The McdAB system positions α-carboxysomes in proteobacteria

Carboxysomes are protein-based organelles essential for carbon fixation in cyanobacteria and proteobacteria. Previously, we showed that the cyanobacterial nucleoid is used to equally space out beta-carboxysomes across cell lengths by a two-component system (McdAB) in the model cyanobacterium Synechococcus elongatus PCC 7942. More recently, we found that McdAB systems are widespread among beta-cyanobacteria, which possess beta-carboxysomes, but are absent in alpha-cyanobacteria, which possess structurally and phyletically distinct alpha-carboxysomes. Cyanobacterial alpha-carboxysomes are thought to have arisen in proteobacteria and then horizontally transferred into cyanobacteria, which suggests that alpha-carboxysomes in proteobacteria may also lack the McdAB system. Here, using the model chemoautotrophic proteobacterium Halothiobacillus neapolitanus, we show that a McdAB system distinct from that of beta-cyanobacteria operates to position alpha-carboxysomes across cell lengths. We further show that this system is widespread among alpha-carboxysome-containing proteobacteria and that cyanobacteria likely inherited an alpha-carboxysome operon from a proteobacterium lacking the mcdAB locus. These results demonstrate that McdAB is a cross-phylum two-component system necessary for positioning both alpha- and beta-carboxysomes. The findings have further implications for understanding the positioning of other protein-based bacterial organelles involved in diverse metabolic processes. Plain language summary Cyanobacteria are well known to fix atmospheric CO2 into sugars using the enzyme Rubisco. Less appreciated are the carbon-fixing abilities of proteobacteria with diverse metabolisms. Bacterial Rubisco is housed within organelles called carboxysomes that increase enzymatic efficiency. Here we show that proteobacterial carboxysomes are distributed in the cell by two proteins, McdA and McdB. McdA on the nucleoid interacts with McdB on carboxysomes to equidistantly space carboxysomes from one another, ensuring metabolic homeostasis and a proper inheritance of carboxysomes following cell division. This study illuminates how widespread carboxysome positioning systems are among diverse bacteria. Carboxysomes significantly contribute to global carbon fixation; therefore, understanding the spatial organization mechanism shared across the bacterial world is of great interest.

Automated summary

Carboxysomes are protein-based organelles essential for carbon fixation in cyanobacteria and proteobacteria. Different types of carboxysomes are positioned by distinct McdAB systems in cyanobacteria and proteobacteria. Understanding the spatial organization mechanism shared across diverse bacteria is crucial for metabolic processes.