after the onset of sporulation in both the mother cell- C-terminal extracellular domain may be accessible to modifica- and forespore-producing strains [supporting information (SI) tion by an enzyme produced in the forespore. To test this Fig. S1]. P -birAP -bir A A B s poIID spoIIQ biotin FS MC BAP-tagged fusion protei n BirA C D IIID-BAP: - - + + + G - BAP : - - + + + BirA : MC FS - MC FS BirA : MC FS - MC FS biotinyl biotinyl G IIID-BAP -BAP MICROBIOLOGY biotinyl biotinyl BCCP BCCP 1234 5 12 34 5 Fig. 2. Compartmentalized biotinylation assay. Cartoon representations of (A) BirA-catalyzed transfer of biotin to biotin acceptor peptide (BAP)-tagged fusion proteins, and (B) strains producing E.coli BirA in the mother cell (MC) and the forespore (FS).
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