Short-term toxicity assessment of a triazine herbicide (terbutryn) underestimates the sensitivity of soil microorganisms

doi:10.1016/j.soilbio.2021.108130

Soil Biology and Biochemistry

Volume 154, March 2021, 108130

https://doi.org/10.1016/j.soilbio.2021.108130 Get rights and content

Highlights

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Microbial toxicity was studied in soil spiked with a herbicide (terbutryn).
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Bacterial and fungal growth were more sensitive endpoints than soil respiration.
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Time-cumulative microbial growth inhibition was observed over 40 days.
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Current ecotoxicological guidelines may underestimate risks posed by chemicals.

Abstract

Little is known about the impacts of persistent triazine herbicides and biocides on soil microorganisms. Terbutryn toxicity in soil microorganisms was studied using bacterial and fungal growth, substrate induced respiration (SIR) and basal respiration as ecotoxicological end-points. In the short-term (0–7 days), increasing concentrations of terbutryn (0–800 mg kg⁻¹) progressively inhibited bacterial and fungal growth by up to 33–36% (4 h) and 49–55% (7 days), whereas SIR and basal soil respiration remained unaffected. Following long-term (40 days) exposure to terbutryn, both bacterial and fungal growth were inhibited by up to 76–78%, and SIR was inhibited by up to 53%. Hence, our results unexpectedly demonstrate time-cumulative microbial growth inhibition over extended time periods in soil and indicate that current ecotoxicological guidelines may underestimate risks posed by chemicals to soil microorganisms.

Section snippets

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The authors acknowledge funding obtained from the Danish Environmental Protection Agency (Project 667-00103). David Fernández Calviño holds a Ramón y Cajal contract (RYC-2016-20411) financed by the Spanish Ministry of Economy, Industry and Competitiveness.

References (23)

K.K. Brandt et al.
Ecotoxicological assessment of antibiotics: a call for improved consideration of microorganisms
Environment International
(2015)
M. Broser et al.
Structural basis of cyanobacterial photosystem II inhibition by the herbicide terbutryn
Journal of Biological Chemistry
(2011)
D. DeZwart et al.
The Microtox as an alternative assay in the acute toxicity assessment of water pollutants
Aquatic Toxicology
(1983)
D. Fernández-Calviño et al.
Ecotoxicological assessment of propiconazole using soil bacterial and fungal growth assays
Applied Soil Ecology
(2017)
G. Imfeld et al.
Measuring the effects of pesticides on bacterial communities in soil: a critical review
European Journal of Soil Biology
(2012)
S. Kresmann et al.
Ecotoxicological potential of the biocides terbutryn, octhilinone and methylisothiazolinone: underestimated risk from biocidal pathways?
The Science of the Total Environment
(2018)
V. Santás-Miguel et al.
Interactions between soil properties and tetracycline toxicity affecting to bacterial community growth in agricultural soil
Applied Soil Ecology
(2020)
C. Thiour-Mauprivez et al.
Effects of herbicide on non-target microorganisms: towards a new class of biomarkers?
The Science of the Total Environment
(2019)
M. Alexander
Aging, bioavailability, and overestimation of risk from environmental pollutants
Environmental Science and Technology
(2000)
U.E. Bollmann et al.
Biocide runoff from building facades: degradation kinetics in soil
Environmental Science and Technology
(2017)

K.K. Brandt et al.

Increased pollution-induced bacterial community tolerance to sulfadiazine in soil hotspots amended with artificial root exudates

Environmental Science and Technology

(2009)

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Citation Excerpt :
At the later stage of the incubation, the IBRv2 values have been reduced, implying the combined toxic effect of herbicides was weakened. A decrease in the inhibition rate of soil enzyme activities was observed, probably because organic pollutants usually become less toxic over time due to reduced bioavailability (degradation) or microbial community-level adaptation leading to development of pollution-induced community tolerance (Fernández-Calviño et al., 2021). Obvious synergistic effects by the combined application of ATZ and ACE were observed for the type of infraction of urease and catalase, indicating that the negative effects of mixture of ATZ and ACE on soil enzymes were not simply additive, whose toxic effect is stronger.
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2022, Environmental Research
Citation Excerpt :
Finally, it can be observed that TMP toxicity increases with incubation time, that is, the toxicity exerted by TMP on soil bacterial communities at day 1 (direct toxicity) is lower than that observed at day 42 of incubation (soils 3 and 4 are examples of this). The increase in toxicity over time is a phenomenon scarcely observed for antibiotics and other environmental pollutants; however, there are studies focused on antibiotics, such as sulfadiazine (Santás-Miguel et al., 2020d), as well as on pesticides, such as terbutryn (Fernández-Calviño et al., 2021), where it was shown that their toxicities on soil bacterial communities increased with incubation time. This may be because antibiotics that show high persistence in soils, such as TMP, may be more susceptible to mineralization over time (Kim et al., 2004; Bouju et al., 2012), becoming more bioavailable to soil microorganisms, and this higher bioavailability would make them more toxic.
The presence of emerging pollutants, and specifically antibiotics, in agricultural soils has increased notably in recent decades, causing growing concern as regards potential environmental and health issues. With this in mind, the current study focuses on evaluating the toxicity exerted by three antibiotics (amoxicillin, trimethoprim, and ciprofloxacin) on the growth of soil bacterial communities, when these pollutants are present at different doses, and considered in the short, medium, and long terms (1, 8 and 42 days of incubation). Specifically, the research was carried out in 12 agricultural soils having different physicochemical characteristics and was performed by means of the leucine (³H) incorporation method. In addition, changes in the structure of soil microbial communities at 8 and 42 days were studied in four of these soils, using the phospholipids of fatty acids method for this. The main results indicate that the most toxic antibiotic was amoxicillin, followed by trimethoprim and ciprofloxacin. The results also show that the toxicity of amoxicillin decreases with time, with values of Log IC₅₀ ranging from 0.07 ± 0.05 to 3.43 ± 0.08 for day 1, from 0.95 ± 0.07 to 3.97 ± 0.15 for day 8, and from 2.05 ± 0.03 to 3.18 ± 0.04 for day 42, during the incubation period. Regarding trimethoprim, 3 different behaviors were observed: for some soils the growth of soil bacterial communities was not affected, for a second group of soils trimethoprim toxicity showed dose-response effects that remained persistent over time, and, finally, for a third group of soils the toxicity of trimethoprim increased over time, being greater for longer incubation times (42 days). As regards ciprofloxacin, this antibiotic did not show a toxicity effect on the growth of soil bacterial communities for any of the soils or incubation times studied. Furthermore, the principal component analysis performed with the phospholipids of fatty acids results demonstrated that the microbial community structure of these agricultural soils, which persisted after 42 days of incubation, depended mainly on soil characteristics and, to a lesser extent, on the dose and type of antibiotic (amoxicillin, trimethoprim or ciprofloxacin). In addition, it was found that, in this research, the application of the three antibiotics to soils usually favored the presence of fungi and Gram-positive bacteria.

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Short CommunicationShort-term toxicity assessment of a triazine herbicide (terbutryn) underestimates the sensitivity of soil microorganisms

Highlights

Abstract

Section snippets

Declaration of competing interest

Acknowledgements

Environment International

Journal of Biological Chemistry

Aquatic Toxicology

Applied Soil Ecology

European Journal of Soil Biology

The Science of the Total Environment

Applied Soil Ecology

The Science of the Total Environment

Aging, bioavailability, and overestimation of risk from environmental pollutants

Environmental Science and Technology

Biocide runoff from building facades: degradation kinetics in soil

Environmental Science and Technology

Increased pollution-induced bacterial community tolerance to sulfadiazine in soil hotspots amended with artificial root exudates

Environmental Science and Technology

Short Communication
Short-term toxicity assessment of a triazine herbicide (terbutryn) underestimates the sensitivity of soil microorganisms