Spatial rearrangement of the Streptomyces venezuelae linear chromosome during sporogenic development

Bacteria of the genus Streptomyces have a linear chromosome, with a core region and two ‘arms’. During their complex life cycle, these bacteria develop multi-genomic hyphae that differentiate into chains of exospores that carry a single copy of the genome. Sporulation-associated cell division requires chromosome segregation and compaction. Here, we show that the arms of Streptomyces venezuelae chromosomes are spatially separated at entry to sporulation, but during sporogenic cell division they are closely aligned with the core region. Arm proximity is imposed by segregation protein ParB and condensin SMC. Moreover, the chromosomal terminal regions are organized into distinct domains by the Streptomyces-specific HU-family protein HupS. Thus, as seen in eukaryotes, there is substantial chromosomal remodelling during the Streptomyces life cycle, with the chromosome undergoing rearrangements from an ‘open’ to a ‘closed’ conformation.

Spatial rearrangement of the Streptomyces venezuelae linear chromosome during sporogenic development

ABSTRACTDepending on the species, bacteria organize their chromosomes with either spatially separated or closely juxtaposed replichores. However, in contrast to eukaryotes, significant changes in bacterial chromosome conformation during the cell cycle have not been demonstrated to date. Streptomyces are unique among bacteria due to their linear chromosomes and complex life cycle. These bacteria develop multigenomic hyphae that differentiate into chains of unigenomic exospores. Only during sporulation-associated cell division, chromosomes are segregated and compacted. In this study, we show that at entry to sporulation, arms of S. venezuelae chromosomes are spatially separated, but they are closely aligned within the core region during sporogenic cell division. Arm juxtaposition is imposed by the segregation protein ParB and condensin SMC. Moreover, we disclose that the chromosomal terminal regions are organized into domains by the Streptomyces-specific protein - HupS. Thus, we demonstrate chromosomal rearrangement from open to close conformation during Streptomyces life cycle.