Abstract
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.
Highlights
Over the past few decades, the occurrence of freshwater cyanobacterial blooms has increased worldwide, and is associated with elevated water temperatures and nutrient enrichment [1,2,3]
Consistent with previous findings [15], the initial proliferation stage coincided with elevated dissolved inorganic nitrogen (DIN) and low dissolved reactive phosphorus (DRP) concentrations, both of which decreased over the sampling period (Fig. 1b, c)
While we predict that DRP was elevated within the sampled biofilms due to Pi liberation from trapped sediments under the high daytime pHs associated with photosynthetic activity [24], we found that both Microcoleus 1 and 2 expressed the high affinity, low velocity phosphate specific transporter system (Pst), while expression of the higher velocity PitA proteins were not detected
Summary
Over the past few decades, the occurrence of freshwater cyanobacterial blooms has increased worldwide, and is associated with elevated water temperatures and nutrient enrichment [1,2,3]. The overgrowth and decomposition of cyanobacterial cells drive excessive oxygen consumption in the aquatic environment [4], and some cyanobacteria produce cyanotoxins, which include potent neurotoxins, cytotoxins, hepatotoxins, and endotoxins [5]. All of these toxins represent a health risk to humans and animals.
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