Unraveling the diversity and functional potential of cyanosphere microbiomes assembled from terrestrial cyanobacteria

The cyanosphere is composed of non-cyanobacterial microorganisms living within the exopolysaccharide sheath of cyanobacteria, interacting with the cyanobacterial hosts and their surrounding environment. Understanding the interactions between cyanobacteria and their cyanospheres can help predict the success of terrestrial cyanobacteria in providing ecosystem services in nutrient-poor environments. However, knowledge of the microbial diversity and functions within the cyanosphere remains limited. Here, we used metagenomic sequencing to reconstruct 415 metagenome-assembled genomes (MAGs) from cyanosphere-associated microbes linked to 56 terrestrial cyanobacteria cultures, representing 12 cyanobacterial orders. Our findings showed that the composition of cyanosphere microbial communities was significantly shaped by environmental factors such as habitat of host origin, including precipitation and temperature. Three microbial genera, Brevundimonas, Devosia, and Sphingopyxis, were present in over 30% of the cyanospheres, suggesting a core cyanosphere microbiome. Functional gene analysis showed a distinction between the cyanobacteria and their associated cyanospheres, with dissimilatory nitrate reduction being the dominant pathway in the cyanosphere, an anaerobic process that retains nitrogen in the host-cyanosphere system in contrast to denitrification. While nitrogen fixation was more common in the cyanobacteria, 15 cyanospheres also contained nitrogen fixation genes, including in hosts that were nitrogen fixation capable themselves. The cyanosphere also contained genes for polysaccharide lyases, indicating a possible link to the exopolysaccharides produced by the cyanobacteria. Given the observed variability in microbial community composition and function across different cyanobacterial hosts, future ecological assessments and restoration efforts involving cyanobacteria should not only focus on the cyanobacteria themselves but also consider their associated microbial communities.IMPORTANCEOur study identifies members of an understudied and under-valued microbial community, the cyanosphere. We used a diversity of terrestrial cyanobacteria to understand how the cyanosphere composition and predicted functions were influenced by the host cyanobacterium and environmental factors using metagenomics. This is a novel approach to studying the cyanosphere, providing insights into the diversity of terrestrial microbial communities. Importantly, our results underscore the need to consider microbial consortia when assessing the ecological potential of cyanobacteria in terrestrial restoration.