Ecophysiological and cellular stress responses in the cosmopolitan brown macroalga Ectocarpus as biomonitoring tools for assessing desalination brine impacts
Introduction
In the last decades, terrestrial water fluxes have been severely affected by direct anthropogenic intervention (e.g. water withdrawals from domestic, agricultural, and industrial activities) [1]. On the other hand, Climate Change driven by massive emissions of greenhouse gases, among others, have been changing the distribution of the weather patterns all over the globe and influencing water cycle dynamics, causing an important impact in water availability and demand worldwide [2,3]. To address the latter, seawater desalination via reverse osmosis (SWRO), has become a feasible solution, which comprises the removal of salt and minerals from saline water. Nowadays, approximately 7% of the world's population is dependent on desalinated water for daily purposes, but it is expected to grow up to 14% by 2025, and 25% by 2050 (United Nations, 2015, [4]). However, and despite the important use of desalination, this procedure may cause impacts on coastal ecosystems, since it can generate large quantities of high salinity brines that are usually discharged into the subtidal zone [5,6]. As brine is denser and twice saline than seawater, it sinks to the bottom and can cause detrimental effects on benthic organisms, mainly through osmotic stress [7,8]. It has been observed that brine-associated impacts are highly species- and ecosystem-specific; thus, the consequences of brine discharges recorded by research so far cannot be directly extrapolated to the impacts caused by desalination projects worldwide [7]. Moreover, different investigations have evidenced that biological stress mediated by brines is principally related with osmotic stress derived from the excess of salt [[9], [10], [11]].
Despite the long history of desalination plants worldwide, most environmental impact data available is related with ecological effects (e.g. [6,[12], [13], [14]]). Available studies demonstrate that the ecological impacts of the hypersaline stream are influenced by several factors including salinity levels, discharge method, dilution rate and tolerance of surrounding marine organism [7,15]. For example, sensitive benthic fauna has been identified, as certain polychaeta [16] and equinoderms [17]. Also, different brine tolerance ranges were observed in reef-building corals species, as well as in associated bacteria; for example, triggering partial coral bleaching [13]. Other study demonstrated that benthic bacteria can be affected by brine effluents in a site-specific manner, where discharge method and local stressors influenced the abundance and diversity of these communities [18]. In photoautotrophs, laboratory approaches have shown that saline excess above 39.1 psu versus control value of 37.5 psu (average Western Mediterranean Sea salinity) results in a reduction of the seagrass Posidonia oceanica vitality, in terms of leaf grow, necrotic spots, and leaves premature senescence; moreover, when exposed to 45 psu, approximately 50% of the seagrasses died in two weeks [19]. Similar results were obtained with the Mediterranean seagrass Cymodocea nodosa, which showed detrimental effects when exposed to increased salinities in laboratory-controlled conditions [20], and during in situ transplantation nearby brine discharges [21]. Also, field experiments nearby a pilot desalination plant in Spain demonstrated the same tendency as the laboratory experiments, disclosing significant damages on P. oceanica viability (at 38.4 psu) and meadow structure (at 39.1 psu) [22].
Until now, most research on the effects of brines on coastal macrophytes has been restricted to seagrasses and their communities; however, no studies have described yet brine impacts on other ecologically-relevant macrophytes, such as macroalgae. Macroalgae (seaweeds) are main primary producers and bioengineers in coastal environments from inter-tropical to polar latitudes [23]. Considering the important biological role of brown macroalgae as habitat forming organisms (e.g. kelp forests) in temperate coastal rocky shores worldwide, and the lack of knowledge about the potential detrimental impact of the desalination industry on them, it is highlighted as a relevant research subject to understand their response mechanisms to address hypersalinity, as well as to extrapolate those to potential ecological and economic consequences.
Peters et al. [24] proposed Ectocarpus sp. (formerly Ectocarpus siliculosus, and henceforth referred as Ectocarpus) as a general model organism for the study of brown macroalgae. Features include its small size, high fertility, rapid growth and the fact that the entire life cycle can be completed under controlled laboratory conditions; these aspects not only makes Ectocarpus a reliable model organism for macroalgae, but also a good prospect to biomonitor anthropogenic impacts. Ectocarpus has been previously used as a biomonitoring organism in order to address the consequences of metal pollution through combined laboratory and field transplantation experiments [[25], [26], [27]], thus, is highlighted as suitable to address for other impacts; e.g., desalination brine discharges.
In this study, we analysed the ecophysiological (photosynthetic activity) and metabolic (oxidative stress damage and tolerance) responses of Ectocarpus, through in situ transplantation experiment to evaluate the space-temporal exposure against brine discharges from a desalination plant, in order to understand tolerances strategies and potential damage; and evaluate these as potential tools for monitoring brine impacts.
Section snippets
Ectocarpus culture
Ectocarpus strain Es524 (Culture Collection of Algae and Protozoa CCAP 1310/333), isolated from Caleta Palito, Chañaral (26°16′29.2″S; 70°39′38.4″W), Chile, was grown in polycarbonate flasks (10 L, Nalgene), using clean filtered and autoclaved seawater enriched with Provasoli nutrients [28], and with a filtered stream of air continuously circulating (0.2 μm pore size filter). Growth conditions comprised a photoperiod of 12 h/12 h light/dark, 120 μmol photons m2 sec−1, and 16 °C constant
Salinities and photosynthetic activity as in vivo chlorophyll a fluorescence
Salinities recorded to site 1, site 2 and control site, shown in Table 1. Salinities in site at 10 m and at 30 m from the discharge were 2.38 and 1.5 psu higher, respectively, compared to that in the control site.
The electron transport rate (ETR) was analysed as a productivity indicator in Ectocarpus samples exposed to the brine effluent (Fig. 2). ETR at day 3 decreased considerably in samples located at 10 m and 30 m from the brine discharge pipe compared to control samples (Fig. 2A). After
Discussion
Studies, protocols and strategies to monitor the biological consequences of desalination brine discharges are still not fully optimized to be reliably incorporated into environmental monitoring programmes. Nevertheless, most of those are limited to survival rates, growth, and effects on community structure. To the extent of our knowledge, this is the first study encompassing physiological, metabolic and molecular aspects in response to direct exposition of brine effluents from a desalination
Conclusions
In this study, we demonstrated for the first time that short-term brine exposure from desalination industry can provoke detrimental effects at the ecophysiological and cellular level, principally in terms of hypersalinity and oxidative stress, using transplants of a macroalga species. In this sense, we suggest that the best physiological and molecular biomarkers for Ectocarpus transplants include: photosynthetic parameters such as Fv/Fm, αETR, and ETRmax; oxidative stress parameters as H2O2 and
CRediT authorship contribution statement
Fernanda Rodríguez-Rojas:Conceptualization, Investigation, Methodology, Formal analysis, Writing - original draft.Américo López-Marras:Investigation, Methodology, Formal analysis.Paula S.M. Celis-Plá:Investigation, Methodology, Formal analysis.Pamela Muñoz:Investigation, Methodology.Enzo García-Bartolomei:Investigation, Writing - review & editing.Fernando Valenzuela:Investigation.Rodrigo Orrego:Investigation, Writing - review & editing.Adoración Carratalá:Investigation, Writing - review &
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgement
This work was funded by the postdoctoral fellowship #3180394 granted by Fondecyt program (CONICYT), Chile, to FRR. EGB was funded by CONICYT doctoral scholarship #21171486 and a IDA Channabasappa Memorial Scholarship.
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These authors contributed equally to the investigation.