The influence of natural dissolved organic matter on herbicide toxicity to marine microalgae is species-dependent

Abstract

Microalgae, which are the foundation of aquatic food webs, may be the indirect target of herbicides used for agricultural and urban applications. Microalgae also interact with other compounds from their environment, such as natural dissolved organic matter (DOM), which can itself interact with herbicides. This study aimed to evaluate the influence of natural DOM on the toxicity of three herbicides (diuron, irgarol and S-metolachlor), singly and in ternary mixtures, to two marine microalgae, Chaetoceros calcitrans and Tetraselmis suecica, in monospecific, non-axenic cultures. Effects on growth, photosynthetic efficiency (Ф') and relative lipid content were evaluated. The chemical environment (herbicide and nutrient concentrations, dissolved organic carbon and DOM optical properties) was also monitored to assess any changes during the experiments. The results show that, without DOM, the highest irgarol concentration (I0.5: 0.5 mg.L) and the strongest mixture (M2: irgarol 0.5 μg.L + diuron 0.5 μg.L + S-metolachlor 5.0 μg.L) significantly decreased all parameters for both species. Similar impacts were induced by I0.5 and M2 in C. calcitrans (around -56% for growth, -50% for relative lipid content and -28% for Ф'), but a significantly higher toxicity of M2 was observed in T. suecica (-56% and -62% with I0.5 and M2 for growth, respectively), suggesting a possible interaction between molecules. With DOM added to the culture media, a significant inhibition of these three parameters was also observed with I0.5 and M2 for both species. Furthermore, DOM modulated herbicide toxicity, which was decreased for C. calcitrans (-51% growth at I0.5 and M2) and increased for T. suecica (-64% and -75% growth at I0.5 and M2, respectively). In addition to the direct and/or indirect (via their associated bacteria) use of molecules present in natural DOM, the characterization of the chemical environment showed that the toxic effects observed on microalgae were accompanied by modifications of DOM composition and the quantity of dissolved organic carbon excreted and/or secreted by microorganisms. This toxicity modulation in presence of DOM could be explained by (i) the modification of herbicide bioavailability, (ii) a difference in cell wall composition between the two species, and/or (iii) a higher detoxification capacity of C. calcitrans by the use of molecules contained in DOM. This study therefore demonstrated, for the first time, the major modulating role of natural DOM on the toxicity of herbicides to marine microalgae.

Dissolved organic matter modulates the impact of herbicides on a freshwater alga: A laboratory study of a three-way interaction

“…However, studies exploring the influence of natural DOM, which is a major component in aquatic environments, on potential interactions between pesticides and microalgae are scarce (e.g. Nikkilä et al, 2001;Coquillé et al, 2018).…”

Impacts of chemical contamination on bacterio-phytoplankton coupling

“…The contaminants cocktail was designed from the main compounds identified and analysed in sediment elutriate (Table S1, supplementary materials) in order to assess the toxic effects of these contaminants without confounding chemical factors, nutrients and/or dissolved organic matter that are released during sediment resuspension (Pringault et al, 2016). Nutrients and organic matter are known to strongly mitigate the toxicity of pesticides and TME against microorganisms, mainly attributed to a decrease of contaminant bioavailability by adsorption on dissolved organic matter (Boyd et al, 2005;Coquillé et al, 2018;Lorenzo et al, 2002) and changes in the nutrient status, toxicity increasing under nutrient limitation (Chia et al, 2016;Miao and Wang, 2006). For offshore waters, spiking with pesticides and MTE resulted in an inhibition of phytoplankton biomass as well as a reduction of metabolic activities involved in the carbon cycle (PP and BCD).…”

Seasonal changes of chemical contamination in coastal waters during sediment resuspension

“…Nevertheless, the concomitant release of nutrients and dissolved organic matter with toxic compounds (pesticides and trace metal elements) upon sediment resuspension can alleviate the potential toxicity of the toxic elements (Pringault et al, 2016), nutrients and organic matter are known to decrease the toxicity of trace metal elements (Anu et al, 2018;Huang et al, 2016) or pesticides for phytoplankton (Chia et al, 2016;Coquillé et al, 2018). The structure and diversity of phytoplankton (Lafabrie et al, 2013) and bacterioplankton (Pringault et al, 2016) can be strongly impacted by sediment resuspension in shallow waters with significant consequences on the primary production as well on the microbial biomass (Ding et al, 2017;McSweeney et al, 2017;Pringault et al, 2016).…”