Metagenomics reveals spatial variation in cyanobacterial composition, function, and biosynthetic potential in the Winam Gulf, Lake Victoria, Kenya

Abstract

The Winam Gulf in the Kenyan region of Lake Victoria experiences prolific, year-round cyanobacterial harmful algal blooms (cyanoHABs) which pose threats to human, livestock, and ecosystem health. To our knowledge, there is limited molecular research on the gulf's cyanoHABs, and thus, the strategies employed for survival and proliferation by toxigenic cyanobacteria in this region remain largely unexplored. Here, we used metagenomics to analyze the Winam Gulf's cyanobacterial composition, function, and biosynthetic potential. <i>Dolichospermum</i> was the dominant bloom-forming cyanobacterium, co-occurring with <i>Microcystis</i> at most sites. <i>Microcystis</i> and <i>Planktothrix</i> were more abundant in shallow and turbid sites. Metagenome-assembled genomes (MAGs) of <i>Dolichospermum</i> harbored nitrogen fixation genes, suggesting diazotrophy as a potential mechanism supporting the proliferation of <i>Dolichospermum</i> in the nitrogen-limited gulf. Over 300 biosynthetic gene clusters (BGCs) putatively encoding the synthesis of toxins and other secondary metabolites were identified across the gulf, even at sites where there were no visible cyanoHAB events. Almost all BGCs identified had no known synthesis product, indicating a diverse and novel biosynthetic repertoire capable of synthesizing harmful or potentially therapeutic metabolites. <i>Microcystis</i> MAGs contained <i>mcy</i> genes encoding the synthesis of hepatotoxic microcystins which are a concern for drinking water safety. These findings illustrate the spatial variation of bloom-forming cyanobacteria in the Winam Gulf and their available strategies to dominate different ecological niches. This study underscores the need for further use of genomic techniques to elucidate the dynamics and mitigate the potentially harmful effects of cyanoHABs and their associated toxins on human, environmental, and economic health.IMPORTANCEThe Winam Gulf (Kenya) is a vital resource that experiences prolific cyanobacterial harmful algal blooms (cyanoHABs). Bloom-forming cyanobacteria produce cyanotoxins, threatening human and environmental health, recreation, and fishing. However, cyanotoxin production in the gulf has not been linked to a specific type of cyanobacteria. We used DNA sequencing of whole microbial communities to track the species of cyanobacteria present across the gulf and investigate the genes responsible for synthesis of known and novel toxins. Our results reveal <i>Dolichospermum</i> as the main bloom-forming cyanobacteria in the gulf, often co-occurring with high abundance of toxigenic <i>Microcystis.</i> Over 300 unique gene clusters were found, with most predicted to encode the synthesis of uncharacterized molecules. These results provide initial insights into the diverse biosynthetic potential encoded by cyanobacteria in the Winam Gulf and underscore the need to further elucidate and investigate the effects of known and novel molecules produced in cyanoHABs in this region.