A DnaK(Hsp70) Chaperone System Connects Type IV Pilus Activity to Polysaccharide Secretion in Cyanobacteria

Surface motility powered by type IV pili (T4P) is widespread among bacteria, including the photosynthetic cyanobacteria. This form of movement typically requires the deposition of a motility-associated polysaccharide, and several studies indicate that there is complex coregulation of T4P motor activity and polysaccharide production, although a mechanistic understanding of this coregulation is not fully defined. Here, using a combination of genetic, comparative genomic, transcriptomic, protein-protein interaction, and cytological approaches in the model filamentous cyanobacterium N. punctiforme, we provided evidence that a DnaK-type chaperone system coupled the activity of the T4P motors to the production of the motility-associated hormogonium polysaccharide (HPS). The results from these studies indicated that DnaK1 and DnaJ3 along with GrpE comprised a chaperone system that interacted specifically with active T4P motors and was required to produce HPS. Genomic conservation in cyanobacteria and the conservation of the protein-protein interaction network in the model unicellular cyanobacterium Synechocystis sp. strain PCC 6803 imply that this system is conserved among nearly all motile cyanobacteria and provides a mechanism to coordinate polysaccharide secretion and T4P activity in these organisms.