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