Microbial diversity and physicochemistry of an estuarine phototrophic bloom in the Trunk River, Wood Hole (MA)

Organic-rich, brackish water bodies are common along coastlines and important for the biogeochemical cycling of carbon, nitrogen, sulfur, and phosphorus. These ecosystems are dynamic and frequently disturbed by weather, tides, erosion, and human activities. Here, we investigated a shallow, brackish lagoon (Trunk River, Woods Hole, MA) that contains layers of decaying organic matter, which releases hydrogen sulfide upon physical disturbance. To study the microbial habitat and community response to perturbations, we carried out replicated in situ experiments, analyzing the physicochemistry and microbial community succession. At each site, yellow blooms of microorganisms formed within three days after disturbance. The water column changed substantially, establishing steep gradients of temperature, oxygen, sulfide, and salinity. The diverse microbial community at early timepoints was replaced by a community largely dominated by a clonal population of green sulfur bacteria (GSB) Prosthecochloris vibrioformis. Despite its dominance, this population coexisted with less abundant GSBs affiliating with Chlorobaculum. This population represents a new Chlorobaculum species, as indicated by phylogenetic and phylogenomic placement, ANI values, and CRISPR-Cas genes. Interestingly, despite their dominance the GSB coexisted with purple sulfur bacteria (Halochromatium sp. and Allochromatium sp.), anoxygenic phototrophic Chloroflexi (Chloroploca sp.) and other phototrophs. A high relative sequence abundance of Microviridae viruses was found in the metagenome, indicating their activity in the bloom. After two weeks the bloom subsided and the ecosystem slowly returned towards a diverse state and ecosystem functions, indicating its resilience after disturbance. This work provides insights into the assembly, succession, and coexistence of oxygenic and anoxygenic phototrophs in a common coastal ecosystem. The transient bloom was spatially structured analogous to a phototrophic microbial mat with distinct ecological niches for multiple clades of Cyanobacteria, purple and green sulfur bacteria. We suggest that a cryptic sulfur cycle in the water column between sulfur-oxidizing phototrophs, sulfate reducers, and sulfur oxidizers enhanced the development of the bloom. The bloom was likely driven by new species in the order Chlorobiales and possibly impacted by viruses of the family Microviridae.