Tools for successful proliferation: diverse strategies of nutrient acquisition by a benthic cyanobacterium

Freshwater cyanobacterial blooms have increased worldwide, channeling organic carbon into these systems, and threatening animal health through the production of cyanotoxins. Both toxic and nontoxic Microcoleus proliferations usually occur when there are moderate concentrations of dissolved inorganic nitrogen, but when phosphorus is scarce. In order to understand how Microcoleus establishes thick biofilms (or mats) on riverbeds under phosphorus-limiting conditions, we collected Microcoleus-dominated biofilms over a 19-day proliferation event for proteogenomics. A single pair of nitrogen-dependent Microcoleus species were consistently present in relatively high abundance, although each followed a unique metabolic trajectory. Neither possessed anatoxin gene clusters, and only very low concentrations of anatoxins (~2 µg kg^-1) were detected, likely originating from rarer Microcoleus species also present. Proteome allocations were dominated by photosynthesizing cyanobacteria and diatoms, and data indicate biomass was actively recycled by Bacteroidetes and Myxococcales. Microcoleus likely acquired nutrients throughout the proliferation event by uptake of nitrate, urea, and inorganic and organic phosphorus. Both species also harbored genes that could be used for inorganic phosphate solubilization with pyrroloquinoline quinone cofactors produced by cohabiting Proteobacteria. Results indicate that Microcoleus are equipped with diverse mechanisms for nitrogen and phosphorus acquisition, enabling them to proliferate and out-compete others in low-phosphorus waters.