The cyanobacterial taxis protein HmpF regulates type IV pilus activity in response to light

Abstract

Significance Many photosynthetic cyanobacteria are capable of migrating in response to light in a process known as phototaxis. In all of the cyanobacteria where this process has been characterized at the genetic and molecular level, motility has been shown to be powered by type IV pili and influenced by chemotaxis-like systems with methyl-accepting chemotaxis proteins containing light-sensing GAF domains. However, the means by which the light-sensing systems modulate T4P activity has not been defined. In this study we provide evidence that cyanobacteria possess a second, distinct system for sensing light, the Hmp chemotaxis-like system, which lacks a GAF domain and modulates direct interaction between the cyanobacterial taxis protein HmpF and the T4P to regulate motility in response to light. Motility is ubiquitous in prokaryotic organisms including the photosynthetic cyanobacteria where surface motility powered by type 4 pili (T4P) is common and facilitates phototaxis to seek out favorable light environments. In cyanobacteria, chemotaxis-like systems are known to regulate motility and phototaxis. The characterized phototaxis systems rely on methyl-accepting chemotaxis proteins containing bilin-binding GAF domains capable of directly sensing light, and the mechanism by which they regulate the T4P is largely undefined. In this study we demonstrate that cyanobacteria possess a second, GAF-independent, means of sensing light to regulate motility and provide insight into how a chemotaxis-like system regulates the T4P motors. A combination of genetic, cytological, and protein–protein interaction analyses, along with experiments using the proton ionophore carbonyl cyanide m-chlorophenyl hydrazine, indicate that the Hmp chemotaxis-like system of the model filamentous cyanobacterium Nostoc punctiforme is capable of sensing light indirectly, possibly via alterations in proton motive force, and modulates direct interaction between the cyanobacterial taxis protein HmpF, and Hfq, PilT1, and PilT2 to regulate the T4P motors. Given that the Hmp system is widely conserved in cyanobacteria, and the finding from this study that orthologs of HmpF and T4P proteins from the distantly related model unicellular cyanobacterium Synechocystis sp. strain PCC6803 interact in a similar manner to their N. punctiforme counterparts, it is likely that this represents a ubiquitous means of regulating motility in response to light in cyanobacteria.