Ulva Lactuca Un Bioindicador de La Contaminación Antropogénica y Su Capacidad de Remediación Ambiental

Marine Environmental Research 171 (2021) 105468
Contents lists available at ScienceDirect
Marine Environmental Research

journal homepage: www.elsevier.com/locate/marenvrev
Ulva lactuca: A bioindicator for anthropogenic contamination and its

environmental remediation capacity
María M. Areco a, b, *, Vanesa N. Salomone a, b, María dos Santos Afonso c
a
Instituto de Investigación e Ingeniería Ambiental -IIIA, UNSAM, CONICET, 3iA, Campus Miguelete, 25 de Mayo y Francia, 1650-San Martín, Provincia de Buenos Aires,
Argentina
b
Consejo Nacional de Investigaciones Científicas y Técnicas. CONICET, Argentina
c
Departamento de Química Inorgánica, Analítica y Química Física, Facultad de Ciencias Exactas y Naturales, Instituto de Química Física de los Materiales, Medio
Ambiente y Energía (INQUIMAE), CONICET-Universidad de Buenos Aires, Ciudad Universitaria Pabellón II 3er Piso, Int. Guiraldes, 2160, C1428EHA Ciudad Autónoma
de, Buenos Aires, Argentina
A R T I C L E I N F O A B S T R A C T
Keywords: Coastal regions are subjected to degradation due to anthropogenic pollution. Effluents loaded with variable
Ulva lactuca concentrations of heavy metal, persistent organic pollutant, as well as nutrients are discharged in coastal areas
Marine pollution leading to environmental degradation. In the past years, many scientists have studied, not only the effect of
Biomonitor
different contaminants on coastal ecosystems but also, they have searched for organisms tolerant to pollutants
Bioindicator
that can be used as bioindicators or for biomonitoring purposes. Furthermore, many researchers have demon
Remediation
strated the capacity of different marine organisms to remove heavy metals and persistent organic pollutants, as
well as to reduce nutrient concentration, which may lead to eutrophication. In this sense, Ulva lactuca, a green
macroalgae commonly found in coastal areas, has been extensively studied for its capacity to accumulate pol
lutants; as a bioindicator; as well as for its remediation capacity. This paper aims to review the information
published regarding the use of Ulva lactuca in environmental applications. The review was focused on those
studies that analyse the role of this macroalga as a biomonitor or in bioremediation experiments.
1. Introduction pollutants (POPs) are of major environmental concern due to their

toxicity in organisms, high persistence in the environment,
In the last century, the economic development namely the urbani non-biodegradability, and bioaccumulation and bioamplification along
zation, land field exploitation and industrialization have resulted in an the food-chain (Christophoridis et al., 2019; Liang et al., 2018; Ozyigit
increase in contamination in the coastal regions. Then, the marine et al., 2017).
environment is globally subjected to an ever-increasing level of pollut Numerous researchers have studied the relationship between eco
ants (Bonanno et al., 2020) leading to a significant environmental and nomic growth and environmental pollution (quality) (Peng et al., 2020);
ecological degradation. The main contaminants found in marine envi however, there are warnings regarding the long-term effects on the
ronments are: potentially toxic elements, such as heavy metals, organic economy if more environmentally friendly practices, monitoring of key
pollutant such as oil hydrocarbons, phenols, polycyclic aromatic hy species and remediation plans are not implemented (Pinheiro et al.,
drocarbons (PHAs) and organochlorine compounds, among others; and 2019). In this sense, the study of possible pollution bioindicators as well
also nutrients (nitrate and phosphorous), that causes eutrophication on as the development of new technologies for water treatment have led
many sea shores (Chen et al., 2018; Lewis et al., 2011). Pollutants have scientist to explore different biomasses that may be used in these senses.
different origins depending on their type and source: leaching of pesti Many studies have been published in the last decades where different
cides and fertilizers from agricultural fields, urban sewage, acid mine macroalgae were used as biomonitors as well as for water remediation
drainage and industrial activities (Bonanno et al., 2020; Gherib et al., (Agarwal et al., 2020; Bonanno et al., 2020; Bonanno and
2016; Y. W. Qiu et al., 2017). Heavy metals and persistent organic Orlando-Bonaca, 2018; Diop et al., 2016a; Jarvis and Bielmyer-Fraser,
* Corresponding author. Instituto de Investigación e Ingeniería Ambiental -IIIA, UNSAM, CONICET, 3iA, Campus Miguelete, 25 de Mayo y Francia, 1650-San
Martín, Provincia de Buenos Aires, Argentina.
E-mail address: [email protected] (M.M. Areco).
https://doi.org/10.1016/j.marenvres.2021.105468
Received 9 June 2021; Received in revised form 24 August 2021; Accepted 27 August 2021
Available online 28 August 2021
0141-1136/© 2021 Elsevier Ltd. All rights reserved.
M.M. Areco et al. Marine Environmental Research 171 (2021) 105468
2015; Trinelli et al., 2019). as diabetes, obesity, endocrine disturbance, cancer, cardiovascular,
The green alga Ulva lactuca, can be found from tropical to polar reproductive and environmental problems (Alharbi et al., 2018).
climates, although the strains most likely vary among regions. Today Even though many of these POPs have been already banned (Table I)
most of the naturally produced and harvested U. lactuca biomass is an (Kovner, 2009), they persist in the environment for more than 10 years
unused resource. The algae can be incorporated into compost and spread with few as long as century (Alharbi et al., 2018). For example, DDT,
on fields as enriching agents, but is mainly dumped or left stranded to endrin, mirex, polychlorinated-dibenzo-p-dioxins and furans remain in
decompose on the shore creating waste problems (Bruhn et al., 2011). the environment for 10–20 years (Wania and Mackay, 1999). In marine
Then, a huge amount of biomass is generated and available for alter environments, among the most studies POPs are: polycyclic aromatic
native purposes such as: a source of pigments and lipids; as an adsorbent hydrocarbons (PAHs), organochlorine pesticides (OCPs) and poly
material; for aquaculture or agriculture applications; and for cosmetic chlorinated biphenyls (PCBs) due to their toxicity and prevalence in a
and pharmaceutical uses (Allouche, 2021; Anjali et al., 2019; Areco wide range of environmental media (Han and Currell, 2017; Obbard
et al., 2020; Martins et al., 2021; Velichkova et al., 2018). et al., 2007). Regarding to the source, PAHs are mainly derived from
incomplete fossil fuel combustion and oil-related discharges to the
1.1. Heavy metals contamination environment. Chlorinated organic compounds have a wide range of in
dustrial and agricultural applications, and includes the pesticides DDT
Metal pollution in aquatic ecosystems is a major environmental (p,p-dichlorodiphenyl trichloroethane) and Lindane (g-hexa
concern impacting various life-forms (Corales-Ultra et al., 2019), since chlorocyclohexane). PCBs have been used historically in an extensive
they are highly persistent and can be toxic at low concentrations range of industrial applications, including as dielectric fluids in elec
(Chaudhuri et al., 2007). They are introduced into the coastal environ trical transformers. Such chemicals can readily enter the aquatic envi
ments by various natural and anthropogenic activities such as discharges ronment via atmospheric deposition, groundwater leaching, soil run-off
from aquaculture, sewage, mining, gasoline from boats, agricultural, and sewage discharge (Obbard et al., 2007).
industrial and domestic effluent, accidental chemical spills, and Gasoline is another important organic contaminant in the marine
dredging activity, related with rapid development, urbanization, and environment, often present at a high level in areas submitted to intense
industrialization (Chakraborty et al., 2014; Satheeswaran et al., 2019). ship traffic. The degradations reactions of organic contaminants with
The toxicity of heavy metals in the environment is related to their saturated bonds in their structure (mainly alkanes) are slow and require
concentrations and environmental speciation and not to their essential more energy; hence they are very resistant to degradation. (Al-Hafedh
characteristics. They may be in waters as organic and inorganic colloids,
mineral particles (suspended solids) and dissolved (cationic or anionic Table 1
complexes in solution), depending upon the nature of the chemical List of the persistent organic pollutants (POPs) banned at the Stockholm
species and physicochemical factors like pH, conductivity, salinity and Convention in 2001; and at the Conference of Parties (COP Meetings) in 2009,
organic matter, and they may exceed the permissible level in sediment 2011 and 2013.
and seawater (Satheeswaran et al., 2019). Consequently, metal con BANNED POPs SOURCES YEAR
centrations in seawater are usually very low and fluctuate whenever the BANNED
physicochemical parameters in the environment change. Besides, the Stockholm Convention of 2001
analysis of total metal content in water and sediment does not predict Aldrin Pesticide 2001
the toxicity of contaminants to biota, because they can be accumulated Chlordane Pesticide 2001
in organisms of different trophic levels of the food chain, damaging their Dieldrin Pesticide 2001
Endrin Pesticide 2001
tissues and suppressing growth and ultimately affecting human beings Heptachlorine Pesticide 2001
(Aljahdali and Alhassan, 2020; El-Kady and Abdel-Wahhab, 2018). Iron, Hexachlorobenzene (HCB) Product from burning 2001
cadmium and mercuric chloride stimulate the production of free reac byproducts from the production
tive oxygen species, which in turn impair the functions of proteins, lipids of another chemical
Mirex Additive in plastics and rubber 2001
and DNA causing oxidative stress and ultimately cell death (Chakraborty
for the reduction of burning rate
et al., 2014). Arsenic, cadmium, chromium, copper, lead, mercury, and Toxaphane 2001
vanadium are the metals included at the list elaborated by the Interna DDT Pesticide 2001
tional Agency for Research on Cancer (Straif et al., 2009), which clas Polychlorinated Biphenyls (PCBs) Oils in heat exchangers, 2001
sifies metals according to their carcinogenicity. Being the main source of transformer, capacitor, as
additives in paints and plastics,
contamination the ingestion of seafood, such as algae, shellfish and fish
carbonless copy (burning
(Briffa et al., 2020), since heavy metals, when found in high concen process paper).
tration in aquatic habitat, are accumulated in different organisms, such Dioxin Burning process 2001
as macroalgae, damaging their tissues and suppressing growth (Chak Furan Burning process 2001
Conference of Parties (COP Meetings) 2009
raborty et al., 2014). Depending on macroalgal species, the metals exert
α -Hexachlorocyclohexane Pesticides byproducts 2009
their toxicity in the general order of Zn < Pb < Ag < Cd < Cu < Hg (Rai β- Hexabromobiphenyl Pesticides 2009
et al., 1981). Monitoring, especially, the levels of these elements in Chlorordecane Pesticides 2009
seawater and marine organisms is crucial to reduce their impact on the Hexabromobiphenyl Industrial Chemical Substances 2009
environment and human health. Hexabromobiphenylether Industrial Chemical Substances 2009
Heptabromobiphenylether 2009
Lindane Pesticide (Head Lice Scabies) 2009
1.2. Persistent organic pollutant in the environment Pentachlorobenzene Pesticide 2009
Tetrabromodiphenylether & Industrial Chemical Substances 2009
Persistent organic pollutants (POPs) are chemicals of global concern Pentabromodiphenylether
Conference of Parties (COP), May
due to their potential for long-range transport, persistence in the envi
2011
ronment, the ability to biomagnify and bioaccumulate in ecosystems, as Endosulfam and its isomers Pesticides/Insecticides 2011
well as their significant negative effects on human health and the Conference of Parties (COP) 2014 (banned April 2013, but effective November
environment. Countless amounts of POPs are introduced into our envi 2014)
ronment as an outcome of anthropogenic activities (Pandey et al., 2019). Hexabromocyclodecane (HBCD) Fire Retardant 2014
Humans are chronically exposed to environmental POPs via the Extracted and adapted from “Persistent Organic Pollutants: A Global Issue, A
ingestion and inhalation pathways, causing various lethal diseases such Global Response”. United States Environmental Protection Agency (EPA).
2
et al., 2015). Accumulation of these substances can result highly toxic or macroalgae cell walls, that consist in a fibril matrix with intercellular
mortal for aquatic organisms and subsequently lead to the loss of marine spaces, enriched with sulfated polysaccharides and different functional
ecosystem diversity and stability (El-Shoubaky and Mohammad, 2016). groups, which are directly involved in the adsorption of organic and
inorganic pollutants. For instance, the cell walls of green marine mac
1.3. Nitrogen and phosphorous: nutrients or pollutants? roalgae of genus Ulva, is made of a polysaccharide fraction described as a
highly charged polyelectrolyte, named Ulvan, that are highly sulfated
The growth and reproduction of photosynthetic biota as well as the and essentially composed of rhamnose 3-sulfate, xylose, xylose 2-sulfate,
large-scale ecosystem primary production are frequently limited by the glucuronic acid, and iduronic acid units (Boubakri, 2020).
supplies of nitrogen (N) and/or phosphorus (P) in freshwater, marine As previously mentioned, U. lactuca’s widespread distribution and its
and terrestrial environments (Elser et al., 2007; Hecky and Kilham, key ecological importance make it a target organism to address for
1988; Vitousek, 2004; Walker and Syers, 1976). Indeed, elevated inputs possible responses to human-mediated environmental disturbances.
of these nutrients have been implicated worldwide in massive changes in Many studies have evaluated the response of this macroalgae to the
biological diversity and ecosystem services, reflecting the fact that presence of different types of pollutants present in the surrounding
global cycles of N and P have been amplified by post-industrial human environment (Bonanno et al., 2020; Diop et al., 2016; Ho, 1990; Ozyigit
activities (Elser et al., 2007; Falkowski et al., 2000). In coastal marine et al., 2017, among others). This specie presents a promising set of
systems, nitrogen has historically been considered to be the predomi characteristics for environmental applications: it has a cosmopolitan
nant limiting nutrient (Howarth and Marino, 2006). However, seques distribution, high growth rates, withstanding high variations of water
tration of P in calcareous sediments might drive P limitation in the salinity, high rates of nutrient assimilation, especially ammonium
tropics (Elser et al., 2007); while limitations on planktonic N-fixation (NH4+), grows well in eutrophic waters and has tolerance to contami
caused by insufficient light (Karl et al., 2001) or trace metal supply nants (Bonanno et al., 2020; Chen et al., 2015; Nielsen et al., 2012;
(Falkowski et al., 2000) are thought to influence the predominance of N Whitehouse and Lapointe, 2015). The differential nitrate and phosphate
or P limitation offshore. Other works question these generalizations uptake and their storage are part of adaptive strategies evolved by
(Downing et al., 1999; Kagami et al., 2013; Moore et al., 2013). As a macroalgae for their successful sustenance (Kumari et al., 2014).
result, the current state of knowledge has made it difficult for ecologists Moreover, it has a large surface area and a relatively simple structure,
to make general recommendations about the need for joint nutrient with uniform and physiologically active cells that, as previously
controls in ameliorating eutrophication because existing paradigms may mentioned, facilitates the interactions between the several functional
not provide accurate insight into the actual role of these nutrients in groups in the surface and the cations in solution (Sarı and Tuzen, 2008;
various ecosystems, such as marine ecosystems (Elser et al., 2007). Turner et al., 2007).
In addition to the natural flux of nutrients in the environment, huge The aim of this paper is to review the articles published on the use of
quantities of nitrogen and phosphorus compounds, of both organic and Ulva lactuca in environmental applications. The research was focused on
inorganic origin, are constantly released into aquatic ecosystems those studies that use this macroalgae as a biomonitor or in bioreme
including rivers, estuaries and coastal waters (Viana et al., 2011; Viana diation experiments.
and Bode, 2013). The main N and P sources are urbanization, defores
tation that may favour nitrification, the septic systems and the use of 2. Environmental monitoring
synthetic fertilisers and animal manure in agriculture (Orlandi et al.,
2017; Valiela et al., 1992). Sewages containing phosphates from de Monitoring the environmental state of coastal habitats is of the up
tergents and other cleaning products, are also a source of phosphorous most importance for the marine ecosystems conservation and associated
(Mueller and Helsel, 1996). The excess of nutrients, specifically nitrogen biodiversity (Bonanno et al., 2020). Bioindicators are organisms that
and phosphorus, are responsible for eutrophication, which may lead to contain information on the quality of the environment (or a part of the
the degradation of natural waters (Palmer et al., 2013). Eutrophication, environment); and biomonitors are organisms that contain information
results in green tides and seasonal hypoxia, damaging both ecosystem on the quantitative aspects of the quality of the environment, providing
functioning and biodiversity. In addition, it could lead to damage the a measure of the degree of the environmental contamination. For that,
inshore fisheries and recreational facilities. such organisms need to be sensitive to specific pollutants and tolerate
The adverse effects of anthropogenic nutrients inputs have led to the high concentrations of these pollutants in the environment (Markert
conclusion that nutrients need to be removed from urban waste effluents et al., 2003). Different aquatic organisms have often been used as both
before being discharged into receiving waters, in order to minimise their ‘biomonitors’ and ‘bioindicators’ of environmental pollution. There are
impact (Johir et al., 2011). Furthermore, the presence of high concen requisites for an ideal biomonitor, some of which are: (i) ability to
trations of nitrate ions in drinking water is a public health hazard accumulate contaminants without being severely affected or killed by
including infant methemoglobinemia ‘‘blue baby’’ syndrome and the the levels encountered in the environment; (ii) sessile, to be represen
possible formation of carcinogenic nitrosamines and nitrosamides tative of the area of study; and (iii) abundant throughout most of the
(Wright et al., 1999). Then, the development of studies to assess water world’s coasts (Phillips, 1980). Although the analysis of total pollutant
quality of marine ecosystems, both for monitoring and remediation are content in water and sediments does not predict the toxicity of con
necessaries. taminants to biota, the use of bioindicators allows also detecting the
fraction of contaminant, that has direct effects on living organisms
1.4. Macroalgae and environmental contamination (Bonanno et al., 2020). For example, the assessment of heavy metals to
determine ecological risk through measurement of biotic response,
Macroalgae constitute the base of trophic network in marine coastal provide information on the extent of bioavailability of metals and their
environments. They provide grazing and detrital food, habitats for influence on the natural state of aquatic ecosystems (Chakraborty et al.,
numerous animal and plant species, as well as up to 50% of the esti 2014).
mated net amount of global oxygen (Bonanno and Orlando-Bonaca, Among marine organism, macroalgae are considered as good bio
2018). Macroalgae have been recognized as bioengineer organisms, indicators and are often used to assess marine ecosystems (Doshi et al.,
which diversity and abundance determine the structure and complexity 2008). In this sense, macroalgae provide qualitative information on
of intertidal and subtidal communities (Valdés et al., 2018). contamination level and environmental quality in seawater due to their
In relation to the presence of pollutants in the marine environment, sedentary lifestyle, considerable biomass, and easy identification and
macroalgae may have different uses such as biomonitoring or biore collection (Chaudhuri et al., 2007). They can accumulate toxic metals,
mediation. Both processes are related to the characteristics of the reaching concentrations that are thousands of times higher than the
3
corresponding values in seawater (Conti and Cecchetti, 2003a). described as different species or even genera (Fort et al., 2020). The
Furthermore, macroalgae play a fundamental role in the nutrient cycle capacity of this macroalgae to adopt different phenotypes can be due to
of coastal systems, and reflect changes in water quality in an efficient environment parameters, such as the degree of water salinity or sym
way (Chaudhuri et al., 2007). A study carried out in different marine biosis with bacteria (Dominguez and Loret, 2019; Fort et al., 2020). The
organism, demonstrate that macroalgae are considered better bio cell wall is constituted by cellulose along with a high percentage of
monitors for metals in the water column than clams or other organisms proteins bonded to polysaccharides (Kidgell et al., 2019; Romera et al.,
with hard exoskeleton (El-Shoubaky and Mohammad, 2016). Never 2007; M.A. Trinelli et al., 2013), which comprises several functional
theless, the remediation and bioaccumulation capacities of living mac groups such as amino, hydroxyl, carboxyl, and sulfate (Romera et al.,
roalgae have been little explored despite its multiple advantages 2007). This alga grows fast since their photosynthetic products are
(Chojnacka, 2010; Henriques et al., 2017). While growing, living mac quickly transformed into biomass. The macroalgal growth rate is closely
roalgae can remove simultaneously contaminants (such as metals or linked to the removal efficiency since a fast growth will lead to a rapid
pharmaceutical compounds), the excess of nutrients (nitrates and increase of biomass, and consequently to a multiplication of specific
phosphates) from marine waters, and capture CO2 emissions (Henriques sites for metal binding (Chojnacka, 2010). U. lactuca is perfectly adapted
et al, 2015, 2017; Lartigue et al., 2003). Therefore, they may be used to to the salinity variations occurring in estuaries, due to tides and it
reduce levels of pollutants in aquaculture wastewaters (Roleda and withstands moderate eutrophic conditions, and it has suggested as a
Hurd, 2019; Shpigel et al., 2019, among others). desirable species for wastewater bioremediation. Nevertheless, many
Macroalgae showed great tolerance to metal contamination. It has investigations assess the role of U. lactuca as biomonitor or bioindicator
been established that the main mechanisms of macroalgae to thrive of metal contamination in marine environments.
under metal excess, and reduce stress and damage, involve cellular
exclusion mechanisms (metal-binding to cell wall and epibionts), syn 2.1. Ulva lactuca as bioindicator of heavy metals
theses of metal-chelating compounds, such as metal-binding proteins
and peptides that are capable of chelating free metals in the cytoplasm; Many studies have evaluated the role of U. lactuca as a biomonitor of
and the activation of the antioxidant system (increase in the activity of heavy metal pollution (such as Cd, Cr, Cu, Ni, Pb and Zn, among others),
antioxidant enzymes in organelles and cytoplasm) (Moenne et al., in different coast of the world with diverse levels of human impact
2016). Several investigations indicate that, for example, the metal (Table II). Table II demonstrate that U. lactuca is widely distributed and
retained in the cell wall can account for up to 95% of the total metal can accumulate essential and non-essential elements at similar concen
accumulated by the macroalgae (Huang et al., 2013; Roncarati et al., trations (Bonanno et al., 2020; Chaudhuri et al., 2007; Conti and Cec
2015; Sáez et al., 2015, among others). The accumulation capacity of chetti, 2003a; Diop et al., 2016). Gherib et al. (2020) have demonstrated
metals, and other pollutants in macroalgae depends on numerous fac that U. lactuca shows different responses to toxic metals, depending on
tors: location, waves, exposure, temperature, salinity, photoperiod, pH, the season, sampling period, age and phenological stage of specimens.
availability of nutrients, biomass age, the metabolism and the affinity of Bonanno et al. (2020) found that the metal content in the biomass of
the species for each element (Kırbaşoğlu, 2001). Trace elements are U. lactuca is significantly correlated with the levels of trace elements in
accumulated more intensively than those that play an important role in water and sediments. Mourad and Abd El-Azim (2019) calculated the
metabolism (Gherib et al., 2016). The accumulation of heavy metals in bioconcentration factor (BCF), which gives information about the ability
algae involves two phases: an initial rapid surface reaction (passive) of the macroalgae to accumulate metal in their tissues from the aquatic
followed by a much slower (active) uptake (Bates et al., 1982). During ecosystem, by comparing the concentrations in the biota (algal biomass)
the passive uptake, metal ions are adsorbed onto the cell surface within a and environment (marine water or sediments). Some environmental
relatively short period of time (few seconds or minutes), and the process conditions affect this parameter such as the physiological state of the
is metabolism-independent. Active uptake is metabolism-dependent, seaweed, the age of the cells, the availability of micronutrients during
causing the transport of metal ions across the cell membrane into the their growth and the environmental conditions during uptake dependent
cytoplasm (van Ginneken and de Vries, 2018). Also, the transport of on pH, temperature, and light intensity, among others. Their results
metal ions may occur through passive diffusion through the cell mem showed that U. lactuca is a great accumulator of non-essential metals
brane (Gadd, 1988). (Pb, Ni, Cd and Cr) from water (and not from sediments) with high BCF
A study conducted by Lee and Wang (2001) examined the influences values; so, it could be used for biomonitoring and remediation of heavy
of major nutrients (nitrate, ammonium, and phosphate) on the accu metals (Mourad and Abd El-Azim, 2019). A similar ratio, denominated
mulation of trace metals (Cd, Cr, Zn and Se) in Ulva fasciata, and they Transfer Factor (TF), was calculated by Diop et al. (2016a). The TF from
found that the uptake of the different metal ions can be enhanced or water (TFW) were greater than those from sediments (TFS). These au
reduced by the presence of nutrients. For example, Zn uptake in nitrate thors also demonstrate that U. lactuca accumulates concentrations of Cd,
enriched medium was significantly higher than its uptake in N-starved Cu and Pb ten or sixty times those measured in water, which confirm the
macroalgae. The accumulation was significantly related to the ambient bioaccumulation of these elements from seawater. Similar results have
phosphate concentration, while Cr accumulation increased with reported by Conti and Cecchetti (2003b) and Chakraborty et al. (2014).
increasing phosphate concentration. Therefore, the dependence on In agreement with reported by Mourad and Abd El-Azim (2019), the TFs
metal accumulation on major nutrients will appreciably affect our pre were lower than 1, suggesting limited bioaccumulation from sediment,
diction of metal accumulation in macroalgae. Similar competitive re despite marine sediment are often regarded as the ultimate sink for
sponses could occur in the presence of different toxic metal ions (Costa many pollutants, including trace elements. Valdés et al. (2018) and
et al., 2020; Henriques et al., 2017b, among others). This will be dis Allam et al. (2016) assessed metal concentrations in U. lactuca biomass
cussed later in the present review. and contrasted with metal levels in sediments. They indicate a high
Hence, many studies have been carried out across the globe using correlation between the metal levels in biomass and sediments, showing
different species of macroalgae including U. lactuca, as bioindicators of the capacity of U. lactuca to reflect the pollution levels. However, they
environmental contamination (Bonanno et al., 2020; Conti and Cec emphasize that it is important to consider that patterns of metal con
chetti, 2003a; Mourad and Abd El-Azim, 2019). U. lactuca is a species centrations in both sediments and U. lactuca not always follow the same
usually resembling lettuce with only two cell layers thick and sheet-like trend within each site, since sediments are regularly washed away, and
thallus, which translates into a large surface area, containing structur thus, metal concentrations in this matrix can change more rapidly than
ally uniform and physiologically active cells (Sarı and Tuzen, 2008). in algal biomass (Valdés et al., 2018). Indeed, it has been recognized that
Recently, genetic analyses demonstrated that another green macroalgae metal accumulation in macroalgae represents longer time frames of
with tubular phenotypes were U. lactuca clades although previously metal impacts on coastal environments (Brown and Depledge, 1998).
4
Table 2
Metal concentrations in Ulva lactuca from different world sites (mg/kg dry weight) (Note: ranges are expressed with “–”).
Location Cd Cr Cu Ni Pb Zn References
Coast of Sicily, Italy 0.06–0.260 25–2.21 1.48–10.4 0.97–8.12 0.67–5.77 8.21–85.1 Bonanno et al. (2020)
Suez Gulf, Egypt 0.657 1.342 5.701 5.654 8.686 22.35 Mourad and Abd El-Azim (2019)
Aqaba Gulf, Egypt 0.531 1.419 5.33 4.285 8.112 13.52 Mourad and Abd El-Azim (2019)
Suez Canal, Egypt 0.593 1.276 8.915 4.479 7.186 13.9 Mourad and Abd El-Azim (2019)
Valparaíso, Chile 0.52 No data 10.7 No data No data 13.0 Valdés et al. (2018)
Coastline of Honaine, Algeria 0.15–0.16 No data 0.45–0.46 0.58–0.82 1.44–2.20 2.81–3.54 Allam et al. (2016)
Senegalese Coast 0.30 ± 0.29 1.37 ± 1.16 6.23 ± 6.55 1.06 ± 0.32 2.64 ± 3.45 14.7 ± 15.1 Diop et al. (2016)
Gulf Of Kutch, India 2.9–3.6 4.09–5.65 14.2–21.5 0.5–2.6 0.8–3.5 146–340 Chakraborty et al. (2014)
Gulf of Gaeta, Italy 0.13–0.21 1.39–2.06 4.9–6.4 No data 1.67–2.28 45.0–56.0 Conti and Cecchetti (2003a)
Thermaikos, Greece 0.42 No data 7.4 9.2 0.02 43.7 Sawidis et al. (2001)
Crete, Greece 0.42–1.10 No data 7.00–14.5 8.7–13.7 0.02 16.4–56.3 Sawidis et al. (2001)
Tartous, Syria 11.0 ± 0.33 4.71 ± 0.02 5.48 ± 0.28 No data 0.55 ± 0.99 11.0 ± 0.33 Al-Masri et al. (2003)
Besides, other studies have demonstrated that U. lactuca is a good However, bioconcentration and bioaccumulation of POPs in macro
bioindicator of As, Se and V (Diop et al., 2016) and Hg (Arici and Bat, algae, including U. lactuca, have not been fully studied. The extent of
2017; Valdés et al., 2018). Henriques et al. (2015) evaluated Hg uptake POPs bioaccumulation by macroalgae is related to the characteristics of
and accumulation using realistic environmental concentrations. The organic substances, macroalgae species and biomass, lipid content and
determination of total Hg content in algal biomass overtime allowed to several environmental factors, such as nutrient concentrations, tem
confirm and to follow the uptake of Hg by the living macroalgae and, to perature, pH, light and also by grazed pressure (Qiu et al., 2017). Many
verify that volatilization of Hg or its conversion to organo-metallic forms studies have reported that nitrogen deficiency induced a significant in
was negligible during the decontamination process. Toxic metals uptake crease in algal lipid content and enhanced the bioconcentration of POPs
can be affected by the presence of other ions. For example, a study (Chai et al., 2013; Cheng et al., 2014; Zhao et al., 2009); since POPs are
showed that in U. lactuca samples, the uptake of Ca and Mg reduce the hydrophobic, they tend to associate with lipids.
uptake of Cd, Cu and Pb (Ozyigit et al., 2017). However, another For instance, many medicinal products are used in animal production
research assessed the removal capacity in multi-metallic solutions with serving several purposes from growth-promotion to the treatment of
excellent efficiencies (Henriques et al., 2017). diseases. Antibiotics are among these potentially harmful substances
Many studies demonstrate that metal bioaccumulation and toxic since they are especially tailored to be biologically active. Among these
effects in primary producers as U. lactuca, may have implications for are chloramphenicol, sulfathiazole or furaltadone, which is a nitrofuran
higher trophic levels (Jarvis and Bielmyer-Fraser, 2015). The bio banned for being mutagenic and carcinogenic (Barbosa et al., 2007;
magnification of metals depends on abiotic and biotic factors (Jar Bartel et al., 2009), but used in the black market for being cheap and
a-Marini et al., 2020; Rainbow, 2007; Wang, 2002). In coastal effective (Vass et al., 2008). In addition to heavy metals, U. lactuca has
ecosystems, sediment is the major repository compartment for metals, shown acceptable results as a biomonitor of furaltadone, an antibacterial
acting as a sink for these contaminants. Depending on certain condi agent illegally used for veterinary purposes (Leston et al., 2011);
tions, these contaminants may be mobilized into the water column chloramphenicol (CAPh) (Leston et al., 2013); sulfathiazole, an anti
and/or to the biota. Phytoplankton incorporates these elements through biotic commonly used in aquaculture (Leston et al., 2014); and diesel
adsorption onto the cell surface and intracellularly through the passive fuel pollution (Nechev et al., 2002; Al-Hafedh et al., 2015, Pilatti et al.,
and active uptake of dissolved fractions (Jara-Marini et al., 2020). It has 2017), among others; many of which are not biodegradable and are
been recognized that primary producers, such as U. lactuca, and primary accumulated and transferred through the food chain to higher trophic
consumers act as the main vectors in the trophic flux of contaminants, levels, including humans.
including metals (Ruelas-Inzunza and Páez-Osuna, 2008; Vizzini et al., Also, studies focused in bioconcentration and bioaccumulation of
2013). In this sense, Jara-Marini et al. (2020) studied the bio POPs, such as organochloride pesticides, in U. lactuca have increased in
magnification of Cd, Cu, Pb and Zn during four seasons, in the food web the last years (Leston et al., 2013; Qiu et al., 2017; among others).
of a semiarid coastal lagoon. Results demonstrate that concentrations of Sundhar et al. (2020) examined the level of residual organochlorine
the four metals increased among functional organism groups, from the pesticide (OCP) toxicity in U. lactuca. The presence of hexa
food web base to the highest trophic levels. In general, the distribution chlorocyclohexane, endosulfan, endrin, and DDT was observed in the
of the elements for the four sampled seasons was Zn > Cu > Pb > Cd. alga. Qiu et al. (2017) studied the occurrence of polybrominated
According to biomagnification factor and trophic biomagnification diphenyl ethers (PBDEs) and organochlorine pesticides (OCPs) in
factor, biomagnification of these metals in the entire food web phytoplankton and U. lactuca. Results demonstrated that the concen
(including primary producers, such as U. lactuca and primary, second trations of both PBDEs and OCPs were an order of magnitude higher in
ary, and tertiary consumers) occurs. phytoplankton than in U. lactuca, indicating that phytoplankton with
Many studies agree that U. lactuca has numerous features that make larger surface areas to volume ratio have higher uptake efficiency for
it one of the best bioindicators of metal pollution in marine environ POPs than this macroalgae.
ments. They are easy to identify and to collect, have a widespread dis The effects pf PCBs on U. lactuca was also studied by different au
tribution and the capacity to accumulate trace elements under toxic thors. Net et al. (2015) found that U. lactuca, at the base of the food
conditions (Bonanno et al., 2020; Mourad and Abd El-Azim, 2019, chain, displayed lower PCB concentrations than a marine organism of
among others). These characteristics would allow to set up large-scale higher up levels in the food chain. A study on bioaccumulation of PCBs
marine monitoring programs. by a seaweed bloom (Ulva rigida) showed that PCB concentrations were
the highest (95–99 mg kg− 1 dry weight) near the contamination source
2.2. Ulva lactuca as bioindicator of persistent organic pollutants (POPs) and provided evidence about its possible role in the trophic transfer of
PCBs and other bioaccumulated pollutants (Cheney et al., 2019).
Persistent organic pollutants attract increasing attention for their
widespread occurrence in the environments and their toxic, mutagenic
and carcinogenic characteristics. Seaweeds have a high capacity to bind
POPs, then they are considered as suitable contaminant biomonitors.
5
2.3. Ulva lactuca as bioindicator of nitrate and phosphorous Biosorption, known as the sorption of pollutants onto biological
contamination materials, is becoming a possible alternative for water remediation
(Miretzky et al., 2006), since is an economical, efficient and sustainable
The availability of nitrate and phosphate in the ocean varies method able to replace the most widely applied industrial materials such
dramatically on spatial and temporal scales and limits the primary as activated carbon and ion-exchange resins by readily available
productivity over large areas (Kumari et al., 2014). Eutrophication biomass from nature, such as algae, fungus, bacteria or agricultural
events, defined as an increase in nutrients, leading in excessive growth products. The prominent and emerging trend of subjecting biosorbent in
of plants such as phytoplankton or macroalgae, have economic and the adsorption technology is mainly because of their natural existence,
environmental effects in coastal shores around the world (Bat et al., abundance, renewable, biodegradable and economic features. Various
2001; Smetacek and Zingone, 2013). At high concentrations of N and P, biomasses (e.g. bacteria, yeast, fungi, algae and agroindustry
the rapid growth and higher photosynthesis for U. lactuca have been by-products and wastes (e.g. fruit peels, egg shells, crab shells and cork
attributed to its higher surface area:volume ratios compared with other stoppers) with low economic value have been tested (Abdelfattah et al.,
macroalgae, such as H. musciformis or G. tikvahiae (Whitehouse and 2016; Mohapatra et al., 2019; Silva et al., 2020). Among different
Lapointe, 2015). Furthermore, macroalgae such as U. lactuca, may biomass materials, algae constitute an excellent biosorbent material
reduce the occurrence of microalgae harmful blooms by reducing the because of its high adsorption coefficients, the low-cost, available in
nutrients available in the water columns (Tang and Gobler, 2011). In large quantities, low sensitivity to environmental and impurity factors,
general, U. lactuca has a maximum thickness of two cell layers (Domi and its excellent retention capacity, comparable in some cases to those
nguez and Loret, 2019), every cell is in contact with the environment; of synthetic resin (Abbas et al., 2019; Silva et al., 2020). In particular,
this makes it an ideal candidate to analyse nutrient uptake kinetics and U. lactuca has a simple morphology consisting of a bi-layered blade of
apply standardized functions for an accurate analysis of nutrient uptake. undifferentiated cells, which are in permanent contact with the envi
Environmental variations in temperature, salinity, light and nutri ronment, a great tolerance to pollutants concentrations as well as broad
ents (nitrate and phosphate), which are season-dependent, influence the ranges of salinity and temperature. In this sense, the use of macroalgae,
macroalgae physiology (Ale et al., 2011). The N/P ratio of wastewater such as U. lactuca, for the remediation of, heavy metals, POPs and nu
can heavily influence nutrient uptake, and macroalgae require more N trients have been studied in the past decades (Table III), with promising
than P, with an optimal N/P ratio varying in a wide range from 10:1 to results.
80:1 (Aquilino et al., 2020; Perini and Bracken, 2014; Roleda and Hurd, A number of chemical groups that contribute to the biosorption of
2019). The depletion of nitrate and phosphate also initiates a cascade of ions in solution have been reported, which includes hydroxyl, carboxyl,
physiological responses including a decrease at photosynthetic and carbonyl, sulphide, amino, amide, phosphonate, phosphodiester, among
respiration rates, inhibition of growth and activation of nutrient acqui others (Crist et al., 1981; Hunt, 1986). The importance of each of these
sition and the transport network (Kumari et al., 2014). Similarly, the groups in the adsorption of, for example heavy metals, depends not only
excess of nutrients can also alter the accumulation of metals in algae on metal affinity with the group, but also on factors such as the number
since macroalgae are often exposed to both nutrient enrichment and of adsorption sites on the adsorbent material, the accessibility to them
metal pollution. In waters rich in nitrogen of the Sacca di Goro lagoon,
nitrate accumulation in Ulva thalli has inversely related with Fe uptake,
indicating an influence of Fe limitation on N acquisition (Viaroli et al., Table 3
2005). Human et al. (2016) collected algal tissue and analysed it for N, P The remediation of different pollutants by U. lactuca.
and four metals (Cd, Cu, Pb and Zn) to evaluate if the macroalgae could Technology Pollutant References
potentially be harvested and used as fertilizer. The low concentration of
Living U. lactuca Cd, Pb and/or Hg Henriques et al. (2019)
metals and high concentration of N and P in the tissue of U. lactuca
Cd, Cr and Pb Kamala-Kannan et al.
demonstrate that this alga may be used as a fertilizer or composted if (2008)
harvested. As, Cd, Pb, Cu, Cr, Hg, Mn Henriques et al. (2019)
The results published concluded that the use of U. lactuca as bio and Ni
Hg Henriques et al. (2015)
monitor is suitable, due to its unique characteristics and for providing a
Pt(II), Pt(IV) and Pd(II) Cosden et al. (2003)
time-integrated measure of nutrient availability in coastal waters, and Phospate Tsagkamilis et al. (2010)
thus for assessing ecosystem health about eutrophication. Poultry manure Agarwal et al. (2020)
N compounds and Elizondo-González et al.
3. Macroalgae remediation potential phosphorus (2018)
Ammonia Cohen and Neori (2021)
Wastewater of a land-base Macchiavello and Bulboa
The presence of a variety of organic and inorganic contaminants in abalone culture (2014)
wastewater is an environmental problem worldwide and its remediation Nitrate and phosphate Tremblay-Gratton et al.
has become a major issue in order to maintain adequate water quality (2018)
U. lactuca derived Remazol Brilian Orange 3 (R Ravindiran Gokulan
for the environment and human health (Bancon-Montigny et al., 2019;
biochar R et al., 2019)
Chaudhuri et al., 2007; Köck-Schulmeyer et al., 2019; Pérez-Fernández Cr El-Sikaily et al. (2007)
et al., 2019; Selman and Greenhalgh, 2009; van Beusekom, 2018). As Cationic dyes Salima et al. (2013)
mention before, the increasing concentration of heavy metals is mainly Remazol dyes (Ravindiran Gokulan
due to industrial discharge; while the discharge of domestic effluents et al., 2019)
Cu(II), Cr(III), Cd(II), and Ibrahim et al. (2016)
and agricultural activities are the main responsible for eutrophication, Pb(II)
algae blooms, and in a great extent the presence of POPs in natural U. lactuca dead Cu(II), Zn(II), Cd(II) and Areco et al. (2012)
waters, which significantly disturbs marine life due to their toxic and biomass. Adsorption Pb(II)
accumulative natures (Chakraborty et al., 2014; Corales-Ultra et al., Ni(II) Long et al. (2018)
Ni(II), Cu(II), Cd(II) and (Zakhama et al., 2011)
2019; Satheeswaran et al., 2019). The impact of polluted discharges on
Pb(II)
the environment depends not only on their characteristics, such as Glyphosate and Cu(II) Trinelli et al. (2013)
biochemical oxygen demand, but also on the content of specific organic Phenol Abbas et al. (2019)
and inorganic substances. The legislation and public concern for the Synthetic azo dye El Nemr et al. (2006)
environment have led scientist to develop new techniques for effluent Methylene blue and Deokar and Sabale (2014)
malachite green
treatment.
6
and the chemical form in which they occur, as was mentioned earlier in by algal biomass and other types of natural biosorbents is ion exchange
the present chapter. One of the main mechanism of metal cation (Davis et al., 2003). This process is a reversible chemical reaction that
adsorption is the formation of complexes between the metal ion and a takes place when an ion of a solution is exchanged for another of the
functional group present on the surface or within the porous structure of same sign, which is attached to a functional group so changes in the
the biological material (Fourest et al., 1996). A site can be occupied by a ionic strength of the solution modified the adsorption process. This
metal ion present in the solution when the bonding strength of the metal process takes place continuously in nature, both in inorganic material as
is greater than the ion, which is previously adsorbed. The occupancy of in living cells.
the surface depends on the total number of surface sites, the free ion The Ulva gender macroalgae contain three polysaccharides: starch,
concentration in solution, the pH and temperature. Most binding sites in cellulose and anionic compounds containing sulfate groups, the last two,
biosorption have acid-base properties (hydroxyl, carboxyl, sulfide, sul are cell wall components. Chlorophyll a and b are also present as well as
fonate, phosphonate), are neutral when they are protonated and nega some carotenoids such as the β-carotene (Paradossi et al., 1999). Ulvan
tively charged when deprotonated. When the pH of the solution exceeds is a cell wall polysaccharide that contributes from 9 to 36% dry weight of
the pKa of the groups, a larger number of binding sites are deprotonated the biomass of Ulva. (Kidgell et al., 2019). They are highly sulfated and
and under these conditions the adsorption of cations is favoured (Trinelli essentially composed of rhamnose 3-sulfate, xylose, xylose 2-sulfate,
et al., 2013). glucuronic acid, and iduronic acid units (Lahaye and Robic, 2007).
The composition of ulvan depends on the source species,
eco-physiology, and processing procedures used to prepare both
3.1. U. lactuca heavy metal remediation potential biomass and ulvan (Kidgell et al., 2019). An example is shown in Fig. I
(Areco et al., 2020).
Different alternatives using U. lactuca biomass to remove heavy The functional groups on the sorbent surface are usually investigated
metals have being published (Henriques et al., 2019, 2017b; Ibrahim by IR and FTIR spectroscopy. Scanning Electron Microscopy with X-ray
et al., 2016, among others). Most research are focused on the remedia microanalysis (SEM/EDS) are used to study the morphology of the
tion potential of mono-metallic solutions. The fact that live macroalgae adsorbent, before and after adsorption of metals, and provide quanti
can simultaneously remove different metals is an interesting aspect tative analysis of elemental composition, SEM/EDS may also show the
because real waters are complex systems, containing different ions that elemental distribution in a sample surface (Areco et al., 2020).
affects the removal capacity of a particular ion. Henriques et al. (2019) Fig. II A and B, show the amorphous superficial structure at two
exposed the capabilities of living U. lactuca, to remove As, Cd, Pb, Cu, Cr, different magnifications (A: 1000X and B: 5000X) of U. lactuca. where
Hg, Mn and Ni from contaminated waters. Their results demonstrated adsorption processes take place. Fig. III, A-E (images were taken by the
for the first time the capacity of living U. lactuca to remove simulta authors) are the EDS analysis of the elemental composition of the
neously several top-priority hazardous substances (As, Pb, Hg and Cd) macroalgae surface, before and after the adsorption process of Cd(II), Pb
and other trace elements (Ni, Cr, Cu and Mn). Besides, the capacity of (II), Cu(II) and Zn(II), respectively. These results demonstrate that: 1)
U. lactuca to remove those elements from water was practically unaf heavy metals are not present in the surface of the macroalgae before
fected by salinity, which can interfere in the performance of conven adsorption experiments (Fig. III A); and 2) U. lactuca adsorbs Cd(II), Pb
tional treatment procedures (Adeli et al., 2017). These results (II), Cu(II) and Zn(II) (Figs III B-E, respectively).
demonstrate the high metal removal efficiency, and the fact that
U. lactuca is broadly distributed, abundant, and easily harvested, sup
port the hypothesis that macroalgae-based technologies may be a viable, 3.2. U. lactuca persistent organic pollutant remediation potential
low-cost, and greener option to reduce the rejection of priority haz
ardous substances in contaminated waters. As previously mentioned in section 1.2. POPs are currently or were in
Another predominant mechanism in the biosorption of heavy metals the past used as pesticides, solvents, pharmaceuticals, and industrial
Fig. 1. Structure of glucuronic acid attached to rhamnose 3-sulfate.
7
Fig. 2. U. lactuca’s SEM images at two magnifications (A: 1000X y B: 5000X) and 5 KV.
Fig. 3. EDS images of U. lactuca: before treatment (A); and after Cd(II), Pb(II), Cu(II) and Zn(II) adsorption (B), (C), (D) and (E), respectively, at pH 5.5 and constant
ionic strength.
chemicals. Even though U. lactuca have demonstrated to be a good Cheng et al. (2020) have synthesized porous graphitized nitrogen-doped
bioindicator for POPs contamination, little have been published biochars from macroalgae, such as U. lactuca, with simple one-pot
regarding its ability to remove them from the environment. In this sense, carbonization, for its applicability for the removal of organic
8
pollutants, such as naphthalene, acenaphthene and phenanthrene from high levels in tissue (Roleda and Hurd, 2019). In this sense, as previously
water. Reports of sorption mechanisms (Xiao et al., 2018) suggest that mentioned, U. lactuca has a high growth rate and N and P uptake
the properties of biochars can be improved to further enhance PAHs (Tremblay-Gratton et al., 2018). The high uptake of nutrients by this
removal by selecting appropriate raw materials, such as macroalgae, or macroalgae may be attributed to its inherent capability of bioremedia
by modifying biochars with various chemical agents. Hence, as the tion. Knowing this, many studies have been published (Azman et al.,
abundant, available and low-cost macroalgae, the resource utilization of 2014; Cole et al., 2016; Ge and Champagne, 2017; Mawi et al., 2020; S.
U. lactuca as biochars is feasible and could greatly reduce the potential Qiu et al., 2017, among others) were micro and macroalgae were
environmental burden (Cheng et al., 2020). cultivated in waste waters in order to reduce the use of fresh water and
Other organic pollutants commonly found in nature environments the addition of salts, while remediating the wastewaters and diminish
are dyes. Organic dyes are considered as serious water pollutants. There ing the costs associated with culture growth and maintenance. Also,
are several ways for removal of these compounds from environment, there are studies describing the capability of U. lactuca to selectively
which are mainly based on biological, chemical, and physical methods. remove nitrate, ammonium or phosphate from waters and sediments
Gokulan et al. (2019; 2019) have demonstrated U. lactuca’s ability to (Lubsch and Timmermans, 2018; Macchiavello and Bulboa, 2014; Van
remediate Remazol in an up-flow column packed with U. lactuca-derived Alstyne, 2016, among others).
biochar. Deokar and Sabale (2014) studied the adsorption of methylene In this sense, Agarwal et al. (2020), studied the remediation of a
blue and malachite green onto dried biomass of U. lactuca, showing that poultry litter by U. lactuca. Seaweed showed 80–100% nutrient uptake
the adsorption might involve monolayer surface coverage and hetero efficiency for 4-day experiment and total nitrogen decreased by 82.6%,
geneous adsorption mechanism. Thus, the alga can be used as a low-cost while the ammonia concentration was observed to reduce by 100%.
adsorbent for removal of both dyes from a binary mixture. Other authors Also, all the residual phosphate was removed from the solution. The
studied the remediation of malachite green with similar results (Omar total organic carbon (TOC) was reduced from 73.4 ppm to 11.7 ppm
et al., 2018). El Nemr et al. (2006), studied the capacity of this macro with corresponding decrease in COD value. Some researchers showed
algae to remediate a synthetic azo dye (Direct Yellow 12 DY-12). The that U. lactuca can remove ammonia from water and sediments as part of
results obtained from the batch experiments revealed that the ability of a toxicity identification and evaluation procedure (Ho et al., 1999; Sode
the U. lactuca to remove DY-12 from its aqueous solution was dependent et al., 2013) contributing to its growth (Van Alstyne, 2016).
on the dye concentration, pH, and algal biomass but less dependent on Other authors tested the nutrient remediation capacity of this mac
the particle size of the macroalgae. roalgae in aquaculture systems. Results published by Gonzalez et al.
U. lactuca was also studied for its potential to remediate glyphosate (2018) revealed the high efficiency of U. lactuca in removing nitrogen
(PMG), an organophosphorus, broad-spectrum, post-emergent, non- compounds and phosphorus from shrimp’s wastewater (80% and 64%,
selective herbicide used for more than 40 years in over 140 countries. respectively) under the integrated recirculation system. Lubsch and
Because of the widespread use of agricultural chemicals in food pro Timmermans (2018), have demonstrated that U. lactuca may remove (by
duction, people are exposed to low levels of pesticide residues through metabolic and nonmetabolic processes) all the dissolved inorganic
their diets. The extensive use of PMG-based herbicides has led scientists phosphorous and nitrogen present in solution at a high rate.
to develop new ways of degrading PMG in order to remove the Fed aquaculture (e.g. fish and shrimp) in coastal areas throughout
remaining herbicide in soils and waters. A new approach to PMG the world has serious environmental impacts. Aquaculture waste, such
remediation is given by the adsorption of the herbicide onto biological as fish excretion and faeces, rich in inorganic nitrogen (N) and phos
materials mediated by metal adsorption (Huguenot et al., 2010; M.A. phorus (P), may significantly contribute to the nutrient loading of
Trinelli et al., 2013). In this sense, Trinelli et al. (2013) study the coastal waters leading to problems of considerable concern, including
adsorption of PMG onto green macroalgae U. lactuca mediated by Cu(II). coastal eutrophication, loss of biodiversity and diseases (Diana et al.,
Results demonstrate that PMG adsorption only occurs if the copper 2013). Integration of invertebrates or finfish aquaculture with seaweeds
adsorption equilibrium is previously established so the presence of metal culture can be considered a practice for bioremediation of the nutrient
is critical to produce the anionic ligand anchor on the surface, which laden effluents. The enhanced water quality in these systems leads to
probably occurs by covalent coordination through phosphonate groups improved fish performance and higher biomass production, and to
as it happens on mineral surfaces. Also, Trinelli et al. (2019) have reduction in the energy power used, contributing to greater profitability
studied the photodegradation of glyphosate (PMG) in aqueous solution (Cunha et al., 2019). Besides its ecological aspect, integrated aquacul
by the action of UV-light and the catalytic effect of copper and ture also has economic incentives as the nutrients contained in effluents,
copper-alga U. lactuca, and they have demonstrated that the rate of PMG such as N and P, could be channelled into the production of valuable
degradation is increased by the presence of copper and Cu-alga products, as algal biomass (Alemañ et al., 2019; Dominguez and Loret,
U. lactuca in the reaction media. 2019; Hurtado et al., 2019; Lubsch and Timmermans, 2018). Numerous
studies have focused on the integration of U. lactuca with fish, shrimp
3.3. U. lactuca nitrogen and phosphorous remediation potential (Calheiros et al., 2019), abalone (Macchiavello and Bulboa, 2014), ur
chin (Shpigel et al., 2018) and mussel (Nardelli et al., 2019), demon
As previously mentioned U. lactuca can be used as bioindicators of strating the benefits in size and growth rate in animals.
nutrients in the water column as their ability to assimilate surrounding All results confirm the high efficiency of Ulva species in bio-filtering
nutrients is rapid, which is clearly reflected by their tissue nutrient of nutrients because of their high efficiencies in absorbing and metab
content within a relatively short period of time (Sutula, 2011). The olize different forms of inorganic nitrogen, mainly nitrate and ammo
demand and management strategy for nutrients by seaweeds is nium, and phosphorous from aquaculture effluents (Elizondo-González
economically and ecologically of central importance, as it allows et al., 2018; Nardelli et al., 2019; S. Qiu et al., 2017; Shpigel et al.,
optimal manipulation in cultivation and bioremediation applications 2019).
(Gao et al., 2017). Besides the economic value of macroalgae, seaweed An interesting aspect from the economic point of view is to find a use
farming can have positive environmental impacts because it makes use for Ulva biomass obtained in remediation processes. In this sense,
of nutrient emissions from anthropogenic nitrogen and phosphorous biomass of U. lactuca can be utilized for their nutritive value for animal
sources that enter the ocean and it can also take up anthropogenic feed e.g. flies, abalones and sea urchins, which is another advantage of
carbon dioxide emissions that cause ocean acidification (Roleda and its cultivation (Dworjanyn et al., 2007; Kamio et al., 2016; Laramore
Hurd, 2019). The selection of seaweed species for their commercial use et al., 2018; S. Qiu et al., 2017; Wan et al., 2019). A study demonstrated
as biofilters depends on several aspects: the commercial value, a rapid that Ulva cultivated under high nutrients offers a sustainable source of
growth in culture conditions and the capacity to accumulate N and P at biomass for n-3 PUFA, pigments and phenolics with attributable
9
anti-oxidant and anti-inflammatory activity (McCauley et al., 2018). waters. Furthermore, their potential has also been attended by the Eu
Besides, U. lactuca has demonstrated potential for energy production ropean Union’s Horizon 2020 research and innovation program, that
(Bruhn et al., 2011). Pilot studies indicated that the yearly yield of Ulva has funded projects involving partners from different countries, where
lactuca is 4–5 times greater than terrestrial energy crops with a methane macro and microalgae are applied for the development of algae-based
yield at a level between cow manure and energy crops (Bruhn et al., technologies.
2011).
Funding
3.4. U. lactuca emerging pollutants remediation potential
This work was supported by Consejo Nacional de Investigaciones
The presence of rare earth elements (REEs) such as yttrium, Científicas y Técnicas (CONICET) (PIP 11220170100770CO).
lanthanum, cerium, praseodymium, neodymium, europium, dyspro
sium, among others, in natural environments, are the consequence of Conflicts of interest
methods currently used for the extraction of metals from solid wastes or
from liquid wastes such as acid mine drainage or industrial wastewaters Not applicable.
(Pinto et al., 2020). Recently, REEs concentration in aquatic ecosystems
has been increasing due to their application in modern technologies Availability of data and material
(Costa et al., 2020). According to the study of Zoll and Schijf (2012),
U. lactuca shows a high affinity for yttrium and the rare earth elements Review. All the literature is depicted in the manuscript.
and it might be an ideal biomonitor or biofilter of REEs contamination in
environments with different degrees of salinity. Also, other results Code availability
published indicate that U. lactuca may remove all REEs with efficiencies
up to 90% (Pinto et al., 2020; Viana et al., 2021), even in Not applicable.
multi-elemental solutions (Pinto et al., 2021).
Microplastics are considered emerging contaminants and, conse Authors’ contributions
quently, the concern about their potential impacts has grown expo
nentially in the last decade (Mateos-Cárdenas et al., 2021). A few studies All authors contributed to the present article. Dr. Areco and Dr.
on the impact of microplastics on macroalgae have been published (Feng Salomone contributed to the study conception, design, and the organi
et al., 2020; Saley et al., 2019; Seng et al., 2020, among others). zation of the information. Data collection were performed by Dr. Maria
Although there are still scarce studies on the mechanism, by which Mar Areco and Dr. Vanesa Salomone. The first draft was written by Dr.
macroalgae incorporate microplastics into their structure, the prevailing Maria Mar Areco and all authors commented on previous versions of the
mechanism would be external adsorption, mainly of microfibers, on the manuscript. Final version was evaluated by Dr. Maria dos Santos Afonso.
entire surface of macroalgae (Li et al., 2020). In accordance with these All authors have read and approved the final manuscript.
results, Sundbæk et al. (2018) found that microplastic particles present
on F. vesiculosus, decreased 94.5% after washing the macroalgae. The Consent to participate
effects of microplastics on U. lactuca have been little reported in litera
ture (Rødland, 2019) and their removal by this macroalgae have not Not applicable.
been reported yet.
Consent for publication
4. Conclusions
Not applicable.
Macroalgae have been recognized as bioengineer organisms. In this
sense many studies agree that U. lactuca has numerous features that Declaration of competing interest
makes it suitable to be used for environmental applications: it wide
spread distribution; high growth rates in normal conditions and in The authors declare that they have no known competing financial
eutrophic waters; resist high variations of salinity; has high rates of interests or personal relationships that could have appeared to influence
nutrient assimilation; and tolerates different pollutants under toxic the work reported in this paper.
conditions. These characteristics would allow to set up large-scale ma
rine monitoring programs. Nevertheless, most of the naturally produced References
and harvested U. lactuca biomass is an unused resource, that could be
used for numerous biotechnological purposes. In this sense, many au Abbas, M.N., Al-Hermizy, S.M.M., Abudi, Z.N., Ibrahim, T.A., 2019. Phenol biosorption
thors studied the capacity of U. lactuca for biomonitoring purposes, as a from polluted aqueous solutions by Ulva lactuca alga using batch mode unit. J. Ecol.
Eng. 20, 225–235. https://doi.org/10.12911/22998993/109460.
bioindicator of contamination and for the remediation of different pol Abdelfattah, I., Ismail, A.A., Sayed, F. Al, Almedolab, A., Aboelghait, K.M., 2016.
lutants. The results published concluded that the use of U. lactuca as Biosorption of heavy metals ions in real industrial wastewater using peanut husk as
biomonitor is suitable, due to these unique characteristics, providing a efficient and cost effective adsorbent. Environ. Nanotechnology, Monit. Manag. 6,
176–183. https://doi.org/10.1016/j.enmm.2016.10.007.
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Ulva Lactuca Un Bioindicador de La Contaminación Antropogénica y Su Capacidad de Remediación Ambiental

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Marine Environmental Research 171 (2021) 105468

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Marine Environmental Research

Ulva lactuca: A bioindicator for anthropogenic contamination and its

1. Introduction pollutants (POPs) are of major environmental concern due to their

Fig. 1. Structure of glucuronic acid attached to rhamnose 3-sulfate.

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