Identification of a hormogonium polysaccharide‐specific gene set conserved in filamentous cyanobacteria

• Published in: Molecular microbiology 2020-10, Vol.114 (4), p.597-608
• Main Authors: Zuniga, Esthefani G., Boateng, Kelvin K. A., Bui, Nhi U., Kurnfuli, Shadi, Muthana, Sawsan M., Risser, Douglas D.
• Format: Article
• Language: English
• Subjects: Assembly; Cyanobacteria; Exports; Filaments; Genes; Gliding; gliding motility; Hormogonia; Motility; Nostoc punctiforme; Photosynthesis; PilA protein; Pilin; polysaccharide; Polysaccharides; Semisolids; Twitching; type IV pili
• ISSN: 0950-382X; 1365-2958
• DOI: 10.1111/mmi.14566

Cyanobacteria comprise a phylum defined by the capacity for oxygenic photosynthesis. Members of this phylum are frequently motile as well. Strains that display gliding or twitching motility across semisolid surfaces are powered by a conserved type IV pilus system (T4P). Among the filamentous, heterocyst‐forming cyanobacteria, motility is usually confined to specialized filaments known as hormogonia, and requires the deposition of an associated hormogonium polysaccharide (HPS). The genes involved in assembly and export of HPS are largely undefined, and it has been hypothesized that HPS exits the outer membrane via an atypical T4P‐driven mechanism. Here, several novel hps loci, primarily encoding glycosyl transferases, are identified. Mutational analysis demonstrates that the majority of these genes are essential for both motility and production of HPS. Notably, most mutant strains accumulate wild‐type cellular levels of the major pilin PilA, but not extracellular PilA, indicating dysregulation of the T4P motors, and, therefore, a regulatory interaction between HPS assembly and T4P activity. A co‐occurrence analysis of Hps orthologs among cyanobacteria identified an extended set of putative Hps proteins comprising most components of a Wzx/Wzy‐type polysaccharide synthesis and export system. This implies that HPS may be secreted through a more canonical pathway, rather than a T4P‐mediated mechanism. Hormogonia are motile cyanobacterial filaments powered by type IV pili (T4P), and require the deposition of an associated hormogonium polysaccharide (HPS) for movement. Here, a large gene set essential for HPS production is defined. These genes are dispersed throughout the genome and encode a Wzy/Wzx‐type polysaccharide synthesis and export system highly conserved in filamentous cyanobacteria. Several of these genes affect the T4P motors as well, implying a regulatory interaction between HPS synthesis and T4P assembly.