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      Differential Spo0A-mediated effects on transcription and replication of the related Bacillus subtilis phages Nf and ϕ29 explain their different behaviours in vivo

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          Abstract

          Members of groups 1 (e.g. ϕ29) and 2 (e.g. Nf) of the ϕ29 family of phages infect the spore forming bacterium Bacillus subtilis. Although classified as lytic phages, the lytic cycle of ϕ29 can be suppressed and its genome can become entrapped into the B. subtilis spore. This constitutes an alternative infection strategy that depends on the presence of binding sites for the host-encoded protein Spo0A in the ϕ29 genome. Binding of Spo0A to these sites represses ϕ29 transcription and prevents initiation of DNA replication. Although the Nf genome can also become trapped into B. subtilis spores, in vivo studies showed that its lytic cycle is less susceptible to spo0A-mediated suppression than that of ϕ29. Here we have analysed the molecular mechanism underlying this difference showing that Spo0A differently affects transcription and replication initiation of the genomes of these phages. Thus, whereas Spo0A represses all three main early promoters of ϕ29, it only represses one out of the three equivalent early promoters of Nf. In addition, contrary to ϕ29, Spo0A does not prevent the in vitro initiation of Nf DNA replication. Altogether, the differences in Spo0A-mediated regulation of transcription and replication between ϕ29 and Nf explain their different behaviours in vivo.

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          Most cited references32

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          Regulation of endospore formation in Bacillus subtilis.

          Spore formation in bacteria poses a number of biological problems of fundamental significance. Asymmetric cell division at the onset of sporulation is a powerful model for studying basic cell-cycle problems, including chromosome segregation and septum formation. Sporulation is one of the best understood examples of cellular development and differentiation. Fascinating problems posed by sporulation include the temporal and spatial control of gene expression, intercellular communication and various aspects of cell morphogenesis.
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            High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis.

            The master regulator for entry into sporulation in Bacillus subtilis is the response regulator Spo0A, which directly governs the expression of about 121 genes. Using cells in which the synthesis of Spo0A was under the control of an inducible promoter or in which production of the regulatory protein was impaired by a promoter mutation, we found that sporulation required a high (threshold) level of Spo0A and that many genes in the regulon differentially responded to high and low doses of the regulator. We distinguished four categories of genes, as follows: (i) those that required a high level of Spo0A to be activated, (ii) those that required a high level of Spo0A to be repressed, (iii) those that were activated at a low level of the regulator, and (iv) those that were repressed at a low dose of the regulator. Genes that required a high dose of Spo0A to be activated were found to have low binding constants for the DNA-binding protein. Some genes that were turned on at a low dose of Spo0A either had a high binding constant for the regulatory protein or were activated by an indirect mechanism involving Spo0A-mediated relief of repression by the repressor protein AbrB. We propose that progressive increases in the level of Spo0A leads to an early phase of transcription in which genes that play auxiliary roles in development, such as cannibalism and biofilm formation, are turned on and a later phase in which genes that play a direct role in sporulation are activated.
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              The transcriptional profile of early to middle sporulation in Bacillus subtilis.

              Spore formation by Bacillus subtilis is governed by global changes in gene transcription. We used nylon-substrate DNA arrays representing approximately 96% of the predicted open reading frames in the B. subtilis chromosome to compare the pattern of transcripts from wild-type cells with the pattern from cells mutant for the sporulation transcription factors Spo0A or final sigma(F). We found 520 genes whose transcript levels were at least 3-fold dependent on Spo0A but not on final sigma(F), and an additional 66 genes whose transcript levels were dependent upon both regulatory proteins. Two strategies were used to help assign genes to the direct control of a particular developmental regulatory protein. In one approach, we analyzed the effects on global gene expression of artificially producing a constitutively active form of Spo0A during growth. In a second approach, Hidden Markov models were used to identify promoters likely to be activated by Spo0A, final sigma(F), or a third sporulation transcription factor, final sigma(E). In addition to detecting known sporulation genes, we identified many genes of unknown function whose patterns of expression and regulation suggest that they could be involved in sporulation. Disruption of two such newly identified genes, yabP and yabQ, blocked sporulation at a late stage.
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                Author and article information

                Journal
                Nucleic Acids Res
                Nucleic Acids Res
                nar
                nar
                Nucleic Acids Research
                Oxford University Press
                0305-1048
                1362-4962
                August 2009
                August 2009
                15 June 2009
                15 June 2009
                : 37
                : 15
                : 4955-4964
                Affiliations
                Instituto de Biología Molecular ‘Eladio Viñuela’ (CSIC), Centro de Biología Molecular ‘Severo Ochoa’ (CSIC-UAM), C/Nicolás Cabrera 1, Universidad Autónoma, Canto Blanco, 28049 Madrid, Spain
                Author notes
                *To whom correspondence should be addressed. Tel: +34 91 196 4675; Fax: +34 91 194 4677; Email: msalas@ 123456cbm.uam.es
                Correspondence may also be addressed to Wilfried J.J. Meijer. Tel: +34 91 196 4515; Fax: +34 91 194 4420; Email: wmeijer@ 123456cbm.uam.es
                Article
                gkp504
                10.1093/nar/gkp504
                2731898
                19528067
                663dcabd-7481-4f4c-b9a7-c4d23a840e6a
                © 2009 The Author(s)

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 10 February 2009
                : 22 May 2009
                : 25 May 2009
                Categories
                Molecular Biology

                Genetics
                Genetics

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