Nickel uptake kinetics and its structural and physiological impacts in the seagrass Halophila stipulacea

The present work aims to provide insight into interactions between trace metals and higher plants, focusing on nickel uptake and its effects in seagrasses at environmentally relevant concentrations. Total and intracellular nickel accumulation kinetics, nickel effects on structural cell components, o...

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Main Authors: Paraskevi Malea, Zoi Mylona, Emmanuel Panteris, Dimitrios Phaedon Kevrekidis, Theodoros Kevrekidis
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651320312239
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spelling doaj-9b356a2e2f864b93934811bb75a35fab2021-04-23T06:13:50ZengElsevierEcotoxicology and Environmental Safety0147-65132021-01-01208111386Nickel uptake kinetics and its structural and physiological impacts in the seagrass Halophila stipulaceaParaskevi Malea0Zoi Mylona1Emmanuel Panteris2Dimitrios Phaedon Kevrekidis3Theodoros Kevrekidis4Department of Botany, School of Biology, Aristotle University of Thessaloniki, GR-54124, Thessaloniki, Greece; Corresponding author.Department of Botany, School of Biology, Aristotle University of Thessaloniki, GR-54124, Thessaloniki, GreeceDepartment of Botany, School of Biology, Aristotle University of Thessaloniki, GR-54124, Thessaloniki, GreeceDepartment of Medicine, Democritus University of Thrace, Dragana, GR-68131, Alexandroupolis, GreeceLaboratory of Environmental Research and Education, Democritus University of Thrace, Nea Hili, GR-68131, Alexandroupolis, Greece; Corresponding author.The present work aims to provide insight into interactions between trace metals and higher plants, focusing on nickel uptake and its effects in seagrasses at environmentally relevant concentrations. Total and intracellular nickel accumulation kinetics, nickel effects on structural cell components, oxidative stress marker and cellular viability, and the accumulation kinetics-toxic effects relationship were investigated in leaves of Halophila stipulacea plants incubated in seawater under laboratory conditions containing nickel ions at 0.01–10 mg L−1 for 14 days. Nickel accumulation kinetics in H. stipulacea young and older apical leaves followed a Michaelis-Menten-type equation, allowing the calculation of uptake parameters; uptake rate (Vc) and equilibrium concentration (Ceq) tended to increase with the increase of nickel concentration in the medium. A dose- and uptake parameter-dependent actin filament (AF) and endoplasmic reticulum (ER) impairment was observed, whereas no effects occurred on microtubules and cell ultrastructure. AF disturbance and ER aggregation were firstly observed in differentiated cells at the lowest concentration on the 12th and 14th day, respectively, while AF disruption in meristematic cells firstly occurred at 0.05 mg L−1; the effects appeared earlier and were more acute at higher concentrations. Increased H2O2 levels were detected, while, at the highest exposures, a significant reduction in epidermal cell viability in older leaves occurred. The lowest total nickel concentrations in young leaves associated with AF disturbance onset at nickel exposure concentrations of 0.01–1 mg L−1 varied between 18.98 and 63.93 μg g−1 dry wt; importantly, they were comparable to nickel concentrations detected in seagrass leaves from various locations. The relationships between exposure concentration, uptake kinetic parameters and toxic effect onset were satisfactorily described by regression models. Our findings suggest that (a) nickel may pose a threat to seagrass meadows, (b) H. stipulacea can be regarded as an efficient biomonitor of nickel, (c) AF and ER impairment in seagrass leaves can be considered as early biomarkers of nickel-induced stress, and (d) the regression models obtained can be used as a tool to evaluate ambient nickel levels and to detect ecotoxicologically significant nickel contamination. The data presented can be utilized in the management and conservation of the coastal environment.http://www.sciencedirect.com/science/article/pii/S0147651320312239Accumulation kineticsBioindicatorBiomarkerMarine angiospermToxicity effectTrace metal
collection DOAJ
language English
format Article
sources DOAJ
author Paraskevi Malea
Zoi Mylona
Emmanuel Panteris
Dimitrios Phaedon Kevrekidis
Theodoros Kevrekidis
spellingShingle Paraskevi Malea
Zoi Mylona
Emmanuel Panteris
Dimitrios Phaedon Kevrekidis
Theodoros Kevrekidis
Nickel uptake kinetics and its structural and physiological impacts in the seagrass Halophila stipulacea
Ecotoxicology and Environmental Safety
Accumulation kinetics
Bioindicator
Biomarker
Marine angiosperm
Toxicity effect
Trace metal
author_facet Paraskevi Malea
Zoi Mylona
Emmanuel Panteris
Dimitrios Phaedon Kevrekidis
Theodoros Kevrekidis
author_sort Paraskevi Malea
title Nickel uptake kinetics and its structural and physiological impacts in the seagrass Halophila stipulacea
title_short Nickel uptake kinetics and its structural and physiological impacts in the seagrass Halophila stipulacea
title_full Nickel uptake kinetics and its structural and physiological impacts in the seagrass Halophila stipulacea
title_fullStr Nickel uptake kinetics and its structural and physiological impacts in the seagrass Halophila stipulacea
title_full_unstemmed Nickel uptake kinetics and its structural and physiological impacts in the seagrass Halophila stipulacea
title_sort nickel uptake kinetics and its structural and physiological impacts in the seagrass halophila stipulacea
publisher Elsevier
series Ecotoxicology and Environmental Safety
issn 0147-6513
publishDate 2021-01-01
description The present work aims to provide insight into interactions between trace metals and higher plants, focusing on nickel uptake and its effects in seagrasses at environmentally relevant concentrations. Total and intracellular nickel accumulation kinetics, nickel effects on structural cell components, oxidative stress marker and cellular viability, and the accumulation kinetics-toxic effects relationship were investigated in leaves of Halophila stipulacea plants incubated in seawater under laboratory conditions containing nickel ions at 0.01–10 mg L−1 for 14 days. Nickel accumulation kinetics in H. stipulacea young and older apical leaves followed a Michaelis-Menten-type equation, allowing the calculation of uptake parameters; uptake rate (Vc) and equilibrium concentration (Ceq) tended to increase with the increase of nickel concentration in the medium. A dose- and uptake parameter-dependent actin filament (AF) and endoplasmic reticulum (ER) impairment was observed, whereas no effects occurred on microtubules and cell ultrastructure. AF disturbance and ER aggregation were firstly observed in differentiated cells at the lowest concentration on the 12th and 14th day, respectively, while AF disruption in meristematic cells firstly occurred at 0.05 mg L−1; the effects appeared earlier and were more acute at higher concentrations. Increased H2O2 levels were detected, while, at the highest exposures, a significant reduction in epidermal cell viability in older leaves occurred. The lowest total nickel concentrations in young leaves associated with AF disturbance onset at nickel exposure concentrations of 0.01–1 mg L−1 varied between 18.98 and 63.93 μg g−1 dry wt; importantly, they were comparable to nickel concentrations detected in seagrass leaves from various locations. The relationships between exposure concentration, uptake kinetic parameters and toxic effect onset were satisfactorily described by regression models. Our findings suggest that (a) nickel may pose a threat to seagrass meadows, (b) H. stipulacea can be regarded as an efficient biomonitor of nickel, (c) AF and ER impairment in seagrass leaves can be considered as early biomarkers of nickel-induced stress, and (d) the regression models obtained can be used as a tool to evaluate ambient nickel levels and to detect ecotoxicologically significant nickel contamination. The data presented can be utilized in the management and conservation of the coastal environment.
topic Accumulation kinetics
Bioindicator
Biomarker
Marine angiosperm
Toxicity effect
Trace metal
url http://www.sciencedirect.com/science/article/pii/S0147651320312239
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