Nucleoid compaction influences carboxysome localization and dynamics in Synechococcus elongatus PCC 7942.

The bacterial nucleoid is not just a genetic repository-it serves as a dynamic scaffold for spatially organizing key cellular components. ParA-family ATPases exploit this nucleoid matrix to position a wide range of cargos, yet how nucleoid compaction influences these positioning reactions remains poorly understood. We previously characterized the maintenance of carboxysome distribution (Mcd) system in the cyanobacterium Synechococcus elongatus PCC 7942, where the ParA-like ATPase McdA binds the nucleoid and interacts with its partner protein, McdB, to generate dynamic gradients that distribute carboxysomes for optimal carbon fixation. Here, we investigate how nucleoid compaction impacts carboxysome positioning, particularly during metabolic dormancy when McdAB activity is downregulated. We demonstrate that a compacted nucleoid maintains carboxysome organization in the absence of active McdAB-driven positioning. This finding reveals that the nucleoid is not merely a passive matrix for positioning but a dynamic player in spatial organization. Given the widespread role of ParA-family ATPases in the positioning of diverse cellular cargos, our study suggests that the nucleoid compaction state is a fundamental, yet underappreciated, determinant of mesoscale organization across bacteria.

Importance: Bacteria can organize their internal components in specific patterns to ensure proper function and faithful inheritance after cell division. In the cyanobacterium Synechococcus elongatus, protein-based compartments called carboxysomes fix carbon dioxide and are distributed in the cell by a two-protein positioning system. Here, we discovered that when cells stop growing or face stress, these positioning proteins stop working, yet carboxysomes remain distributed in the cell. Our study shows that the bacterial chromosome, which holds genetic information, can also act as a flexible scaffold that holds carboxysomes in place when compacted. This insight reveals that the bacterial chromosome plays a key physical role in organizing the cell. Similar positioning systems are found across many types of bacteria; therefore, our findings suggest that nucleoid compaction may be a universal and underappreciated factor in maintaining spatial order in cells that are not actively growing.