The microbiome of marine mat-forming cyanobacteria - A microcosm of taxonomic novelty and phototrophic diversity

Abstract Intertidal biological mats are highly dynamic ecosystems typically dominated by filamentous cyanobacteria of the genus Coleofasciculus. These primary producers play important roles in primary production, biogeochemical cycling, and coast protection. 16S rRNA gene profiling of non-axenic cultures has recently revealed an astonishing wealth of associated bacteria. We analyzed the microbiomes of 14 non-axenic Coleofasciculus cultures from nine globally distributed marine sampling sites, representing seven distinct phylogenomic lineages. Metagenome sequencing and binning resulted in 320 metagenome-assembled genomes (MAGs) representing a broad spectrum of ‘uncultivated’ bacterial diversity mostly belonging to Pseudomonadota, Bacteroidota and Planctomycetota. Marinovum algicola and Roseitalea porphyridii were found in twelve of the microbiomes studied, making them the most common housemates. The complex microbiome of Coleofasciculus sp. WW12 contained seven Planctomycetota MAGs from so far undescribed species, representing inter alia a new family in the order Phycisphaerales and a MAG from a deeply branching sister lineage of all cultivated planctomycetes. The discovery of 36 proteobacterial MAGs with photosynthesis gene clusters (PGCs) and 32 MAGs with proteorhodopsin or xanthorhodopsin operons documented the coexistence with many photoheterotrophic bacteria, indicating that the cyanosphere is a hotspot of phototrophic life. The presence of a PGC-containing Myxococcales MAG (Ca. Photomyxococcus marinus) is of special interest, because it paves the way to investigate the photosynthesis in Deltaproteobacteria. In a Mediterranean Coleofasciculus culture, three alphaproteobacterial MAGs were found that have both a xanthorhodopsin operon and the PGC, suggesting that dual phototrophy is not restricted to alpine lakes or glaciers, and can also be found in marine habitats.