Widespread anatoxin-a detection in benthic cyanobacterial mats throughout a river network

Abstract

Benthic algae fuel summer food webs in many sunlit rivers, and are hotspots for primary and secondary production and biogeochemical cycling. Concerningly, riverine benthic algal assemblages can become dominated by toxic cyanobacteria, threatening water quality and public health. In the Eel River in Northern California, over a dozen dog deaths have been attributed to cyanotoxin poisonings since 2000. During the summers of 2013–2015, we documented spatial and temporal patterns of cyanotoxin concentrations in the watershed, showing widespread distribution of anatoxin-a in benthic cyanobacterial mats. Solid phase adsorption toxin tracking (SPATT) samplers were deployed weekly to record dissolved microcystin and anatoxin-a levels at 10 sites throughout the watershed, and 187 Anabaena-dominated or Phormidium-dominated cyanobacterial mat samples were collected from 27 locations to measure intracellular anatoxin-a (ATX) and microcystins (MCY). Anatoxin-a levels were higher than microcystin for both SPATT (mean MCY = 0.8 and ATX = 4.8 ng g resin-1 day-1) and cyanobacterial mat samples (mean MCY = 0.074 and ATX = 1.89 μg g-1 DW). Of the benthic mats sampled, 58.9% had detectable anatoxin-a (max = 70.93 μg g-1 DW), while 37.6% had detectable microcystins (max = 2.29 μg g-1 DW). SPATT cyanotoxin levels peaked in mid-summer in warm mainstem reaches of the watershed. This is one of the first documentations of widespread anatoxin-a occurrence in benthic cyanobacterial mats in a North American watershed.

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

“…The concentrations of anatoxins, NOD-R and MCYs were consistent with data in previous studies from these sites [16, 28], with anatoxin concentrations five times greater than microcystin/nodularin concentrations. Solid-phase adsorption toxin tracking samplers (SPATTs) in the Eel River accumulated ATX and MCYs in 53% – 54% and 41% – 76% of samples for each toxin, respectively [16].…”

“…The concentrations of anatoxins, NOD-R and MCYs were consistent with data in previous studies from these sites [16, 28], with anatoxin concentrations five times greater than microcystin/nodularin concentrations. Solid-phase adsorption toxin tracking samplers (SPATTs) in the Eel River accumulated ATX and MCYs in 53% – 54% and 41% – 76% of samples for each toxin, respectively [16]. The site with the highest concentrations of both anatoxins and NOD-R was dominated by Anabaena , a finding that contrasts with that of Bouma-Gregson et al [16], who found no differences in ATX concentrations between Anabaena and Microcoleus dominated mats, although the authors only measured ATX, not dhATX so may have underestimated the total anatoxin concentrations.…”

“…This is consistent with results from Anabaena cultures isolated, and Anabaena draft-genomes assembled from the Eel and Russian rivers (unpublished observations; K.B.G.). This study detected the anaC gene at sites where Bouma-Gregson et al [18] did not find anatoxin biosynthesis gene clusters in their metagenomes; however our results correspond with previous anatoxin detections in the upper reaches of the Eel watershed [16]. Bouma-Gregson et al [18] found that only one of four Microcoleus strains detected in the metagenomes contained the anatoxin biosynthesis gene cluster.…”

“…Recently toxic benthic cyanobacteria have been recorded in Californian streams (Fetscher et al 2015; Bouma-Gregson et al 2018; Anderson et al 2018). Anatoxins, MCYs, NODs and CYNs have all been recorded in the mats and in samples collected using solid-phase absorption toxin tracking (SPATT) samplers [16, 17]. A number of sites on the Eel and Russian rivers in Northern California regularly experience benthic cyanobacterial and chlorophyte proliferations [16].…”

Toxicity, transfer and depuration of anatoxin-a (cyanobacterial neurotoxin) in medaka fish exposed by single-dose gavage

“…Anatoxin-a and homoanatoxin-a are potent neurotoxins produced by some planktonic and benthic strains of the genera Anabaena, Oscillatoria, Aphanizomenon and Cylindrospermum (Bouma-Gerson et al, 2018). Indeed, numerous fatal intoxications of animals, by anatoxin-a and homoanatoxin-a, have been reported all over the world (Gugger et al, 2005; Puschner et al, 2010; Wood et al, 2007).…”