Impacts of microbial assemblage and environmental conditions on the distribution of anatoxin-a producing cyanobacteria within a river network

Keith Bouma-Gregson,Mary E Power,Matthew R Olm,Karthik Anantharaman,Jillian F Banfield,Alexander J Probst

doi:10.1038/s41396-019-0374-3

Abstract

Blooms of planktonic cyanobacteria have long been of concern in lakes, but more recently, harmful impacts of riverine benthic cyanobacterial mats been recognized. As yet, we know little about how various benthic cyanobacteria are distributed in river networks, or how environmental conditions or other associated microbes in their consortia affect their biosynthetic capacities. We performed metagenomic sequencing for 22 Oscillatoriales-dominated (Cyanobacteria) microbial mats collected across the Eel River network in Northern California and investigated factors associated with anatoxin-a producing cyanobacteria. All microbial communities were dominated by one or two cyanobacterial species, so the key mat metabolisms involve oxygenic photosynthesis and carbon oxidation. Only a few metabolisms fueled the growth of the mat communities, with little evidence for anaerobic metabolic pathways. We genomically defined four cyanobacterial species, all which shared <96% average nucleotide identity with reference Oscillatoriales genomes and are potentially novel species in the genus Microcoleus. One of the Microcoleus species contained the anatoxin-a biosynthesis genes, and we describe the first anatoxin-a gene cluster from the Microcoleus clade within Oscillatoriales. Occurrence of these four Microcoleus species in the watershed was correlated with total dissolved nitrogen and phosphorus concentrations, and the species that contains the anatoxin-a gene cluster was found in sites with higher nitrogen concentrations. Microbial assemblages in mat samples with the anatoxin-a gene cluster consistently had a lower abundance of Burkholderiales (Betaproteobacteria) species than did mats without the anatoxin-producing genes. The associations of water nutrient concentrations and certain co-occurring microbes with anatoxin-a producing Microcoleus motivate further exploration for their roles as potential controls on the distributions of toxigenic benthic cyanobacteria in river networks.

Highlights

IntroductionNuisance benthic cyanobacterial mats in rivers have been documented across the globe, including New Zealand [7, 8], California [9, 10], France [5], and Spain [11]
Supplementary information The online version of this article contains supplementary material, which is available to authorized users.When cyanobacteria proliferate in freshwaters, their toxins can threaten water quality and public health [1]
Nuisance benthic cyanobacterial mats in rivers have been documented across the globe, including New Zealand [7, 8], California [9, 10], France [5], and Spain [11]

Summary

Introduction

Nuisance benthic cyanobacterial mats in rivers have been documented across the globe, including New Zealand [7, 8], California [9, 10], France [5], and Spain [11]. Benthic mats are often formed by filamentous genera such as Anabaena, Phormidium, Microcoleus, Nodularia, Lyngbya, or Oscillatoria, which sometimes produce cyanotoxins such as anatoxin-a, microcystins, saxitoxin, and lyngbyatoxin [3]. Cyanobacterial blooms in lakes and estuaries are predicted to increase due to eutrophication and climate warming [12, 13], and more study of riverine benthic cyanobacterial mats is needed to anticipate environmental and ecological triggers of toxigenic cyanobacterial blooms in rivers

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