Cyanobacterial growth and morphology are influenced by carboxysome positioning and temperature

Cyanobacteria are the prokaryotic group of phytoplankton responsible for a significant fraction of global CO2 fixation. Like plants, cyanobacteria use the enzyme Ribulose 1,5-bisphosphate Carboxylase/Oxidase (RuBisCO) to fix CO2 into organic carbon molecules via the Calvin-Benson-Bassham cycle. Unlike plants, cyanobacteria evolved a carbon concentrating organelle called the carboxysome - a proteinaceous compartment that encapsulates and concentrates RuBisCO along with its CO2 substrate. In the rod-shaped cyanobacterium Synechococcus elongatus PCC7942, we recently identified the McdAB system responsible for uniformly distributing carboxysomes along the cell length. It remains unknown what role carboxysome positioning plays with respect to cellular physiology. Here, we show for the first time that a failure to distribute carboxysomes leads to a temperature-dependent decrease in cell growth rate, cell division arrest, cell elongation, asymmetric cell division, and a significant reduction in cellular levels of RuBisCO. Unexpectedly, we also report that even wild-type S. elongatus undergoes filamentous growth at the cool, but environmentally-relevant, growth temperature of 20{degrees}C. The findings suggest that carboxysome positioning by the McdAB system functions to maintain the carbon-fixation efficiency of RuBisCO by preventing carboxysome aggregation, which is particularly important at temperatures where rod-shaped cyanobacteria adopt a filamentous morphology. IMPORTANCEPhotosynthetic cyanobacteria are responsible for almost half of global CO2 fixation. Due to eutrophication, rising temperatures, and increasing atmospheric CO2 concentrations, cyanobacteria have recently gained notoriety for their ability to form massive blooms in both freshwater and marine ecosystems across the globe. Like plants, cyanobacteria use the most abundant enzyme on Earth, RuBisCO, to provide the sole source of organic carbon required for its photosynthetic growth. Unlike plants, cyanobacteria have evolved a carbon-concentrating organelle called the carboxysome that encapsulates and concentrates RuBisCO with its CO2 substrate to significantly increase carbon-fixation efficiency and cell growth. We recently identified the positioning system that distributes carboxysomes in cyanobacteria. However, the physiological consequence of carboxysome mispositioning in the absence of this distribution system remains unknown. Here we find that carboxysome mispositioning triggers temperature-dependent changes in cell growth and morphology as well as a significant reduction in cellular levels of RuBisCO.