Light-dependent changes in the higher-order DNA structure of the cyanobacterium Synechocystis sp. PCC 6803

Abstract

Chromosome spatial organization plays critical roles in transcriptional regulation and DNA protection. In cyanobacteria--photosynthetic bacteria that experience dramatic fluctuations in light intensity--chromosome reorganization could facilitate rapid transcriptional reprogramming and protect DNA from photodamage. However, chromosome organization in these polyploid organisms has remained technically challenging to observe, leaving light-dependent responses unexplored. Here, we show that higher-order chromosome organization in Synechocystis sp. PCC 6803 is associated with light intensity, revealing a previously unrecognized light-dependent adaptation in cyanobacteria. We established fluorescence in situ hybridization (FISH) methods for this model cyanobacterium carrying multi-copy genomes, together with a computational pipeline to assign paired FISH signals to individual genome copies. The slope relating genomic and spatial distance was steeper under standard conditions ({beta} = 0.972 nm/kbp, R{superscript 2} = 0.12) than under high-light conditions ({beta} = 0.450 nm/kbp, R{superscript 2} = 0.02), indicating that local chromosome organization is substantially disrupted by elevated light intensity. The spatial distribution of the multiple genome copies also differed between conditions, independently supporting condition-dependent chromosome reorganization. Hi-C analysis corroborated these findings, revealing reduced chromosomal interactions within the 10-100 kbp range under high-light conditions. Together, these results demonstrate that light intensity is a previously unrecognized determinant of higher-order chromosome organization in a photosynthetic bacterium.