Dynamical localization of a thylakoid membrane binding protein is required for acquisition of photosynthetic competency

Abstract

Vipp1 is highly conserved and essential for photosynthesis, but its function is unclear as it does not participate directly in light-dependent reactions. We analyzed Vipp1 localization in live cyanobacterial cells and show that Vipp1 is highly dynamic, continuously exchanging between a diffuse fraction that is uniformly distributed throughout the cell and a punctate fraction that is concentrated at high curvature regions of the thylakoid located at the cell periphery. Experimentally perturbing the spatial distribution of Vipp1 by relocalizing it to the nucleoid causes a severe growth defect during the transition from non-photosynthetic (dark) to photosynthetic (light) growth. However, the same perturbation of Vipp1 in dark alone or light alone growth conditions causes no growth or thylakoid morphology defects. We propose that the punctuated dynamics of Vipp1 at the cell periphery in regions of high thylakoid curvature enable acquisition of photosynthetic competency, perhaps by facilitating biogenesis of photosynthetic complexes involved in light-dependent reactions of photosynthesis.

What is Vipp1 good for?

“…Gutu et al . have now analyzed a GFP‐labeled Vipp1/IM30 variant to monitor the localization of IM30 in living cyanobacterial cells via super‐resolution fluorescence microscopy (Gutu et al ., ). When analyzed under normal growth conditions (100 µE m −2 s −1 ), the protein continuously exchanged between a diffuse fraction that is uniformly distributed within the cyanobacterial cytoplasm and TM‐associated puncta that form at the cell periphery in TM regions with high curvature.…”

“…When analyzed under normal growth conditions (100 µE m −2 s −1 ), the protein continuously exchanged between a diffuse fraction that is uniformly distributed within the cyanobacterial cytoplasm and TM‐associated puncta that form at the cell periphery in TM regions with high curvature. In growing cells, such puncta are rather short‐lived (1–2 min), whereas in non‐growing cells they appear to be stable (Gutu et al ., ). It has been calculated that the formed puncta contain ∼ 100 to 300 GFP molecules and exhibit an estimated diameter of ∼ 100 nm (Bryan et al ., ).…”

“…The in vivo study of Gutu et al . now enlivens the ongoing discussion on the physiological Vipp1/IM30 function by highlighting the subcellular localization of Vipp1/IM30 and by selectively depleting the cytoplasmic Vipp1/IM30 content at defined growth conditions (Gutu et al ., ). In the past, Vipp1/IM30 has been identified in the soluble fraction as well as being localized at the cyanobacterial cytoplasmic membrane and at TMs (Srivastava et al ., ; Fuhrmann et al ., ).…”

“…and Gutu et al . (Bryan et al ., ; Gutu et al ., ) seem to contradict the suggestion that Vipp1/IM30 rings form extended rod‐shaped assemblies of more than nine rings (Nordhues et al ., ; Rutgers and Schroda, ). More likely, Vipp1/IM30 rings disassemble on the membrane after binding and form defined regions (IM30‐enriched regions) or scaffold‐like aggregates on the membrane under certain conditions (Thurotte et al ., ) (Fig.…”

“…Thus, it is well possible that the function of IM30 involves tight binding to TMs as large and densely packed structures in order to maintain TM integrity and/or to control TM biogenesis. The bacterial proteins PspA and LiaH, which are close homologous of Vipp1/IM30, are also more evenly distributed throughout the cytoplasm of non‐photosynthetic bacteria under non‐stress conditions, but form localized puncta under defined stress conditions (Engl et al ., ; Yamaguchi et al ., ; Dominguez‐Escobar et al ., ), as also observed in the present study with Vipp1/IM30 (Gutu et al ., ). Thus, the homologous PspA, LiaH and Vipp1/IM30 proteins all appear to exhibit their function in large, membrane‐bound clusters, and formation of such membrane‐attached structures appears to be involved in membrane protection under membrane‐stress conditions.…”