Microbial Metabolism and Disease Virulence Changes Across Day and Night in Coral Black Band Disease Lesions

Coral black band disease (BBD) is characterised as a cyanobacteria-dominated microbial mat that rapidly kills underlying coral tissue. Solar radiation promotes lesion progression by fuelling the cyanobacterial photosynthesis, while sulphate-reducing bacteria and sulphide-oxidising bacteria are implicated in sulphide dynamics within the mat. How the metabolism of the key microbial communities in the mat varies under light and dark conditions and impacts lesion virulence is poorly characterised, however. To compare microbial gene expression under different light regimes, we recovered 28 near-complete BBD-derived metagenome-assembled genomes (MAGs) using Oxford Nanopore Technologies long-read sequencing and profiled Illumina metatranscriptomic reads from BBD lesions collected at day and night by mapping to these MAGs. Genes from the cyanobacterium Roseofilum reptotaenium dominated the differentially expressed genes, with photosynthesis highly represented during the daytime. Relative expression of sulphur and nitrogen metabolism, cofactor biosynthesis, chemotaxis and motility increased among the non-cyanobacterial members at night. Enhanced sulphur reduction by Campylobacteriales and Desulfovibrionaceae at night likely supports a sulphide-rich and low oxygen micro-environment in the lesion, while increased chemotaxis and motility by Campylobacteriales and other heterotrophic bacteria drive lesion progression towards healthy coral tissue. This study provides insights into how diurnal light dynamics drive microbial metabolic pathways changes, thereby promoting BBD virulence.