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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Physiological responses of the microalgae Thalassiosira weissflogii to the presence of the herbicide glyphosate in the medium

Ekaterina Solomonova https://orcid.org/0000-0001-5373-4954 A * , Natalia Shoman https://orcid.org/0000-0002-0924-1244 A and Arkady Akimov https://orcid.org/0000-0001-8583-1468 A
+ Author Affiliations
- Author Affiliations

A A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS, 2, Nakhimov Avenue, Sevastopol, Russian Federation.

* Correspondence to: solomonov83@mail.ru

Handling Editor: Vadim Demidchik

Functional Plant Biology 51, FP23205 https://doi.org/10.1071/FP23205
Submitted: 6 September 2023  Accepted: 7 April 2024  Published: 26 April 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

We evaluated changes in growth, chlorophyll fluorescence and basic physiological and biochemical parameters of the microalgae Thalassiosira weissflogii cells under the influence of the herbicide glyphosate in concentrations 0, 25, 95 and 150 μg L−1. The toxic effect of glyphosate on algae is weakly dependent on the level of cell mineral nutrition. High concentrations of the herbicide do not lead to the death of microalgae but block the process of algae cell division. An increase in the glyphosate concentration in the medium leads to a slowdown or stop of algal growth, a decrease in their final biomass, an increase in the production of reactive oxygen species (ROS), depolarisation of mitochondrial membranes and metabolic activity of algae. Glyphosate inhibits the photosynthetic activity of cells and inhibits the relative rate of electron transport in the photosynthetic apparatus. Glyphosate at the studied concentrations does not affect the size characteristics of cells and the intracellular content of chlorophyll in T. weissflogii. The studied herbicide or products of its decay retain their toxic properties in the environment for at least 9 days. This result shows the need for further in-depth studies to assess the physiological response and possible acclimation changes in the functional state of oxygenic phototrophs in response to the herbicide action. The species specificity of microalgae to the effects of glyphosate in natural conditions is potentially dangerous due to a possible change in the species structure of biocoenoses, in particular, a decrease in the contribution of diatoms.

Keywords: algae, ecotoxicology, flow cytometry, growth, herbicides toxicity, photosynthetic activity, plankton algae, pollution.

References

Ahsan N, Lee D-G, Lee K-W, Alam I, Lee S-H, Bahk JD, Lee B-H (2008) Glyphosate-induced oxidative stress in rice leaves revealed by proteomic approach. Plant Physiology and Biochemistry 46, 1062-1070.
| Crossref | Google Scholar | PubMed |

Akimov AI, Shoman NY, Solomonova ES (2019) Fluorescence characteristics of the diatom Cylindrotheca closterium (Ehrenberg) Reimann et Lewin, 1964. Marine Biological Journal 4, 89-92.
| Crossref | Google Scholar |

Aytan U, Valente A, Senturk Y, Usta R, Esensoy Sahin FB, Mazlum RE, Agirbas E (2016) First evaluation of neustonic microplastics in Black Sea waters. Marine Environmental Research 119, 22-30.
| Crossref | Google Scholar | PubMed |

Bai F, Liu R, Yang Y, Ran X, Shi J, Wu Z (2014) Dissolved organic phosphorus use by the invasive freshwater diazotroph cyanobacterium, Cylindrospermopsis raciborskii. Harmful Algae 39, 112-120.
| Crossref | Google Scholar |

Battaglin WA, Meyer MT, Kuivila KM, Dietze JE (2014) Glyphosate and its degradation product AMPA occur frequently and widely in U.S. soils, surface water, groundwater, and precipitation. JAWRA Journal of the American Water Resources Association 50, 275-290.
| Crossref | Google Scholar |

Borggaard OK, Gimsing AL (2008) Fate of glyphosate in soil and the possibility of leaching to ground and surface waters: a review. Pest Management Science 64, 441-456.
| Crossref | Google Scholar | PubMed |

Brito IP, Tropaldi L, Carbonari CA, Velini ED (2018) Hormetic effects of glyphosate on plants. Pest Management Science 74, 1064-1070.
| Crossref | Google Scholar | PubMed |

Calabrese EJ, Baldwin LA (2003) Hormesis at the National Toxicology Program (NTP): evidence of hormetic dose responses in NTP dose-range studies. Nonlinearity in Biology, Toxicology, Medicine 1, 15401420390271056.
| Crossref | Google Scholar |

Cerdeira AL, Duke SO (2006) The current status and environmental impacts of glyphosate-resistant crops: a review. Journal of Environmental Quality 35, 1633-1658.
| Crossref | Google Scholar | PubMed |

Cid A, Herrero C, Torres E, Abalde J (1995) Copper toxicity on the marine microalga Phaeodactylum tricornutum: effects on photosynthesis and related parameters. Aquatic Toxicology 31, 165-174.
| Crossref | Google Scholar |

Cobb AH, Reade JP (2010) The inhibition of amino acid biosynthesis. In ‘Herbicides and plant physiology’. 2nd edn. (Eds AH Cobb, JP Reade) pp. 176–199. (Wiley-Blackwell)

Cruz de Carvalho R, Feijão E, Matos AR, Cabrita MT, Novais SC, Lemos MF, et al. (2020) Glyphosate-based herbicide toxicophenomics in marine diatoms: impacts on primary production and physiological fitness. Applied Sciences 10, 7391.
| Crossref | Google Scholar |

Daboussi F, Leduc S, Maréchal A, Dubois G, Guyot V, Perez-Michaut C, et al. (2014) Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology. Nature Communications 5, 3831.
| Crossref | Google Scholar | PubMed |

Daouk S, Copin P-J, Rossi L, Chèvre N, Pfeifer H-R (2013) Dynamics and environmental risk assessment of the herbicide glyphosate and its metabolite AMPA in a small vineyard river of the Lake Geneva catchment. Environmental Toxicology and Chemistry 32, 2035-2044.
| Crossref | Google Scholar | PubMed |

Delpy F, Lucas Y, Merdy P (2022) Evaluation of Roundup® effects on Chlorella vulgaris through spectral changes in photosynthetic pigments in fresh and marine water. Environmental Advances 8, 100240.
| Crossref | Google Scholar |

Demmig-Adams B, Adams WW, III (2000) Harvesting sunlight safely. Nature 403, 371-373.
| Crossref | Google Scholar | PubMed |

Deryabina Y, Isakova E, Sekova V, Antipov A, Saris N-EL (2014) Inhibition of free radical scavenging enzymes affects mitochondrial membrane permeability transition during growth and aging of yeast cells. Journal of Bioenergetics and Biomembranes 46, 479-492.
| Crossref | Google Scholar | PubMed |

Dorsey J, Yentsch CM, Mayo S, McKenna C (1989) Rapid analytical technique for the assessment of cell metabolic activity in marine microalgae. Cytometry 10, 622-628.
| Crossref | Google Scholar | PubMed |

Forlani G, Pavan M, Gramek M, Kafarski P, Lipok J (2008) Biochemical bases for a widespread tolerance of cyanobacteria to the phosphonate herbicide glyphosate. Plant and Cell Physiology 49, 443-456.
| Crossref | Google Scholar | PubMed |

Franklin NM, Adams MS, Stauber JL, Lim RP (2001) Development of an improved rapid enzyme inhibition bioassay with marine and freshwater microalgae using flow cytometry. Archives of Environmental Contamination and Toxicology 40, 469-480.
| Crossref | Google Scholar | PubMed |

Geider RJ, La Roche J, Greene RM, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. Journal of Phycology 29, 755-766.
| Crossref | Google Scholar |

Gomes MP, Juneau P (2016) Oxidative stress in duckweed (Lemna minor L.) induced by glyphosate: is the mitochondrial electron transport chain a target of this herbicide? Environmental Pollution 218, 402-409.
| Crossref | Google Scholar | PubMed |

Gomes MP, Le Manac’h SG, Maccario S, Labrecque M, Lucotte M, Juneau P (2016) Differential effects of glyphosate and aminomethylphosphonic acid (AMPA) on photosynthesis and chlorophyll metabolism in willow plants. Pesticide Biochemistry and Physiology 130, 65-70.
| Crossref | Google Scholar | PubMed |

Gudda FO, Ateia M, Waigi MG, Wang J, Gao Y (2022) Ecological and human health risks of manure-borne steroid estrogens: a 20-year global synthesis study. Journal of Environmental Management 301, 113708.
| Crossref | Google Scholar | PubMed |

He Y, Zhou Y, Zhou Z, He J, Liu Y, Xiao Y, et al. (2023) Allelopathic effect of pyrogallic acid on cyanobacterium Microcystis aeruginosa: the regulatory role of nitric oxide and its significance for controlling harmful algal blooms (HABs). Science of The Total Environment 858, 159785.
| Crossref | Google Scholar | PubMed |

Huang J, Silva EN, Shen Z, Jiang B, Lu H (2012) Effects of glyphosate on photosynthesis, chlorophyll fluorescence and physicochemical properties of cogongrass (Imperata cylindrical L.). Plant Omics Journal 5, 177-183.
| Google Scholar |

Hyka P, Lickova S, Přibyl P, Melzoch K, Kovar K (2013) Flow cytometry for the development of biotechnological processes with microalgae. Biotechnology Advances 31, 2-16.
| Crossref | Google Scholar | PubMed |

Iummato MM, Fassiano A, Graziano M, dos Santos Afonso M, Ríos de Molina MdC, Juárez ÁB (2019) Effect of glyphosate on the growth, morphology, ultrastructure and metabolism of Scenedesmus vacuolatus. Ecotoxicology and Environmental Safety 172, 471-479.
| Crossref | Google Scholar | PubMed |

Jamers A, Lenjou M, Deraedt P, Bockstaele DV, Blust R, Coen Wd (2009) Flow cytometric analysis of the cadmium-exposed green alga Chlamydomonas reinhardtii (Chlorophyceae). European Journal of Phycology 44, 541-550.
| Crossref | Google Scholar |

Kabanova YuG (1961) On the cultivation of marine planktonic diatoms and peridinium algae in laboratory conditions. Trudy IO AN SSSR 47, 203-216 [In Russian].
| Google Scholar |

Kaeoboon S, Suksungworn R, Sanevas N (2021) Toxicity response of Chlorella microalgae to glyphosate herbicide exposure based on biomass, pigment contents and photosynthetic efficiency. Plant Science Today 8, 293-300.
| Crossref | Google Scholar |

Kielak E, Sempruch C, Mioduszewska H, Klocek J, Leszczyński B (2011) Phytotoxicity of Roundup Ultra 360 SL in aquatic ecosystems: biochemical evaluation with duckweed (Lemna minor L.) as a model plant. Pesticide Biochemistry and Physiology 99, 237-243.
| Crossref | Google Scholar |

Lippemeier S, Hintze R, Vanselow K, Hartig P, Colijn F (2001) In-line recording of PAM fluorescence of phytoplankton cultures as a new tool for studying effects of fluctuating nutrient supply on photosynthesis. European Journal of Phycology 36, 89-100.
| Crossref | Google Scholar |

Lopes AR, Moraes JS, Martins CdMG (2022) Effects of the herbicide glyphosate on fish from embryos to adults: a review addressing behavior patterns and mechanisms behind them. Aquatic Toxicology 251, 106281.
| Crossref | Google Scholar |

Maroli AS, Nandula VK, Dayan FE, Duke SO, Gerard P, Tharayil N (2015) Metabolic profiling and enzyme analyses indicate a potential role of antioxidant systems in complementing glyphosate resistance in an Amaranthus palmeri biotype. Journal of Agricultural and Food Chemistry 63, 9199-9209.
| Crossref | Google Scholar | PubMed |

Mateos-Naranjo E, Redondo-Gómez S, Cox L, Cornejo J, Figueroa ME (2009) Effectiveness of glyphosate and imazamox on the control of the invasive cordgrass Spartina densiflora. Ecotoxicology and Environmental Safety 72, 1694-1700.
| Crossref | Google Scholar | PubMed |

Matteucci E, Giampietro O (2008) Flow cytometry study of leukocyte function: analytical comparison of methods and their applicability to clinical research. Current Medicinal Chemistry 15, 596-603.
| Crossref | Google Scholar | PubMed |

Mertens M, Höss S, Neumann G, Afzal J, Reichenbecher W (2018) Glyphosate, a chelating agent – relevant for ecological risk assessment? Environmental Science and Pollution Research 25, 5298-5317.
| Crossref | Google Scholar | PubMed |

Mikaelyan AS, Pautova LA, Chasovnikov VK, Mosharov SA, Silkin VA (2015) Alternation of diatoms and coccolithophores in the north-eastern Black Sea: a response to nutrient changes. Hydrobiologia 755, 89-105.
| Crossref | Google Scholar |

Miteva LP-E, Ivanov SV, Alexieva VS (2010) Alterations in glutathione pool and some related enzymes in leaves and roots of pea plants treated with the herbicide glyphosate. Russian Journal of Plant Physiology 57, 131-136.
| Crossref | Google Scholar |

Murthy SDS, Bukhov NG, Mohanty P (1990) Mercury-induced alterations of chlorophyll a fluorescence kinetics in cyanobacteria: multiple effects of mercury on electron transport. Journal of Photochemistry and Photobiology B: Biology 6, 373-380.
| Crossref | Google Scholar |

Myers JP, Antoniou MN, Blumberg B, Carroll L, Colborn T, Everett LG, et al. (2016) Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement. Environmental Health 15, 19.
| Crossref | Google Scholar |

Nassiri Y, Mansot JL, Wéry J, Ginsburger-Vogel T, Amiard JC (1997) Ultrastructural and electron energy loss spectroscopy studies of sequestration mechanisms of Cd and Cu in the marine diatom Skeletonema costatum. Archives of Environmental Contamination and Toxicology 33, 147-155.
| Crossref | Google Scholar | PubMed |

Ozkoc HB, Bakan G, Ariman S (2007) Distribution and bioaccumulation of organochlorine pesticides along the Black Sea coast. Environmental Geochemistry and Health 29, 59-68.
| Crossref | Google Scholar | PubMed |

Peng X, Palma S, Fisher NS, Wong SS (2011) Effect of morphology of ZnO nanostructures on their toxicity to marine algae. Aquatic Toxicology 102, 186-196.
| Crossref | Google Scholar | PubMed |

Perry SW, Norman JP, Barbieri J, Brown EB, Gelbard HA (2011) Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. BioTechniques 50, 98-115.
| Crossref | Google Scholar | PubMed |

Peruzzo PJ, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environmental Pollution 156, 61-66.
| Crossref | Google Scholar | PubMed |

Pikula K, Chaika V, Zakharenko A, Markina Z, Vedyagin A, Kuznetsov V, et al. (2020) Comparison of the level and mechanisms of toxicity of carbon nanotubes, carbon nanofibers, and silicon nanotubes in bioassay with four marine microalgae. Nanomaterials 10, 485.
| Crossref | Google Scholar | PubMed |

Pogosyan SI, Matorin DN (2005) Variability in the condition of the photosynthetic system of the Black Sea phytoplankton. Oceanology 45, S139-S148.
| Google Scholar |

Pollegioni L, Molla G (2011) New biotech applications from evolved D-amino acid oxidases. Trends in Biotechnology 29, 276-283.
| Crossref | Google Scholar | PubMed |

Powell HA, Kerbby NW, Rowell P (1991) Natural tolerance of cyanobacteria to the herbicide glyphosate. New Phytologist 119, 421-426.
| Crossref | Google Scholar |

Prado R, García R, Rioboo C, Herrero C, Abalde J, Cid A (2009) Comparison of the sensitivity of different toxicity test endpoints in a microalga exposed to the herbicide paraquat. Environment International 35, 240-247.
| Crossref | Google Scholar | PubMed |

Readman JW, Devilla RA, Tarran G, Llewellyn CA, Fileman TW, Easton A, et al. (2004) Flow cytometry and pigment analyses as tools to investigate the toxicity of herbicides to natural phytoplankton communities. Marine Environmental Research 58, 353-358.
| Crossref | Google Scholar | PubMed |

Reddy KN, Rimando AM, Duke SO (2004) Aminomethylphosphonic acid, a metabolite of glyphosate, causes injury in glyphosate-treated, glyphosate-resistant soybean. Journal of Agricultural and Food Chemistry 52, 5139-5143.
| Crossref | Google Scholar | PubMed |

Rioboo C, González O, Herrero C, Cid A (2002) Physiological response of freshwater microalga (Chlorella vulgaris) to triazine and phenylurea herbicides. Aquatic Toxicology 59, 225-235.
| Crossref | Google Scholar | PubMed |

Rioboo C, O’Connor JE, Prado R, Herrero C, Cid Á (2009) Cell proliferation alterations in Chlorella cells under stress conditions. Aquatic Toxicology 94, 229-237.
| Crossref | Google Scholar | PubMed |

Roubeix V, Mazzella N, Schouler L, Fauvelle V, Morin S, Coste M, et al. (2011) Variations of periphytic diatom sensitivity to the herbicide diuron and relation to species distribution in a contamination gradient: implications for biomonitoring. Journal of Environmental Monitoring 13, 1768-1774.
| Crossref | Google Scholar | PubMed |

Sergiev IG, Alexieva VS, Ivanov SV, Moskova II, Karanov EN (2006) The phenylurea cytokinin 4PU-30 protects maize plants against glyphosate action. Pesticide Biochemistry and Physiology 85, 139-146.
| Crossref | Google Scholar |

Shoman N, Solomonova E, Akimov A (2021) Application of structural, functional, fluorescent, and cytometric indicators for assessing physiological state of marine diatoms under different light growth conditions. Turkish Journal of Botany 45, 511-521.
| Crossref | Google Scholar |

Silva FB, Costa AC, Pereira Alves RR, Megguer CA (2014) Chlorophyll fluorescence as an indicator of cellular damage by glyphosate herbicide in Raphanus sativus L. plants. American Journal of Plant Sciences 5, 2509-2519.
| Crossref | Google Scholar |

Sohal RS, Mockett RJ, Orr WC (2002) Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Radical Biology and Medicine 33, 575-586.
| Crossref | Google Scholar | PubMed |

Solomonova ES, Akimov AI (2021) Assessing the physiological state of microalgae using cytometric and fluorescent indicators. Russian Journal of Plant Physiology 68, 981-987.
| Crossref | Google Scholar |

Solomonova ES, Mukhanov VS (2011) Flow cytometry for the assessment of physiological 541 active cells in batch cultures of Phaeodactylum tricornutum and Nitzschia specia. Marine Ecological Journal 10, 67-72 [In Russian].
| Google Scholar |

Solomonova ES, Shoman NY, Akimov AI, Rylkova OA (2022) Ecotoxicological aspects of the influence of ionic and nano copper on structural and functional characteristics of Dunaliella salina (Teod.). Russian Journal of Plant Physiology 69, 97.
| Crossref | Google Scholar |

Solomonova ES, Shoman NY, Akimov AI, Rylkova OA (2023) Comparative assessment of stress responses of the microalgae Prorocentrum cordatum (Ostenfeld) Dodge and Dunaliella salina (Teod.) to the presence of copper nanoparticles. Microbiology 92, 66-74.
| Crossref | Google Scholar |

Stachowski-Haberkorn S, Becker B, Marie D, Haberkorn H, Coroller L, de La Broise D (2008) Impact of Roundup on the marine microbial community, as shown by an in situ microcosm experiment. Aquatic Toxicology 89, 232-241.
| Crossref | Google Scholar | PubMed |

Stanciu G, Mititelu M, Gutaga S (2005) Pesticides and heavy metals determination in marine organisms from Black Sea. Chemical Bulletin 50, 1-2.
| Google Scholar |

Valiente Moro C, Bricheux G, Portelli C, Bohatier J (2012) Comparative effects of the herbicides chlortoluron and mesotrione on freshwater microalgae. Environmental Toxicology and Chemistry 31, 778-786.
| Crossref | Google Scholar | PubMed |

Van Bruggen AHC, He MM, Shin K, Mai V, Jeong KC, Finckh MR, Morris JG, Jr. (2018) Environmental and health effects of the herbicide glyphosate. Science of The Total Environment 616–617, 255-268.
| Crossref | Google Scholar | PubMed |

Vera MS, Lagomarsino L, Sylvester M, Pérez GL, Rodríguez P, Mugni H, et al. (2010) New evidences of Roundup® (glyphosate formulation) impact on the periphyton community and the water quality of freshwater ecosystems. Ecotoxicology 19, 710-721.
| Crossref | Google Scholar | PubMed |

Visviki I, Rachlin JW (1992) Ultrastructural changes in Dunaliella minuta following acute and chronic exposure to copper and cadmium. Archives of Environmental Contamination and Toxicology 23, 420-425.
| Crossref | Google Scholar | PubMed |

Visviki I, Rachlin JW (1994) Acute and chronic exposure of Dunaliella salina and Chlamydomonas bullosa to copper and cadmium: effects on ultrastructure. Archives of Environmental Contamination and Toxicology 26, 154-162.
| Crossref | Google Scholar | PubMed |

Wang H, Joseph JA (1999) Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radical Biology and Medicine 27, 612-616.
| Crossref | Google Scholar | PubMed |

Wang C, Lin X, Li L, Lin S (2016) Differential growth responses of marine phytoplankton to herbicide glyphosate. PLoS ONE 11, e0151633.
| Crossref | Google Scholar | PubMed |

Wang C, Sun X, Wang J, Tang J-M, Gu Y, Lin S (2022) Physiological and metabolic effects of glyphosate as the sole P source on a cosmopolitan phytoplankter and biogeochemical implications. Science of The Total Environment 832, 155094.
| Crossref | Google Scholar | PubMed |

Wong PK (2000) Effects of 2,4-D, glyphosate and paraquat on growth, photosynthesis and chlorophyll – a synthesis of Scenedesmus quadricauda Berb 614. Chemosphere 41, 177-182.
| Crossref | Google Scholar | PubMed |

Wu L, Qiu Z, Zhou Y, Du Y, Liu C, Ye J, Hu X (2016) Physiological effects of the herbicide glyphosate on the cyanobacterium Microcystis aeruginosa. Aquatic Toxicology 178, 72-79.
| Crossref | Google Scholar | PubMed |

Ye J, Huang C, Qiu Z, Wu L, Xu C (2019) The growth, apoptosis and oxidative stress in Microcystis viridis exposed to glyphosate. Bulletin of Environmental Contamination and Toxicology 103, 585-589.
| Crossref | Google Scholar | PubMed |

Zulu NN, Zienkiewicz K, Vollheyde K, Feussner I (2018) Current trends to comprehend lipid metabolism in diatoms. Progress in Lipid Research 70, 1-16.
| Crossref | Google Scholar | PubMed |