In this NSF's Rule of Life funded project, we sampled the Virgin River in Zion’s National Park in 2021 and 2023 in which a dog was reported to potentially succumb to death after swallowing benthic mats. .Our extensive sampling, followed by deep metagenomics and metatranscriptomics, revealed the presence of the toxic genus Microcoleus in these mats. The presence of Microcoleus has been recorded in New Zealand, Switzerland, Australia, and other countries. This genus exhibits unusual ecophysiology, and we uncovered some of its adaptations. For instance, we found that Microcoleus employs the pho regulon, including the expression of pstS and alkaline phosphatase genes, to adapt to phosphorus limitation and efficiently acquire phosphorus in low-nutrient environments. However, this genus lacks nitrogen-fixing genes, making it important to understand how Microcoleus thrives in nitrogen-limited environments like the Virgin River. We found that this genus takes help from other nitrogen-fixing genera coexisting bacteria contributing to nitrogen fixation (nif) and assimilation, and denitrification (nosZ, nir, and nar genes) in toxic benthic mats. A Microcoleus metagenome-assembled genome (MAG), Microcoleus_ZNC_2, was phylogenetically classified as Microcoleus anatoxicus and harbored an anatoxin-a gene cluster but lacked the anaK gene, potentially limiting dihydroanatoxin-a production. Other toxic genera, such as Oscillatoria and Pseudoanabaena, co-occurred with Microcoleus, thriving under nutrient-limited conditions, which underscores their adaptability and risks to human and animal health. We are also developing a time series model to predict the occurrence of toxic benthic mats in U.S. waters. Our deep omics provided important insights into how the toxic Microcoleus grows in shallow streams under nutrient limitations, the toxin gene cluster and their expressions, its synergism with other heterotrophic bacteria, and its ecophysiology. It emphasizes the significance of integrated molecular approaches to unravel nutrient cycling dynamics and toxin production within benthic cyanobacterial mats. These insights are critical for understanding and managing harmful cyanobacterial blooms in freshwater ecosystems.