Niche formation and metabolic interactions contribute to stable diversity in a spatially structured cyanobacterial community

Understanding how microbial communities maintain stable compositional diversity is a key question in microbial ecology. Studies from pairwise interactions and synthetic communities indicate that metabolic interactions and spatial organisation can influence diversity, but the relevance of these factors in more complex communities is unclear. Here we used a cyanobacterial enrichment community that consistently forms millimetre-scale granular structures, to investigate compositional diversity and its stability. Over a year of passaging in media without significant carbon source, we found stable co-existence of 17 species belonging to diverse bacterial phyla. Metagenomic analysis revealed polysaccharide breakdown genes and complementary vitamin biosynthesis pathways in these species. Supporting these findings, we show growth of several isolated species on cyanobacterial slime components and experimentally verify vitamin exchanges between two members of the community. Several species had genes for (an)oxygenic photosynthesis and sulfur cycling, the expression of which we verified via metatranscriptomics. Consistent with this, we found that the granular structures displayed oxygen gradients with anoxic interiors. Cyanobacteria and other bacteria were distributed on the periphery and insides of these structures, respectively. Perturbation of the community via glucose addition resulted in fold increases of the heterotrophs, whereas disturbing the community by continual shaking led to fold reductions in several heterotrophs, including anoxygenic phototrophs. In contrast, removal of vitamins supplementation did not consistently alter species coverages, due to predicted vitamin sharing amongst community members. Taken together, these findings indicate that spatial organisation, microenvironment niche formation and metabolic interactions contribute to community compositional diversity and stability.