Alternate succession of aggregate-forming cyanobacterial genera correlated with their attached bacteria by co-pathways

Freshwater lakes are threatened by harmful blooms characterized by Cyanobacterial Aggregates (CAs) that are normally aggregated with extracellular polysaccharides released by cyanobacteria to form a phycosphere. It is possible that mutualistic relationships exist between bacteria and cyanobacteria in these CAs wherein bacterial products supplement cyanobacterial growth, and cyanobacterial exudates, in turn, serve as substrates for bacteria, thus augmenting the stability of each constituent. However, little is known about the exact interaction between cyanobacteria and their attached bacteria in CAs. Therefore, in this study, we collected 26 CA samples from Lake Taihu, a large freshwater lake in China from March of 2015 to February of 2016. We then sequenced both the V4 regions of 16S rRNA genes and full metagenomes, resulting in 610 Mb of 16S rRNA gene data and 198.98 Gb of high-quality metagenomic data. We observed that two cyanobacteria genera (Microcystis and Dolichospermum) alternately dominated CAs along the sampling time and specific bacterial genera attached to different cyanobacteria genera dominated CAs. More specifically, Dolichospermum dominates CAs when water temperature is low and total nitrogen is high, while Microcystis dominates CAs when water temperature is high and total nitrogen is low. Moreover, we found specific bacterial genera attached to different cyanobacteria genera dominated CAs. The cyanobacteria-bacteria related pairs Dolichospermum-Burkholderia and Microcystis-Hyphomonas were detected by ecological networks construction. Bacterial communities in CAs were found to be more correlated with the cyanobacterial community (Mantel's r = 0.76, P = 0.001) than with environmental factors (Mantel's r = 0.27, P = 0.017). A potential codependent nitrogen-cycling pathway between cyanobacteria and their attached bacteria was constructed, indicating their functional link. Overall, these results demonstrated that mutualistic relationships do, indeed, exist between cyanobacteria and bacteria in CAs at both taxonomic and gene levels, providing biological clues potentially leading to the control of blooms by interventional strategies to disrupt bacteria-cyanobacteria relationships and co-pathways.