Marine biofilms: cyanobacteria factories for the global oceans

Abstract Marine biofilms were newly revealed as a giant microbial diversity pool for global oceans. However, the cyanobacterial diversity in marine biofilms within the upper seawater column and its ecological and evolutionary implications remains undetermined. Here, we reconstructed a full picture of modern marine cyanobacteria habitats by re-analysing 9.3 terabyte metagenomic datasets and 2648 metagenome-assembled genomes (MAGs). The abundance of cyanobacteria lineages exclusively detected in marine biofilms were up to 9-fold higher than those in seawater at similar sample size. Analyses revealed that cyanobacteria in marine biofilms are specialists with strong geographical and environmental constraints on their genome and functional adaption, which in stark contrast to the generalistic features of seawater-derived cyanobacteria. Molecular dating suggests the important diversifications in biofilm-forming cyanobacteria appear to coincide with the Great Oxidation Event (GOE), “boring billion” middle Proterozoic, and the Neoproterozoic Oxidation Event (NOE). These new insights suggest that marine biofilms are large and important cyanobacterial factories for the global oceans. Importance Cyanobacteria, highly diverse microbial organisms, play a crucial role in Earth’s oxygenation and biogeochemical cycling. However, their connection to these processes remains unclear, partly due to incomplete surveys of oceanic niches. Our study uncovered significant cyanobacterial diversity in marine biofilms, showing distinct niche differentiation compared to seawater counterparts. These patterns reflect three key stages of marine cyanobacterial diversification, coinciding with major geological events in Earth’s history. Thus, surface-associated biomass within oceanic niches emerges as a pivotal factor in Earth’s evolution.