Journal of Hazardous Materials 404 (2021) 124001
Available online 18 September 2020
0304-3894/© 2020 Elsevier B.V. All rights reserved.
Evaluation of the spatiotemporal effects of bisphenol A on the leaves of the
seagrass Cymodocea nodosa
Ioannis-Dimosthenis S. Adamakis
a, *
, Paraskevi Malea
b, *
, Ilektra Sperdouli
c
,
Emmanuel Panteris
b
, Danae Kokkinidi
b
, Michael Moustakas
b
a
Department of Botany, Facutty of Biology, National and Kapodistrian University of Athens, 15784 Athens, Greece
b
Department of Botany, School of Biology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
c
Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organisation–Demeter, Thermi, 57001 Thessaloniki, Greece
A R T I C L E INFO
Keywords:
BPA
Chlorophyll fluorescence imaging
Hydrogen peroxide
Oxidative damage
Phenolic compounds
Reactive oxygen species
ABSTRACT
The organic pollutant bisphenol A (BPA) causes adverse effects on aquatic biota. The present study explored the
toxicity mechanism of environmentally occurring BPA concentrations (0.03–3 μg L
1
) on the seagrass Cymodocea
nodosa intermediate leaf photosynthetic machinery. A "mosaic" type BPA effect pattern was observed, with
"unaffected" and "affected”" leaf areas. In negatively affected leaf areas cells had a dark appearance and lost their
chlorophyll auto-fluorescence, while hydrogen peroxide (H
2
O
2
) content increased time-dependently. In the
"unaffected" leaf areas, cells exhibited increased phenolic compound production. At 1 μg L
1
of BPA exposure,
there was no effect on the fraction of open reaction centers (q
P
) compared to control and also no significant effect
on the quantum yield of non-regulated non-photochemical energy loss in PSII (Φ
NΟ
). However, a 3 μg L
1
BPA
application resulted in a significant Φ
NΟ
increase, even from the first exposure day. Ultrastructural observations
revealed electronically dense damaged thylakoids in the plastids, while effects on Golgi dictyosomes and the
endoplasmic reticulum were also observed at 3 μg L
1
BPA. The up-regulated H
2
O
2
BPA-derived production
seems to be a key factor causing both oxidative damages but probably also triggering retrograde signalling,
conferring tolerance to BPA in the "unaffected" leaf areas.
1. Introduction
Plastic marine litter consists of various fragmentation debris of
single-use and multipurpose items, the size of which ranges from some
nanometres to several meters. Plastic wastes are commonly found in the
marine environment, on the seashores and the seafloor, buried in the
sediment, floating in the water column or the sea water surface (Windsor
et al., 2019). Besides the harmful physiological/behavioural/cellular
effects on marine biota, due to the consumption of plastic pieces (Sigler,
2014), plastics in the maritime could also cause an additional hazard,
since many of them contain substances belonging to the endocrine-
disrupting chemicals (EDCs) which are classified as widespread
organic pollutants (Gallo et al., 2018; Wu and Seebacher, 2020).
Bisphenol-A (BPA) belongs to these chemicals and is a composite used in
manufacturing daily-use plastic commodities or the coatings of either
carton or metal food packages (Barrios-Estrada et al., 2018). The input
of BPA to the environment follows the trend of its consumption rate; due
to increase within the following decades, leading unavoidably to an
increased BPA environmental pollution (Jalal et al., 2018). Since, the
European Chemical Agency (ECHA) placed BPA to the substances of
emerging environmental concern in 2017 (Lehmler et al., 2018); BPA in
baby and kid utensils is now forbidden by the European Union, Brazil,
Canada, and the United States of America (Jalal et al., 2018).
The effluents from landfill wastes, wastewater treatment plants
(0.087–5.625 μg L
1
), industrial wastewater treatment facilities (1–150
μg L
1
) and sewage pulps (10 ≥ 100,000 μg kg
1
dry wt), are considered
to be the major inputs of BPA to the estuary and marine environment
(Corrales et al., 2015). Therefore, BPA is found at concentrations of
0.014–21.0 μg L
1
in rivers, from < 0.0005–2.470 μg L
1
in marine
waters (Corrales et al. 2015) and in sediments between < 0.24–492 μg
Kg
1
dry wt (Careghini et al., 2015). Flint et al. (2012) judging from the
measurable effects in wildlife from 11 studies suggested that environ-
mentally relevant BPA concentrations are considered to range between
0.08 and 12.5 μg L
1
. Regardless of the large amount of robust infor-
mation on the presence of BPA, ecotoxicological studies on aquatic or-
ganisms (Mihaich et al., 2009; Wu and Seebacher, 2020), especially
* Corresponding authors.
E-mail addresses: iadamaki@biol.uoa.gr (I.-D.S. Adamakis), malea@bio.auth.gr (P. Malea).
Contents lists available at ScienceDirect
Journal of Hazardous Materials
journal homepage: www.elsevier.com/locate/jhazmat
https://doi.org/10.1016/j.jhazmat.2020.124001
Received 20 March 2020; Received in revised form 31 August 2020; Accepted 14 September 2020