Topoisomerase I (TopA) Is Recruited to ParB Complexes and Is Required for Proper Chromosome Organization during Streptomyces coelicolor Sporulation

• Published in: Journal of Bacteriology 2013-10, Vol.195 (19), p.4445-4455
• Main Authors: Szafran, Marcin, Skut, Patrycja, Ditkowski, Bartosz, Ginda, Katarzyna, Chandra, Govind, Zakrzewska-Czerwińska, Jolanta, Jakimowicz, Dagmara
• Format: Article
• Language: English
• Subjects: bacteria; Bacteriology; chromosome segregation; Chromosome Segregation - physiology; Chromosomes; Chromosomes, Bacterial - genetics; Cloning, Molecular; DNA Primase - genetics; DNA Primase - metabolism; DNA topoisomerase; DNA Topoisomerases, Type I - genetics; DNA Topoisomerases, Type I - metabolism; DNA, Superhelical; Enzymes; fungi; Gene Deletion; Gene Expression Regulation, Bacterial - physiology; Gene Expression Regulation, Enzymologic - physiology; Gram-positive bacteria; hyphae; Nucleoproteins - metabolism; spores; Spores, Bacterial; sporulation; Streptomyces; Streptomyces coelicolor; Streptomyces coelicolor - genetics; Streptomyces coelicolor - physiology
• ISSN: 0021-9193; 1098-5530; 1067-8832
• DOI: 10.1128/JB.00798-13

Streptomyces species are bacteria that resemble filamentous fungi in their hyphal mode of growth and sporulation. In Streptomyces coelicolor, the conversion of multigenomic aerial hyphae into chains of unigenomic spores requires synchronized septation accompanied by segregation of tens of chromosomes into prespore compartments. The chromosome segregation is dependent on ParB protein, which assembles into an array of nucleoprotein complexes in the aerial hyphae. Here, we report that nucleoprotein ParB complexes are bound in vitro and in vivo by topoisomerase I, TopA, which is the only topoisomerase I homolog found in S. coelicolor. TopA cannot be eliminated, and its depletion inhibits growth and blocks sporulation. Surprisingly, sporulation in the TopA-depleted strain could be partially restored by deletion of parB. Furthermore, the formation of regularly spaced ParB complexes, which is a prerequisite for proper chromosome segregation and septation during the development of aerial hyphae, has been found to depend on TopA. We hypothesize that TopA is recruited to ParB complexes during sporulation, and its activity is required to resolve segregating chromosomes.