SummaryCarboxysomes are protein-based organelles essential for carbon fixation in cyanobacteria and proteobacteria. Previously, we showed that the cyanobacterial nucleoid is utilized as a surface for the equidistant-spacing of β-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 β-cyanobacteria, which possess β-carboxysomes, but are absent in α-cyanobacteria, which possess structurally distinct α-carboxysomes. Since cyanobacterial α-carboxysomes are thought to have arisen in proteobacteria and were subsequently horizontally transferred into cyanobacteria, this raised the question whether α-carboxysome containing proteobacteria possess a McdAB system for positioning α-carboxysomes. Here, using the model chemoautotrophic proteobacterium H. neapolitanus, we show that a McdAB system distinct from that of β-cyanobacteria operates to position α-carboxysomes across cell lengths. We further show that this system is widespread among α-carboxysome containing proteobacteria and that cyanobacteria likely inherited an α-carboxysome operon from a proteobacterium lacking the mcdAB locus. These results demonstrate that McdAB is a cross-phylum two-component system necessary for positioning α- and β-carboxysomes. The findings have further implications for understanding the positioning of other bacterial protein-based organelles involved in diverse metabolic processes.
The McdAB system positions α-carboxysomes in proteobacteria