Spatial and Temporal Variability in the Development and Potential Toxicity of Phormidium Biofilms in the Tarn River, France

Abstract

Proliferation of Phormidium biofilms in rivers is becoming a worldwide sanitation problem for humans and animals, due to the ability of these bacteria to produce anatoxins. To better understand the environmental conditions that favor the development of Phormidium biofilms and the production of anatoxins, we monitored the formation of these biofilms and their toxins for two years in the Tarn River, biofilms from which are known to have caused the deaths of multiple dogs. As previously observed in New Zealand, Phormidium biofilm development occurred in riffle areas. The coverage of these biofilms at the bottom of the river exhibited strong spatial and temporal variations, but was positively correlated with water temperature and depth. Anatoxin-a was detected in less than 50% of the biofilms. The concentrations of these toxins in the biofilms exhibited high spatiotemporal variability, with the highest concentrations being recorded at the end of the summer period at the upstream sampling sites. These findings suggest that the maturity of the biofilms, combined with the local environmental conditions, have an impact on the production of anatoxin, making risk assessment for these benthic proliferations challenging.

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

“…All samples were dominated by ATX and dhATX, and not HTX and dhHTX, which contrasts with observations elsewhere: dhATX, dhHTX and HTX typically dominate in New Zealand [8, 15], and in France ATX dominates [29], although dhATX has also been detected [30]. However, Anderson et al [19] used anatoxins in crude extracts of Microcoleus cultures isolated from the Russian river in their toxicological study and dhATX comprised > 99% of the anatoxins, demonstrating that there is likely large strain to strain variability in the variants produced.…”

Toxic benthic freshwater cyanobacterial proliferations: Challenges and solutions for enhancing knowledge and improving monitoring and mitigation

“…Loza, Berrendero, Perona, & Mateo, 2013; Loza, Perona, Carmona, & Mateo, 2013; Loza, Perona, & Mateo, 2013; Monteagudo & Moreno, 2016; Takano, Igarashi, Mikami, & Hino, 2003; Voorhies et al., 2012). Echenique‐Subiabre, Tenon, et al (2018) found that proliferations of Phormidium occurred with nitrate concentrations of 1.46 mg/L, whereas McAllister, Wood, Atalah, et al (2018) and Wood, Atalah, et al (2017) found that proliferations occurred when dissolved inorganic nitrogen concentrations were as low as 0.02 mg/L. Concentrations of dissolved reactive phosphorus in the water column below 0.05 mg/L have been shown to favour M. autumnalis proliferation over other periphyton in New Zealand streams (McAllister, Wood, Atalah, et al, 2018).…”

“…The general accrual cycle for benthic cyanobacteria typically involves: (1) initiation of a mat through colonisation by filaments or hormogonia that settle on a substrate, or regrowth of relic populations; (2) subsequent growth through increase in thickness, or lateral expansion; and (3) detachment of mats (Echenique‐Subiabre, Tenon, Humbert, & Quiblier, 2018; McAllister et al., 2016). After colonisation, the balance of growth‐ and loss‐promoting factors determines the length of the accrual cycle, and the size and persistence of the proliferation.…”

“…One of the most researched toxic benthic cyanobacteria is Microcoleus autumnalis (Gomont) Strunecky, Komárek & J.R.Johansen (basionym Phormidium autumnale ). This genus has become problematic worldwide (Bouma‐Gregson et al., 2018; Echenique‐Subiabre, Tenon, et al, 2018; McAllister et al., 2016). In the following analysis, we use our knowledge of M. autumnalis and the genus Phormidium to describe a generalised accrual cycle for benthic cyanobacteria proliferations.…”

“…Once a habitat has been colonised, physicochemical conditions strongly determine the growth and expansion rate of M. autumnalis and Phormidium proliferations. Current velocities between 0.3 and 0.8 m/s have been shown to favour M. autumnalis and Phormidium growth in streams (Echenique‐Subiabre, Tenon, et al, 2018; Hart, Biggs, Nikora, & Flinders, 2013; Heath et al., 2015; McAllister, Wood, Mackenzie, & Hawes, 2019). In experimental stream mesocosms, McAllister, Wood, Greenwood, Broghammer, and Hawes (2018) found that those with lower velocities (0.1 compared to 0.2 m/s) had less biomass accrual.…”