Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, Michigan, USA.
mBio. 2021 Aug 31;12(4):e0269620. doi: 10.1128/mBio.02696-20. Epub 2021 Aug 3.
Cyanobacteria are the prokaryotic group of phytoplankton responsible for a significant fraction of global CO fixation. Like plants, cyanobacteria use the enzyme ribulose 1,5-bisphosphate carboxylase/oxidase (Rubisco) to fix CO 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 CO substrate. In the rod-shaped cyanobacterium Synechococcus elongatus PCC 7942, 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 that a failure to distribute carboxysomes leads to slower cell growth, cell elongation, asymmetric cell division, and elevated levels of cellular Rubisco. Unexpectedly, we also report that even wild-type S. elongatus undergoes cell elongation and asymmetric cell division when grown at the cool, but environmentally relevant, growth temperature of 20°C or when switched from a high- to ambient-CO environment. 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 under growth conditions where rod-shaped cyanobacteria adopt a filamentous morphology. Photosynthetic cyanobacteria are responsible for almost half of global CO fixation. Due to eutrophication, rising temperatures, and increasing atmospheric CO concentrations, cyanobacteria have 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 CO 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 changes in cell growth and morphology as well as elevated levels of cellular Rubisco.
蓝藻是负责全球 CO 固定的浮游植物的原核组。与植物一样，蓝藻使用核酮糖 1,5-二磷酸羧化酶/加氧酶（Rubisco）通过卡尔文-本森-巴斯汉姆循环将 CO 固定到有机碳分子中。与植物不同的是，蓝藻进化出了一种叫做羧化体的碳浓缩细胞器——一种包裹和浓缩 Rubisco 及其 CO 底物的蛋白隔间。在棒状蓝藻 Synechococcus elongatus PCC 7942 中，我们最近确定了 McdAB 系统负责沿细胞长度均匀分布羧化体。羧化体定位在细胞生理学方面的作用尚不清楚。在这里，我们表明，羧化体分布不良会导致细胞生长、细胞伸长、不对称细胞分裂和细胞内 Rubisco 水平升高。出乎意料的是，我们还报告说，即使是野生型 S. elongatus 在 20°C 的凉爽但与环境相关的生长温度下生长或从高 CO 环境切换到环境 CO 时，也会经历细胞伸长和不对称细胞分裂。这些发现表明，McdAB 系统通过防止羧化体聚集来维持 Rubisco 的碳固定效率，这在棒状蓝藻采用丝状形态的生长条件下尤为重要。 光合蓝藻负责全球近一半的 CO 固定。由于富营养化、温度升高和大气 CO 浓度增加，蓝藻因其在全球淡水和海洋生态系统中形成大量水华的能力而声名狼藉。与植物一样，蓝藻使用地球上最丰富的酶——Rubisco——为其光合作用生长提供唯一的有机碳来源。与植物不同的是，蓝藻进化出了一种叫做羧化体的碳浓缩细胞器，它将 Rubisco 与其 CO 底物包裹并浓缩，从而显著提高碳固定效率和细胞生长。我们最近确定了在蓝藻中分布羧化体的定位系统。然而，在没有这种分布系统的情况下，羧化体定位错误的生理后果仍然未知。在这里，我们发现羧化体定位错误会引发细胞生长和形态的变化以及细胞内 Rubisco 水平的升高。
