Transcription-driven DNA supercoiling counteracts H-NS-mediated gene silencing in bacterial chromatin

Nara Figueroa-Bossi, Rocío Fernández-Fernández, Patricia Kerboriou, Philippe Bouloc, Josep Casadesús, María Antonia Sánchez-Romero and Lionello Bossi ()
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Nara Figueroa-Bossi: Institut de Biologie Intégrative de la Cellule (I2BC)
Rocío Fernández-Fernández: Universidad de Sevilla
Patricia Kerboriou: Institut de Biologie Intégrative de la Cellule (I2BC)
Philippe Bouloc: Institut de Biologie Intégrative de la Cellule (I2BC)
Josep Casadesús: Universidad de Sevilla
María Antonia Sánchez-Romero: Universidad de Sevilla
Lionello Bossi: Institut de Biologie Intégrative de la Cellule (I2BC)

Nature Communications, 2024, vol. 15, issue 1, 1-12

Abstract: Abstract In all living cells, genomic DNA is compacted through interactions with dedicated proteins and/or the formation of plectonemic coils. In bacteria, DNA compaction is achieved dynamically, coordinated with dense and constantly changing transcriptional activity. H-NS, a major bacterial nucleoid structuring protein, is of special interest due to its interplay with RNA polymerase. H-NS:DNA nucleoprotein filaments inhibit transcription initiation by RNA polymerase. However, the discovery that genes silenced by H-NS can be activated by transcription originating from neighboring regions has suggested that elongating RNA polymerases can disassemble H-NS:DNA filaments. In this study, we present evidence that transcription-induced counter-silencing does not require transcription to reach the silenced gene; rather, it exerts its effect at a distance. Counter-silencing is suppressed by introducing a DNA gyrase binding site within the intervening segment, suggesting that the long-range effect results from transcription-driven positive DNA supercoils diffusing toward the silenced gene. We propose a model wherein H-NS:DNA complexes form in vivo on negatively supercoiled DNA, with H-NS bridging the two arms of the plectoneme. Rotational diffusion of positive supercoils generated by neighboring transcription will cause the H-NS-bound negatively-supercoiled plectoneme to “unroll” disrupting the H-NS bridges and releasing H-NS.

Date: 2024
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DOI: 10.1038/s41467-024-47114-w

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