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

Abstract

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.

The involvement of type IV pili and the phytochrome CphA in gliding motility, lateral motility and photophobotaxis of the cyanobacterium Phormidium lacuna

“…Most genetic and molecular studies on cyanobacterial motility have been performed with the single celled species Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7924 [ 10 – 12 ] and one member of Nostocales [ 7 ], Nostoc punctiforme [ 8 , 13 ]. Type IV pili act as driving complexes for gliding motility (often referred to as twitching motility) and have been intensely investigated in other bacteria such as Pseudomonas aeruginosa [ 14 ] or Neisseria meningitidis [ 15 ].…”

PATAN-domain response regulators interact with the Type IV pilus motor to control phototactic orientation in the cyanobacterium Synechocystis sp. PCC 6803

“…Therefore, it can be reasonably assumed that phototaxis in Synechocystis is controlled by two distinct regulatory pathways. The first regulatory circuit establishes cell polarity, presumably through indirect light sensing via alterations in proton motive force (45). At the same time, another system integrates the spectral quality of the incoming light to determine the orientation of polarity and thereby the direction of phototaxis.…”

“…We speculate that apart from PilB1 and PilC, Synechocystis PatA-type regulators interact with other proteins to determine the orientation of pilus assembly during phototaxis. A promising candidate would be HmpF, a filament-forming protein essential for motility in Synechocystis and N. punctiforme that exhibits dynamic, unipolar localization to the leading cell poles in motile filaments (45,50,52,53).…”

Thermosynechococcus switches the direction of phototaxis by a c-di-GMP dependent process with high spatial resolution

“…However, the pixJ orthologue is deleted from the genome of our WT strain (33). Recent work reported that the GAF domain-containing photoreceptor PixJ is not responsible for the phototactic motility of the filament-forming cyanobacterium Nostoc punctiforme (34). The authors hypothesized that the localized proton motive force is the first input for directional light sensing (34).…”

“…Recent work reported that the GAF domain-containing photoreceptor PixJ is not responsible for the phototactic motility of the filament-forming cyanobacterium Nostoc punctiforme (34). The authors hypothesized that the localized proton motive force is the first input for directional light sensing (34). Considering the micro-optic effects in rod-shaped cyanobacteria (Fig.…”