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

Ecotoxicol Environ Saf. 2021 Jan 15:208:111386. doi: 10.1016/j.ecoenv.2020.111386. Epub 2020 Oct 6.

Abstract

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.

Keywords: Accumulation kinetics; Bioindicator; Biomarker; Marine angiosperm; Toxicity effect; Trace metal.

MeSH terms

  • Biological Transport
  • Biomarkers / analysis
  • Cell Survival / drug effects
  • Hydrocharitaceae / metabolism*
  • Hydrogen Peroxide / metabolism
  • Kinetics
  • Microtubules / drug effects
  • Nickel / metabolism*
  • Oxidative Stress / drug effects
  • Plant Leaves / drug effects
  • Seawater / chemistry
  • Trace Elements / analysis
  • Water Pollutants, Chemical / metabolism*

Substances

  • Biomarkers
  • Trace Elements
  • Water Pollutants, Chemical
  • Nickel
  • Hydrogen Peroxide