Multiple cyanotoxin congeners produced by sub-dominant cyanobacterial taxa in riverine cyanobacterial and algal mats

PLoS One. 2019 Dec 16;14(12):e0220422. doi: 10.1371/journal.pone.0220422. eCollection 2019.

Abstract

Benthic cyanobacterial proliferations in rivers are have been reported with increasing frequency worldwide. In the Eel and Russian rivers of California, more than a dozen dog deaths have been attributed to cyanotoxin toxicosis since 2000. Periphyton proliferations in these rivers comprise multiple cyanobacterial taxa capable of cyanotoxin production, hence there is uncertainty regarding which taxa are producing toxins. In this study, periphyton samples dominated by the cyanobacterial genera Anabaena spp. and Microcoleus spp. and the green alga Cladophora glomerata were collected from four sites in the Eel River catchment and one site in the Russian River. Samples were analysed for potential cyanotoxin producers using polymerase chain reaction (PCR) in concert with Sanger sequencing. Cyanotoxin concentrations were measured using liquid chromatography tandem-mass spectrometry, and anatoxin quota (the amount of cyanobacterial anatoxins per toxigenic cell) determined using droplet digital PCR. Sequencing indicated Microcoleus sp. and Nodularia sp. were the putative producers of cyanobacterial anatoxins and nodularins, respectively, regardless of the dominant taxa in the mat. Anatoxin concentrations in the mat samples varied from 0.1 to 18.6 μg g-1 and were significantly different among sites (p < 0.01, Wilcoxon test); however, anatoxin quotas were less variable (< 5-fold). Dihydroanatoxin-a was generally the most abundant variant in samples comprising 38% to 71% of the total anatoxins measured. Mats dominated by the green alga C. glomerata contained both anatoxins and nodularin-R at concentrations similar to those of cyanobacteria-dominated mats. This highlights that even when cyanobacteria are not the dominant taxa in periphyton, these mats may still pose a serious health risk and indicates that more widespread monitoring of all mats in a river are necessary.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anabaena / pathogenicity
  • Bacterial Toxins / analysis*
  • California
  • Chlorophyta / genetics
  • Chlorophyta / metabolism
  • Chromatography, Liquid
  • Cyanobacteria / genetics
  • Cyanobacteria / metabolism
  • Cyanobacteria / pathogenicity*
  • Polymerase Chain Reaction
  • Proline / analogs & derivatives
  • Proline / analysis
  • Rivers / chemistry*
  • Water Microbiology

Substances

  • Bacterial Toxins
  • dihydroanatoxin-A
  • Proline

Grants and funding

L.T.K., S.A.W., J.P., T.W.D. and K.B.G. acknowledge funding for this study from the Troubled Waters Catalyst Seeding Grant from the Royal Society of New Zealand. K.G.R and L.T.K. were supported by Victoria University of Wellington grant 80837. S.A.W. acknowledges funding to support her time on this study from the National Institute of Water and Atmospheric Research Ltd. under the causes and effects of water quality degradation: eutrophication risk assessment programme. J.P. acknowledges funding from the Marsden Fund of the Royal Society of New Zealand (CAW1601, Blooming Buddies) to support his time on this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.