journal article·2024-09-23Open access

Molecular and Enzymatic Responses of Chlorococcum dorsiventrale to Heavy Metal Exposure: Implications for Their Removal

Rihab Hmani, Jihen Elleuch, Fatma Elleuch, Marwa Drira, Philippe Michaud, Lotfi Aleya, Slim Abdelkafi, Imen Fendri

Applied Sciences· Volume 14· Issue 18

Abstract

Heavy metals are one of the main threats to marine life and ecosystems and any remedial action in that regard is urgently required. The aim of this work is to study the bioremoval of cadmium, chromium and lead in a microalgae strain Chlorococcum dorsiventrale isolated from Tunisian coastal waters along with assessing its enzymatic and molecular responses. The microalgae were tested in artificial seawater to evaluate their capacity for phycoremediation in an aquatic environment. This strain tolerated exposure to Cd (II), Cr (VI), and Pb (II) and was able to grow for 14 days. Cd and Cr exposures elicited a decrease in chlorophyll, lipid and polysaccharide contents, whereas no damages were detected following Pb treatment. For protein content, no significant changes were seen except after Pb exposure which induced a slight increase after treatment with 5 mg/L. The assessment of stress defense-related gene expression using qRT-PCR revealed that exposure to Pb and Cr induced an up-regulation of catalase, superoxide dismutase and photosystem II protein D1 encoding genes. Moreover, heat shock protein 70 was slightly overexpressed. Removal efficiencies for Cr and Pb attained 89% and 95%, respectively. The mechanisms by which C. dorsiventrale removed Cr involved both intracellular and extracellular biosorption, while Pb was predominantly removed through membrane adsorption. This study highlights the potential of C. dorsiventrale as an efficient agent for the bioremediation of heavy metal-contaminated water, including industrial wastewater, thus paving the way for practical and environmental applications in pollution control.
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Research context

OpenAlex topics: Fluoride Effects and Removal · Heavy metals in environment

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Affiliations

Laboratoire de Biotechnologies des Plantes Appliquées à l’Amélioration des Cultures, Faculté des Sciences de Sfax, Université de Sfax, Sfax 3038, Tunisia

Laboratoire de Génie Enzymatique et Microbiologie, Equipe Biotechnologie des Algues, Ecole Nationale d’Ingénieurs de Sfax, Université de Sfax, Sfax 3038, Tunisia

Laboratory of Biotechnology and Plant Improvement, Center of Biotechnology of Sfax, Sfax 3038, Tunisia

Institut Pascal, Université Clermont Auvergne, Clermont Auvergne INP, CNRS, F-63000 Clermont-Ferrand, France

Chrono-Environnement Laboratory, UMR CNRS 6249, Bourgogne Franche-Comté University, F-25030 Besançon Cedex, France

Funding

Tunisian Ministry of Higher Education and Scientific Research

References (77)

Show source-provided references
1. Balzano, S., Sardo, A., Blasio, M., Chahine, T.B., Dell’Anno, F., Sansone, C., and Brunet, C. (2020). Microalgal metallothioneins and phytochelatins and their potential use in bioremediation. Front. Microbiol., 11.10.3389/fmicb.2020.00517 ↗
2. Insight into biosorption of heavy metals by extracellular polymer substances and the improvement of the efficacy: A review10.1111/lam.13563 ↗
3. Diversity and functions of microbes in surface sediments under heavy metal pollution of western Chaohu Lake10.1111/lam.13627 ↗
4. Health and environmental effects of heavy metals10.1016/j.jksus.2021.101653 ↗
5. Toxic heavy metals: Impact on the environment and human health, and treatment with conducting organic polymers, a review10.1007/s11356-020-09354-3 ↗
6. Carcinogenic risk of Pb, Cd, Ni, and Cr and critical ecological risk of Cd and Cu in soil and groundwater around the municipal solid waste open dump in central Thailand10.1155/2022/3062215 ↗
7. Comparative utilization of dead and live fungal biomass for the removal of heavy metal: A concise review10.1155/2021/5588111 ↗
8. Ecological evaluation of heavy metal pollution in the soil of Pb-Zn mines10.1007/s10646-021-02505-3 ↗
9. Contamination assessment, health risk evaluation, and source identification of heavy metals in the soil-rice system of typical agricultural regions on the Southeast Coast of China10.1007/s11356-020-11229-6 ↗
10. Carmona, B., and Abejón, R. (2023). Innovative membrane technologies for the treatment of wastewater polluted with heavy metals: Perspective of the potential of electrodialysis, membrane distillation, and forward osmosis from a bibliometric analysis. Membranes, 13.10.3390/membranes13040385 ↗
11. Removal methods of heavy metals from laboratory wastewater
12. Microalgae in removing heavy metals from wastewater—An advanced green technology for urban wastewater treatment10.1016/j.hazadv.2024.100444 ↗
13. Chen, Z., Osman, A.I., Rooney, D.W., Oh, W.-D., and Yap, P.-S. (2023). Remediation of heavy metals in polluted water by immobilized algae: Current applications and future perspectives. Sustainability, 15.10.3390/su15065128 ↗
14. Algal bioremediation of heavy metals: An insight into removal mechanisms, recovery of by-products, challenges, and future opportunities10.1016/j.nexus.2022.100129 ↗
15. Bioremediation of heavy metals from wastewater: A current perspective on microalgae-based future10.1111/lam.13564 ↗
16. Potential of three local marine microalgae from Tunisian coasts for cadmium, lead and chromium removals10.1016/j.scitotenv.2021.149464 ↗
17. Ben Mohamed, J., Elleuch, J., Drira, M., Esteban, M.Á., Michaud, P., Abdelkafi, S., and Fendri, I. (2021). Characterization and biotechnological potential of two native marine microalgae isolated from the Tunisian coast. Appl. Sci., 11.10.3390/app11115295 ↗
18. Phycoremediation mechanisms of heavy metals using living green microalgae: Physicochemical and molecular approaches for enhancing selectivity and removal capacity10.1016/j.heliyon.2021.e07609 ↗
19. A sustainable cultivation of microalgae using dairy and fish wastes for enhanced biomass and bio-product production10.1007/s13399-021-01817-y ↗
20. Characterization of cellular toxicity induced by sub-lethal inorganic mercury in the marine microalgae Chlorococcum dorsiventrale isolated from a metal-polluted coastal site10.1016/j.chemosphere.2023.139391 ↗
21. Interaction effects of polycyclic aromatic hydrocarbons and heavy metals on a soil microalga, Chlorococcum sp. MM1110.1007/s11356-013-1679-9 ↗
22. Nam, S.-H., Kim, D., An, S., and An, Y.-J. (2022). Validation of the paper-disc soil method using soil alga Chlorococcum infusionum to quantitatively determine the toxicity of heavy metals. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol., 258.10.1016/j.cbpc.2022.109380 ↗
23. Application of live Chlorococcum aquaticum biomass for the removal of Pb(II) from aqueous solutions10.1007/s10811-020-02242-w ↗
24. Shiels, K., Tsoupras, A., Lordan, R., Nasopoulou, C., Zabetakis, I., Murray, P., and Saha, S.K. (2021). Bioactive lipids of marine microalga Chlorococcum sp. SABC 012504 with anti-inflammatory and anti-thrombotic activities. Mar. Drugs, 19.10.3390/md19010028 ↗
25. Zinc biosorption by Dunaliella sp. AL-1: Mechanism and effects on cell metabolism10.1016/j.scitotenv.2021.145024 ↗
26. Optimization of biomass production by Chlorella saccharophila UTEX 247 employing response surface methodology10.1007/s13399-022-02966-4 ↗
27. Isolation and screening of Tetradesmus dimorphus and Desmodesmus asymmetricus from natural habitats in Northwestern China for clean fuel production and N, P removal10.1007/s13399-020-01034-z ↗
28. Smith, W.L., and Chanley, M.H. (1975). Culture of phytoplankton for feeding marine invertebrates. Culture of Marine Invertebrate Animals, Springer US.10.1007/978-1-4615-8714-9 ↗
29. Development of a new TaqMan-based PCR assay for the specific detection and quantification of Simkania negevensis10.1016/j.mcp.2020.101645 ↗
30. Ben Amor, F., Elleuch, F., Ben Hlima, H., Garnier, M., Saint-Jean, B., Barkallah, M., Pichon, C., Abdelkafi, S., and Fendri, I. (2017). Proteomic analysis of the chlorophyta Dunaliella new strain AL-1 revealed global changes of metabolism during high carotenoid production. Mar. Drugs, 15.10.3390/md15090293 ↗
31. Characterisation of novel Bacillus thuringiensis isolates against Aedes aegypti (Diptera: Culicidae) and Ceratitis capitata (Diptera: Tephridae)10.1016/j.jip.2014.11.005 ↗
32. Ahmad, S., Pandey, A., Pathak, V.V., Tyagi, V.V., and Kothari, R. (2020). Phycoremediation: Algae as eco-friendly tools for the removal of heavy metals from wastewaters. Bioremediation of Industrial Waste for Environmental Safety: Volume II: Biological Agents and Methods for Industrial Waste Management, Springer.10.1007/978-981-13-3426-9_3 ↗
33. The effect of heavy metals on the viability of Tetraselmis marina AC16-MESO and an evaluation of the potential use of this microalga in bioremediation10.7717/peerj.5295 ↗
34. Cadmium (Cd) tolerance evaluation of three strains of microalgae of the genus Ankistrodesmus, Chlorella, and Scenedesmus
35. Extracellular neutral protease from Arthrospira platensis: Production, optimization and partial characterization10.1016/j.ijbiomac.2020.11.102 ↗
36. Biomass and lipid production of marine microalgae using municipal wastewater and high concentration of CO210.1016/j.apenergy.2011.03.043 ↗
37. Testing of two different strains of green microalgae for Cu and Ni removal from aqueous media10.1016/j.scitotenv.2017.05.222 ↗
38. Formulae and program to determine total carotenoids and chlorophylls a and B of leaf extracts in different solvents
39. Solvent extraction and spectrophotometric determination of pigments of some algal species from the shore of Puthumadam, Southeast Coast of India
40. A simple method for the isolation and purification of total lipids from animal tissues10.1016/S0021-9258(18)64849-5 ↗
41. Isolation, identification and characterization of a new lipolytic Pseudomonas sp., strain AHD-1, from Tunisian soil10.1080/09593330903369994 ↗
42. A Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding10.1016/0003-2697(76)90527-3 ↗
43. New Bacillus thuringiensis toxin combinations for biological control of lepidopteran larvae10.1016/j.ijbiomac.2014.01.029 ↗
44. Elleuch, J., Drira, M., Ghribi, I., Hadjkacem, F., Pierre, G., Khemakhem, H., and Abdelkafi, S. (2024). Lead removal from the aqueous solution by extracellular polymeric substances produced by the marine diatom Navicula salinicola. Environ. Technol., 1–13.10.1080/09593330.2024.2338456 ↗
45. Optimization of phenol-chloroform RNA extraction
46. Derbel, H., Elleuch, J., Tounsi, L., Nicolo, M.S., Rizzo, M.G., Michaud, P., Fendri, I., and Abdelkafi, S. (2022). Improvement of biomass and phycoerythrin production by a strain of Rhodomonas sp. isolated from the Tunisian coast of Sidi Mansour. Biomolecules, 12.10.3390/biom12070885 ↗
47. Influence of the sulfate content of the exopolysaccharides from Porphyridium sordidum on their elicitor activities on date palm vitroplants10.1016/j.plaphy.2022.06.012 ↗
48. Elleuch, F., Ben Hlima, H., Barkallah, M., Baril, P., Abdelkafi, S., Pichon, C., and Fendri, I. (2019). Carotenoids overproduction in Dunaliella sp.: Transcriptional changes and new insights through lycopene β cyclase regulation. Appl. Sci., 9.10.3390/app9245389 ↗
49. DsCaf1 is involved in environmental stress response of Dunaliella salina10.1016/j.ijbiomac.2015.10.015 ↗
50. Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae)10.1016/j.chemosphere.2005.06.029 ↗
51. El-Naggar, N.E., Hussein, M.H., Shaaban-Dessuuki, S.A., and Dalal, S.R. (2020). Production, extraction and characterization of Chlorella vulgaris soluble polysaccharides and their applications in AgNPs biosynthesis and biostimulation of plant growth. Sci. Rep., 10.10.1038/s41598-020-59945-w ↗
52. Responses of green algae and diatom upon exposure to chromium and cadmium10.31276/VJSTE.62(1).69-73 ↗
53. Effects of cadmium stress on growth and amino acid metabolism in two compositae plants10.1016/j.ecoenv.2018.04.045 ↗
54. Phycoremediation of Pb, Cd, Cu, and Cr by Chaetoceros calcitrans (Paulsen) Takano
55. Toxicity and accumulation of lead and cadmium in the filamentous green alga Cladophora fracta (O.F. Muller ex Vahl) Kutzing: A laboratory study10.2306/scienceasia1513-1874.2005.31.121 ↗
56. Responses of Dunaliella sp. AL-1 to chromium and copper: Biochemical and physiological studies10.1016/j.chemosphere.2024.143133 ↗
57. Bioaccumulation and toxicity of As in the alga Chlorococcum sp.: Prospects for As bioremediation10.1007/s00128-020-02964-0 ↗
58. Effects of zinc and mercury on ROS-mediated oxidative stress-induced physiological impairments and antioxidant responses in the microalga Chlorella vulgaris10.1007/s11356-021-12950-6 ↗
59. Čypaitė, A., Žaltauskaitė, J., and Venclovienė, J. (2014, January 22–23). Assessment of chlorophyll-a, chlorophyll-b and growth rate in freshwater green algae Pseudokirchneriella subcapitata exposed to cadmium and copper. Proceedings of the 9th International Conference Environmental Engineering (9th ICEE)—Selected Papers, Vilnius, Lithuania.10.3846/enviro.2014.009 ↗
60. Aquatic pollution caused by mercury, lead, and cadmium affects cell growth and pigment content of marine microalga Nannochloropsis oculata10.1007/s10661-020-8222-5 ↗
61. Toxic effects of boscalid on the growth, photosynthesis, antioxidant system and metabolism of Chlorella vulgaris10.1016/j.envpol.2018.06.055 ↗
62. Influence of cadmium stress on the lipid production and cadmium bioresorption by Monoraphidium sp. QLY-110.1016/j.enconman.2019.03.041 ↗
63. Effects of lead on two green microalgae Chlorella and Scenedesmus: Photosystem II activity and heterogeneity10.1016/j.algal.2016.03.006 ↗
64. Lead induced antioxidant response and phenotypic plasticity of Scenedesmus quadricauda (Turp.) de Brébisson under different nitrogen concentrations10.1007/s10811-014-0312-8 ↗
65. Heavy metals phycoremediation using tolerant green microalgae: Enzymatic and non-enzymatic antioxidant systems for the management of oxidative stress10.1016/j.jece.2020.104460 ↗
66. Zinc oxide nanoparticles (ZnONPs) alleviate heavy metal-induced toxicity in Leucaena leucocephala seedlings: A physiochemical analysis10.1016/j.plaphy.2016.08.022 ↗
67. First line defence antioxidants—Superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid
68. Effect of metals, metalloids and metallic nanoparticles on microalgae growth and industrial product biosynthesis: A review10.3390/ijms161023929 ↗
69. Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-110.1016/j.bbabio.2007.10.015 ↗
70. Toxicological effects of cadmium and lead on two freshwater diatoms10.1016/j.etap.2018.03.013 ↗
71. Heat shock protein genes in the green alga Tetraselmis suecica and their role against redox and non-redox active metals10.1016/j.ejop.2019.01.006 ↗
72. Applications and pitfalls of stress-proteins in biomonitoring10.1016/S0300-483X(00)00304-8 ↗
73. Interaction between tolerance and 70 kDa stress protein (hsp70) induction in collembolan populations exposed to long-term metal pollution10.1016/S0929-1393(98)00127-9 ↗
74. Heat shock proteins hsp32 and hsp70 as biomarkers of an early response? In vitro induction of heat shock proteins after exposure of cell culture to carcinogenic compounds and their real mixtures10.1016/j.mrgentox.2003.09.005 ↗
75. Biosorption of Pb2+ from water solution by using Chroococcus minutus and Chlorococcum aegyptiacum as biosorbents
76. Toxicity and bioaccumulation of lead, cadmium and zinc in Chroococcus minutus and Chlorococcum aegyptiacum
77. Potentiality of Chroococcus minutus (Cyanophyta) and Chlorella vulgaris (Chlorophyta) isolated from Manzala Lake for bioremediation of cadmium and lead