Microbial diversity and metabolic potential in cyanotoxin producing cyanobacterial mats throughout a river network

Abstract

Microbial mats formed by Cyanobacteria of the genus Phormidium produce the neurotoxin anatoxin-a that has been linked to animal deaths. Blooms of planktonic Cyanobacteria have long been of concern in lakes, but recognition of potential harmful impacts of riverine benthic cyanobacterial mats is more recent. Consequently little is known about the diversity of the biosynthetic capacities of cyanobacterial species and associated microbes in mats throughout river networks. Here we performed metagenomic sequencing for 22 Phormidium-dominated microbial mats collected across the Eel River network in Northern California to investigate cyanobacterial and co-occurring microbial assemblage diversity, probe their metabolic potential and evaluate their capacities for toxin production. We genomically defined four Cyanobacterial species clusters that occur throughout the river network, three of which have not been described previously. From the genomes of seven strains from one species group we describe the first anatoxin-a operon from the genus Phormidium. Community composition within the mat appears to be associated with the presence of Cyanobacteria capable of producing anatoxin-a. Bacteroidetes, Proteobacteria, and novel Verrucomicrobia dominated the microbial assemblages. Interestingly, some mats also contained organisms from candidate phyla such as Canditatus Kapabacteria, as well as Absconditabacteria (SR1), Parcubacteria (OD1) and Peregrinibacteria (PER) within the Candidate Phyla Radiation. Oxygenic photosynthesis and carbon respiration were the most common metabolisms detected in mats but other metabolic capacities include aerobic anoxygenic photosynthesis, sulfur compound oxidation and breakdown of urea. The results reveal the diversity of metabolisms fueling the growth of mats, and a relationship between microbial assemblage composition and the distribution of anatoxin-a producing cyanobacteria within freshwater Phormidium mats in river networks.

Rapid Changes in Microbial Community Structures along a Meandering River

“…A decrease in the abundance of lineages could also be explained by the absence of these lineages at the water sampling depth (15 cm below the surface) and could reveal a resettlement of these microorganisms. In response to environmental changes, some microorganisms could form microbial mats, which is an organization often observed in riverine cyanobacterial lineages [ 53 , 54 , 55 ], and resettle at the river bed or on the surface of macro-algae.…”

Spatial and Temporal Variation in Paralytic Shellfish Toxin Production by Benthic Microseira (Lyngbya) wollei in a Freshwater New York Lake

“…The source of anatoxin-a was uncertain. While Anabaena and Phormidium species were associated with anatoxin-a production in wadeable streams in California and New Zealand [46,47,48], these genera were not observed during microscopic examination of the cyanobacterial mats from Butterfield Lake. These and/or other anatoxin-a producing benthic cyanobacteria may have been present in the mat in small quantities and could account for the low levels of anatoxin-a.…”

“…The environmental drivers of M. wollei PSTs were interesting in the context of freshwater pelagic blooms, where pelagic bloom size is closely related to phosphorus, while microcystins and anatoxin-a content is more closely related to nitrogen availability [59,60,61,62,63] and genetic factors [64]. The drivers of benthic toxin production may not be the same as those for pelagic cyanobacteria, with genetic factors, physical parameters, and nutrient parameters all playing important roles [47,65]. This neglects the important role sediments play as a source of nutrients to the cyanobacteria.…”

Reviewing Interspecies Interactions as a Driving Force Affecting the Community Structure in Lakes via Cyanotoxins

“…The diversity of the bacterial community assemblage associated with benthic neurotoxin-producer dominated mats has been reported in recent studies. In the Eel River (Northern California, U.S.), the microbial assemblage within benthic ATX-producing and -deficient Phormidium mats were found to differ substantially [ 137 ]. The microbial community related to ATX-producing species was dominated by Bacteroidetes, Proteobacteria and Verrucomicrobia.…”