Temporal and spatial dynamics of harmful algal bloom-associated microbial communities in eutrophic Clear Lake, California

Clear Lake is a large, natural eutrophic lake located in northern California, United States. Persistent, toxic cyanobacterial blooms have been reported in the lake since 2011. However, our understanding of the spatiotemporal distribution of toxin-producing genera and their interaction with the biotic and abiotic environment is limited. Moreover, few studies have addressed how the co-occurring microbial communities respond to these toxic cyanobacterial blooms. Using multi-domain 16S/18S rRNA gene amplicon sequencing, a strong seasonal succession within the cyanobacterial and co-occurring eukaryotic assemblage was identified, which was primarily explained by variation in total phosphorus (~30%, <i>P</i> < 0.001) and temperature (~15%, <i>P</i> < 0.01). Cyanobacterial seasonal succession was often initiated by proliferation of diazotrophs (<i>Dolichospermum</i> and <i>Nodularia</i>) with concomitant increases in total nitrogen, followed by blooms of non-diazotrophs, such as <i>Microcystis, Limnothrix,</i> and <i>Planktothrix</i>. The picocyanobacterium <i>Cyanobium</i>, previously undocumented in the lake, was a dominant summer taxon in the western part of Clear Lake, accounting for ~45%-80% relative abundance of the cyanobacterial reads. Seasonal succession within the eukaryotic assemblage was influenced by photosynthetic chlorophytes and diatoms, as well as mixotrophic ciliates and cryptophytes. Among all toxin-producing cyanobacterial genera, <i>Microcystis</i> abundance was most strongly correlated with microcystin concentrations (<i>P</i> < 0.001), both of which appeared to influence co-occurring eukaryotes. Finally, using putative relationships based on correlation of sequence abundance and environmental variables, several potential grazers of <i>Microcystis</i> were identified, including cyclopoid copepods and <i>Cryptomonas</i>. These correlations need further confirmation and experimental work to validate the nature of the relationships.IMPORTANCEClear Lake is an important habitat for fish and wildlife, which also provides a myriad of human benefits, such as recreation, irrigation, and drinking water. Moreover, the lake is vital for tribal tradition and cultural practices. However, since the last decade, the lake has experienced recurring harmful algal blooms with toxin levels that frequently exceed California voluntary guidance levels. These high toxin concentrations pose a substantial threat to the residents, visitors, and tribal sustenance fishing and beneficial uses. However, significant gaps remain in our understanding of these toxic algal bloom dynamics and their interaction with the abiotic and biotic environments. This study characterized the seasonal and spatial patterns in the distribution of bloom-causing cyanobacteria and identified <i>Microcystis</i> as the major toxin producer in Clear Lake. Additionally, the co-occurring bacterial and eukaryotic microbial communities were also characterized, and their potential interactions with the cyanobacterial assemblage were identified and discussed.