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Article

The Use of Aquatic Macrophytes as a Nature-Based Solution to Prevent Ciprofloxacin Deleterious Effects on Microalgae

by
Rafael Shinji Akiyama Kitamura
1,
Tayna Fusaro
2,
Raizza Zorman Marques
2,
Julio Cesar Moreira Brito
3,
Philippe Juneau
4 and
Marcelo Pedrosa Gomes
2,*
1
Ecology and Conservation Post-Graduation Program and Department of Genetics, Federal University of Paraná, P.O. Box 19031, Curitiba 81530-980, PR, Brazil
2
Plant Stress Physiology Laboratory, Department of Botany, Federal University of Paraná, P.O. Box 19031, Curitiba 81530-980, PR, Brazil
3
Fundação Ezequiel Dias, Rua Conde Pereira Carneiro, 80, Belo Horizonte 30510-010, MG, Brazil
4
Ecotoxicology of Aquatic Microorganisms Laboratory, GRIL, EcotoQ, TOXEN, Department of Biological Sciences, Université du Québec à Montréal, Succ. Centreville, C.P. 8888, Montreal, QC H2C 3P8, Canada
*
Author to whom correspondence should be addressed.
Water 2023, 15(12), 2143; https://doi.org/10.3390/w15122143
Submission received: 19 April 2023 / Revised: 29 May 2023 / Accepted: 2 June 2023 / Published: 6 June 2023
(This article belongs to the Special Issue Environmental Feedbacks between Global Changes, Contaminants and Aquatic Plants)
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Abstract

:
Macrophytes have demonstrated excellent potential for the removal of pharmaceuticals from water. However, there is a lack of studies on the ecotoxicity of water after phytoremediation. In this study, we evaluated the toxicity of ciprofloxacin (Cipro) on the microalgae cells of Desmodesmus subspicatus exposed to water contaminated with Cipro and previously treated by Salvinia molesta or Egeria densa for 96 h. Microalgae exposed to Cipro (1, 10, and 100 µg L−1) in untreated water showed decreased rates of growth, respiration, and photosynthesis, and increased oxidative status (hydrogen peroxide concentration) and oxidative damages (lipid peroxidation). S. molesta exhibited a greater phytoremediation capacity than E. densa, reducing Cipro concentrations in water to below its toxic threshold to D. subspicatus (2.44 µg L−1), even when the antimicrobial was present at a concentration of 10 µg L−1. During the water treatment, neither S. molesta nor E. densa released compounds that had a toxic effect on D. subspicatus. This work demonstrates the novelty of using S. molesta and E. densa as a nature-based solution to remove Cipro from contaminated water. For the first time, we provide evidence of the ecotoxicological safety of this approach, as it prevents the deleterious effects of Cipro on photosynthetic microorganisms and helps to avoid the development of antimicrobial resistance.

1. Introduction

Ciprofloxacin (Cipro) is an antimicrobial belonging to the fluoroquinolone class that is often found in aquatic systems [1,2,3]. Its incorrect disposal and excessive use associated with the inefficiency of wastewater treatment plants to remove antimicrobials during water treatment have contributed to water contamination [4,5]. The presence of Cipro in ecosystems is of growing concern, mainly due to the possibility of inducing resistance in bacteria [2,6,7], which is recognized as one of the major threats to global public health in the 21st century [2]. Global surveillance studies demonstrate that fluoroquinolone resistance rates increased in the past years, causing several public health problems. Fluoroquinolone resistance rates in some pathogenic species, such as Neisseria gonorrhoeae, are highly variable and can be as high as almost 100% [8]. In addition to antibiotic resistance, at environmental representative concentrations, Cipro has shown toxicological effects to non-target aquatic [9,10,11,12,13] and terrestrial organisms [14,15]. Therefore, it is urgent to develop technologies aimed at removing Cipro from the environment.
Aquatic organisms are particularly vulnerable to Cipro toxicity as this antimicrobial is commonly introduced into waterways due to the disposal of contaminated sewage. At environmental representative concentrations, Cipro induced genotoxicity, histopathologic, hematologic, and biochemical alterations in fish [9,13,16,17,18]. In tadpoles, the antimicrobial exhibited teratogenic potential caused locomotor changes, and induced oxidative damage [11]. Photosynthetic organisms also showed reductions in primary metabolism (photosynthesis and cellular respiration) and biochemical alterations in response to Cipro exposure, as observed in microalgae [19] and plants [12,20,21,22,23]. Despite the ecological risks and proven toxicity to non-target organisms, there are still no regulations governing the environmental monitoring of Cipro in aquatic systems [3,24,25,26]. Therefore, the scientific community has stressed the importance of applying technologies, particularly to wastewater treatment systems, to remove antimicrobials from water and prevent their possible toxic effect on biota. However, physicochemical technologies with proven efficiency are often expensive and may be unaffordable for many municipalities [27]. As a result, nature-based solutions (NbS) have then emerged as a possibility to reduce water contamination by Cipro.
Phytoremediation is an NbS that has gained attention to its comparable or greater efficiency and lower cost compared to physicochemical technologies for removing antimicrobials from water [10,12,28,29,30,31]. This technique involves using plants to stabilize, accumulate, degrade, and/or transform contaminants into their biomass, with or without the involvement of associated microorganisms [29,31,32,33]. Aquatic macrophytes have demonstrated high efficiency in removing Cipro from water and their use in phytoremediation is gaining increasing attention. For instance, after just 96 h, the floating macrophyte Salvinia molesta and the submerged macrophyte Egeria densa were able to remove over 58% of Cipro from the media, with up to 90% removal efficiency after 168 h of exposure [12]. Other macrophyte species such as Elodea canadensis [34], Ricciocarpus natans [23], Eichhornia crassipes [35,36,37], and Lemna minor [21,38] have been also indicated for phytoremediation of waters contaminated by fluoroquinolones.
Although plants can be used to remove antimicrobials from water, some aquatic macrophytes produce and release allelochemicals into the water during the depuration process, which may constrain the growth of other organisms [39,40]. In this context, after being remediated for antimicrobial removal, water treated with plants can present secondary plant products that can affect aquatic organisms, in addition to the antimicrobial. However, very few studies have evaluated the ecotoxicity of water after posttreatment using phytoremediation [10]. Recently, we demonstrated that the phytoremediation capacity of Salvinia molesta prevents the harmful effects of Cipro on neotropical catfish and risks to human health [10]. To the best of our knowledge, however, no study has evaluated the toxicity of water treated by phytoremediation to photosynthetic organisms. Therefore, we evaluated the toxicity of Cipro-contaminated waters treated with the aquatic macrophytes Salvinia molesta and Egeria densa on the microalgae Desmodesmus subspicatus. Both S. molesta and E. densa species have been indicated for phytoremediation purposes, including the removal of antimicrobials [12,41,42]. However, these plants are also known for their ability to produce allelochemicals that can have detrimental effects on aquatic organisms [43,44,45]. The microalgae D. subspicatus was chosen as the model species for this study due to its easy culture, short reproductive cycle, and sensitivity to different contaminants [46]. As a primary producer, D. subspicatus plays a vital role in the aquatic food chain and is an important organism to study when assessing the potential ecological impacts of contaminants on aquatic ecosystems [46]. We compared the toxicity of Cipro to the microalgae with cells exposed to contaminated water previously treated by S. molesta or E. densa for 96 h. We hypothesised that the macrophytes removed enough Cipro and did not release any toxic compounds into the water, thereby decreasing the toxicological effects of Cipro on the microalgae. In addition to improving our understanding of the toxicological effects of Cipro on non-target organisms, our study aims to explore the potential use of S. molesta and E. densa in phytoremediation programs for Cipro as an NbS to improve water quality and sanitization, both of which are essential components of the Sustainable Development Goals [47,48,49,50,51].

2. Materials and Methods

2.1. Cultures

Salvinia molests DS. (Mitch) plants were collected from Barigui Park (Curitiba, Brazil, 25°25′18″ S; 49°18′22″ W) while Egeria densa Planch. plants were collected from the Guraraguaçu River (Paraná, Brazil, 25°40′19.95″ S; 48°30′47.20″ W). Before the start of the experiments, the macrophytes were acclimated and depurated in reconstituted water (5.298 μM CaCl2, 2.044 μM MgSO4, 1.500 μM NaHCO3, and 0.7377 μM KCl in ultrapure water) under controlled temperature (25 ± 2 °C) and photoperiod (10/14 h; 80 μmol photons m2·s−1) conditions for a period of 30 days. Desmodesmus subspicatus (Chodat) E. Hegewald and A. W. F. Schmidt were obtained from the cultures held at the Laboratory of Stress Plant Physiology of the Federal University of Paraná (Curitiba, Brazil). Stock cultures of microorganisms were in an exponential growth phase and were kept in 250 mL sterile Erlenmeyer flasks containing CHU10 medium (pH 7.30 ± 0.50). The flasks were incubated in a growth chamber at a controlled temperature of 24 ± 2 °C under a 10/14 h photoperiod with a light intensity of 45 μmol photons m2·s−1.

2.2. Bioassays

2.2.1. Phytoremediation Using Aquatic Macrophytes

For the bioassays, the plants were transferred to 250 mL Erlenmeyer flasks (each constituting one replicate) containing 100 mL of sterile reconstituted water with appropriate concentrations of Cipro. The flasks were stoppered with cotton wool to avoid evaporation and contamination. A density of 10 g plants L−1 was used for macrophyte species. To achieve this, the plants were centrifuged at 3000 rpm for 10 min at room temperature (in centrifuge tubes with small holes to remove surface water) and weighed to determine their fresh weights [52]. The plants were then distributed in the flasks based on the proportion of plant weight to medium volume. The E. densa apices were cut from the stems of mature plants, from the apex in the direction of the base, to obtain the 1 g plant weight including the apex. Four replicates per species for each Cipro concentration were tested. The bioassays had a duration of 96 h and were conducted in biological oxygen demand chambers under the same temperature and illumination conditions as the acclimatization of macrophytes. Macrophytes were exposed to different Cipro concentrations: 0 (Control), 1, 10, and 100 μg L−1. Parallel experiments were conducted in flasks without plants (n = 4) to study the natural degradation of Cipro.
To evaluate phytoremediation capacity, water samples were taken at the initial and at the end of the exposure time for Cipro evaluations. For that purpose, water samples were collected and stored in Falcon tubes under refrigeration at 4 °C until the analysis. Subsequently, Cipro detection and quantification were performed according to Shi and collaborators [53] with a modification in the mobile phase proposed by Kitamura et al. [12] by high-efficiency liquid chromatography (Waters 2695 HPLC, Milford, MA, USA) coupled to a fluorescence detector (FD 2475, Waters) [53,54]. The fluorescence wavelengths analyzed were 278 nm for excitation and 453 nm for emission. Analytical-grade Cipro (United States Pharmacopeia, Rockville, MD, USA) was used in bioassays to establish the calibration curves. The curves were composed of six points and demonstrated good linearity for the analyte (r2 = 0.999; p < 0.0001). For the calculation of Cipro concentration, a linear equation was used (y = 11,800 x − 6572.7, in which: y = Cipro concentration and x = area). For quality control, each batch of samples included three blanks, three standards, and three fortified samples. Recovery rates were 94.4% and the limit of detection and limit of quantification were 0.3 and 1.0 µg Cipro L−1, respectively.
The efficiency of phytoremediation treatment was calculated, according to Gomes et al. [38]), as follows:
D e g r a d a t i o n % = 100 − ( c 2   w i t h o u t   p l a n t s c 1   w i t h o u t   p l a n t s ∗ 100 )
P h y t o r e m e d i a t i o n   e f f i c i e n c y % = 100 − c 2   w i t h   p l a n t s c 1   w i t h   p l a n t s ∗ 100 − d e g r a d a t i o n
In which: c1: is the initial concentration of Cipro in water and c2—is the final concentration of Cipro in water.

2.2.2. Toxicological Evaluations in Microalgae

After removing a volume for chromatographic evaluation, the remaining 50 mL of each flask was collected, and the pH was checked and adjusted to 7.3 when necessary, using 1 M HCl or NaOH. Then the water samples were filtered through a 0.45 µm filter and used in the bioassay with D. subspicatus. Experiments were carried out in 12-well sterile microplates under identical conditions as those previously described for stock cultures. Four wells corresponding to one replicate were used for each treatment. Each well of the microplates was inoculated with a respective volume of the stock culture corresponding to an initial concentration of 1 × 106 cells mL−1 (total culture volume of 5 mL/well). The microplates were incubated in a growth chamber at a controlled temperature of 24 ± 2 °C under a 10/14 h photoperiod with a light intensity of 45 μmol photons m2·s−1.
The microalgae were exposed to the water after treatment with plants (treated media) or to freshly contaminated autoclaved reconstituted water with the same drug concentration used for treatment with macrophytes (Control, 1, 10, and 100 μg L−1). The microalgae were exposed for 96 h, and 3 mL samples were collected for growth evaluations at 0, 48, and 96 h of exposure. At the end of the experiment, the remaining volume was filtered on microfiber filters (grade GF/F—0.45 μm, Whatman Ltd., Maidstone, UK) and used for physiological evaluations (respiration and photosynthesis). Subsequently, the filters were frozen in liquid nitrogen and kept at −20 °C until biochemical analyses (total protein [55], hydrogen peroxide—H2O2 [56] and malondialdehyde concentration—MDA [57], and catalase activity—CAT [58]).
The respiration and net photosynthesis rate (Pn) were measured using an infrared gas system analyzer (CI-340 Photosynthesis System, CID Bio-science, Inc., Camas, WA, USA). The filters containing the cells were first kept in darkness for 20 min, and then the carbon dioxide (CO2) production was measured three times per sample. After that, the filters were exposed to light for 15 min (with a light intensity of 45 μmol photons m2·s−1) and the net rates of photosynthesis were measured three times per sample during each evaluation, again with a light intensity of 45 μmol photons m2 s−1.
Microalgae growth was performed by counting the number of cells in Neubauer chambers under an optical microscope (BIOPTIKA, model 12MP, Belém, Brazil) at an increase of 1000×. To determine the cell concentration, Equation (1) or (2) were used, depending on which quadrant was used for cell counting. Equation (1) was used for cell counts performed in the large quadrants, while Equation (2) was used for the middle quadrants,
y = XA × FD × 104
y = XC × FD × 1.6 × 105
where: y = cell concentration (cells·mL−1); XA = average of the counts between the four fields indicated by the letter A; XC = average of the counts between the five fields indicated by the letter C; FD = factor used for dilutions that are performed (when no dilution is performed, the value is 1).
The daily growth rate (DGR) was calculated considering the initial (0 h) and final (96 h) cell concentrations after exposure to the treatments. DGR was calculated using Equation (3) as follows:
D G R = ( F C − I C ) ( F T − I T ) × 24   ( d a y )
In which: FC = Final cell concentration (96 h); IC = Initial concentration (0 h); FT = Final time (96 h); IT = initial time (0 h).
The inhibition rate (IR) was calculated according to Equation (4) [59]), by comparing the final cell concentrations of the control treatment with the groups exposed to Cipro and macrophyte-treated water.
I R = C c − C t C c × 100
In which: Cc = Cell concentration of the Control group (96 h); Ct = Cell concentration of groups exposed to ciprofloxacin and post-treatment (96 h).

2.3. Data Analysis

The data were tested for normality (Shapiro–Wilk) and homoscedasticity (Levene) and were analyzed using two-way ANOVA. For phytoremediation capacity, the model included interactions between Cipro concentrations (Control, 1, 10, and 100 µg L−1) and macrophyte species (S. molesta and E. densa). For toxicological results, the model included interactions between Cipro concentrations (Control, 1, 10, and 100 µg L−1) treatments (untreated and treated water). When differences were detected by ANOVA, means were compared using the Tukey test at a 0.05% significance level. The data were statistically analyzed using R software (R.3.2.2, Team 2015, USA) and expressed as the mean of four replicates. Graphs were generated using the PRISM software (version 8.01, USA).

3. Results

3.1. Phytoremediation Capacity of Aquatic Macrophytes

No Cipro was observed in water samples of the control treatments (0 µg L−1) (Table 1). The natural degradation of Cipro varied with its concentration in water, ranging from 2.40% to 21.70%, and was greater at the highest Cipro concentration (Table 1). Regardless of the concentration and macrophyte species, lower Cipro concentrations were observed in flasks with plants in relation to flasks without plants (p < 0.001) (Table 1). Greater Cipro phytoremediation efficiency was demonstrated by S. molesta compared to E. densa plants, regardless of the antimicrobial concentration (Table 1).

3.2. Toxicological Effects of Cipro on D. subcapitatus

When D. subspicatus were exposed to untreated-contaminated water, a negative daily growth rate (DGR) was observed in cells treated with Cipro in comparison to the control group, regardless of the antimicrobial concentration (Figure 1, Table 2). As the Cipro concentration increased, the inhibition rate (IR) increased, and the rates of respiration and net photosynthesis decreased (Figure 1; Table 2).
The activity of catalase and the lipid peroxidation (as evaluated by MDA concentrations) increased in cells exposed to Cipro concentrations ≥ 10 µg L−1 in relation to the control group (p < 0.001). Furthermore, exposure to Cipro increased hydrogen peroxide (H2O2) concentrations in cells, regardless of its concentration (Figure 2, Table 2).
Cells grown in water contaminated with 100 µg Cipro L−1 treated with macrophytes showed increased CAT activity compared to the control groups (Figure 2A, Table 2). Lower CAT activity was observed in D. subspicatus cells grown in water contaminated with 10 µg Cipro L−1 and treated with plants as compared to those from the same treatment without plants (Figure 2). Although MDA concentrations were not significantly affected in cells grown in macrophyte-treated water (p < 0.05; Figure 2C, Table 2), the concentration of H2O2 increased in D. subspicatus s cells grown in water contaminated with 100 µg L−1 and treated with E. densa and in water contaminated with Cipro concentrations ≥10 µg L−1 treated with S. molesta (Figure 2B, Table 2).

4. Discussion

Although eukaryotes are not a target of Cipro, exposure to this antimicrobial has been shown to negatively affect several organisms, such as fish [10,13], insects [60], phytoplankton [61], and plants [12,20]. Cipro acts on bacterial topoisomerase II (DNA gyrase) and topoisomerase IV, preventing DNA replication [2,62]. However, the eukaryote freshwater microbial community was more sensitive to Cipro than prokaryotes (cyanobacteria) [63], reinforcing the use of microalgae to test antimicrobial ecotoxicity. In photosynthetic organisms, Cipro impacts mitochondrial activity [12], possibly due to the similarities between mitochondria and prokaryotic organisms (the target of Cipro) [20]. The activities of Complexes I and II in the mitochondrial electron transport chain (ETC) of L. minor plants were particularly sensitive to Cipro, which appears to compete with ubiquinone (UQ) in the quinol-reducing site of Complex III (Center N), leading to reduced activity of the previous enzymatic complexes (I and II) [20]. As a result of the impairment of the initial steps of mitochondrial ETC, there is an overproduction of reactive oxygen species (ROS; i.e., H2O2), which can result in decreased photosynthesis and plant growth [20].
As observed here, once exposed to Cipro in untreated waters, D. subspicatus cells showed reduced respiration and photosynthesis rates (Figure 1A,B) and increased H2O2 and MDA concentrations (Figure 2B,C). As stated for L. minor [20], in D. subspicatus cells, Cipro may disrupt respiratory metabolism, inducing the overproduction of ROS, which, in turn, affects photosynthesis in chloroplasts, whose photosystem II is very sensitive to ROS accumulation [64]. The activity of antioxidant systems is central to the tolerance of photosynthetic organisms to antimicrobials [21]. Although CAT activity increased in microalgae exposed to Cipro (Figure 2A), it appears to be insufficient to avoid ROS accumulation and related oxidative damages. Summarily, by disrupting primary metabolism and inducing oxidative stresses, Cipro negatively affects D. subspicatus cell growth, and this species is sensitive enough to test the ecotoxicity of waters containing environmentally representative concentrations of Cipro.
Both S. molesta and E. densa have already been confirmed to have the ability to phytoremediate Cipro [12]. Their phytoremediation capacity differs between the two species (Table 1) and the macrophytes employ distinct methods for Cipro removal: while S. molesta bioaccumulate the antimicrobial in their tissues (phytoaccumulation), E. densa appears to metabolize Cipro (phytodegradation/phytotransformation) [12]. In this study, both plants showed a high removal efficiency of above 80% within 96 h, which is considered a relatively short time when compared to other phytoremediation systems (Table 3). Generally, it takes seven or more days for plants to achieve the observed removal efficiency in the plants tested. However, certain compounds produced and released by S. molesta and E. densa are toxic to phytoplankton [43,44], and may thus constrain the use of these plants for phytoremediation purposes. Particularly, it is interesting to investigate the ecotoxicity of water after the treatment with E. densa since, in addition to allelochemicals, this plant may release Cipro metabolites in water, which can be more toxic than the parent molecule. Despite that, very few studies evaluate the toxicity of emerging contaminants after phytoremediation (Table 3), which underscores the importance of this study.
Compared to their respective control (without plant treatment), water treated with macrophytes either induced no negative effects or reduced the negative effects of Cipro on D. subspicatus cells. Microalgae in the treated water were exposed to lower concentrations of Cipro (Table 1). After 96 h of treatment with S. molesta, the concentrations of Cipro in water containing 1, 10, and 100 µg Cipro L−1 were reduced to 0, 0.56, and 2.47 µg CiproL−1, respectively, while they were reduced to 0.17, 2.44 and 12.08 µg L−1 with the treatment using E. densa (Table 2). These findings suggest that concentrations under 2.44 µg Cipro L−1 may not induce toxicity to D. subspicatus cells. Furthermore, due to its greater phytoremediation capacity, S. molesta exhibited better Cipro reduction in water, thus preventing the antimicrobial toxicity to microalgae, even when Cipro was present at a high concentration of 10 µg L−1. The superior performance of S. molesta in removing Cipro from the water was reflected in the lower IR observed in cells of D. subscatus exposed to Cipro-contaminated water treated with S. molesta compared to those treated with E. densa. As no significant differences were observed in the physiological measures evaluated in the control group of water without treatment and those treated with macrophytes, S. molesta and E. densa do not release compounds toxic to D. subscatus in the water. Finally, if some metabolite from Cipro is being released by plants, especially by E. densa, they are in a concentration not toxic to microalgae.
The use of macrophytes in phytoremediation is a NbS to remove Cipro from water, in contrast to more traditional methods that rely on chemicals or energy-intensive technologies. By removing antibiotics and other pharmaceuticals from contaminated water sources, phytoremediation can help to reduce the selective pressure for antibiotic resistance in the environment. This can help to slow the spread of antibiotic-resistant bacteria, which are a serious threat to human and animal health. NbS like the use of macrophytes such as S. molesta and E. densa in phytoremediation have the potential to address environmental contamination while also promoting public health by helping to prevent the development of antibiotic resistance in the environment. Additionally, maintaining plants requires little effort, and once they have been utilized for phytoremediation, they can be repurposed for various purposes such as the production of construction materials, fertilizers, bioenergy, and biogas [68]. This helps prevent the reintroduction of the captured contaminants back into the natural environment [69].

5. Conclusions

Desmodesmus subspicatus is a sustainable model for investigating Cipro toxicity because of its sensitivity to antimicrobials. When exposed to Cipro, microalgae cells experienced reduced growth, which may be attributed to the harmful effects of the antimicrobial on respiration and/or photosynthesis, leading to the overproduction of ROS that cause oxidative damage to cells, mainly at concentrations ≥10 µg L−1. These toxic effects were reduced or eliminated when contaminated waters were treated with macrophytes (S. molesta or E. densa). For almost all Cipro concentrations in water, the treatment with macrophytes reduced the drug to concentrations below the levels observed to induce toxicity (2.44 µg L−1). Additionally, both plant species did not release toxic compounds in the water during treatment. However, S. molesta showed better performance in water treatment than E. densa, with a percentage of removal ranging from 76% to 97%, whereas for E. densa, it ranged from 57% to 81%. Due to their phytoremediation capacity, S. molesta and E. densa should be considered for Cipro removal from water, reducing antimicrobial toxicity and preventing the development of antibiotic resistance in the environment, showing high efficiency after 96 h of treatment.

Author Contributions

R.S.A.K.: Conceptualization, methodology, validation, formal analysis, investigation, writing—original draft preparation, review and editing; T.F., R.Z.M. and J.C.M.B.: Methodology, Writing; P.J.: Conceptualization, writing—review editing, funding acquisition; M.P.G.: Conceptualization, methodology, investigation, writing—original draft preparation, review and editing, resources, supervision, funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This research was partially funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001 and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil)—Finance Code 406190/2018-6. Marcelo Pedrosa Gomes received a research productivity grant from CNPq.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Water 15 02143 g001 550
Figure 1. The effects of Cipro on primary metabolism and growth in Desmodesmus subspicatus cells exposed to water contaminated with Cipro at increasing concentrations (Control, 1, 10, and 100 µg L−1), with or without prior treatment using Egeria densa or Salvinia molesta plants. (A) Respiration; (B) Net photosynthesis rate; (C) Daily growth rate; and (D) Inhibition rate. The values are represented as the mean ± standard error of four replicates. Lowercase letters indicate significant differences in Cipro concentrations within the same treatment system, while uppercase letters indicate significant differences between treatment systems within the same Cipro concentration, as determined by the post-hoc Tukey test (considering p ≤ 0.05).
Figure 1. The effects of Cipro on primary metabolism and growth in Desmodesmus subspicatus cells exposed to water contaminated with Cipro at increasing concentrations (Control, 1, 10, and 100 µg L−1), with or without prior treatment using Egeria densa or Salvinia molesta plants. (A) Respiration; (B) Net photosynthesis rate; (C) Daily growth rate; and (D) Inhibition rate. The values are represented as the mean ± standard error of four replicates. Lowercase letters indicate significant differences in Cipro concentrations within the same treatment system, while uppercase letters indicate significant differences between treatment systems within the same Cipro concentration, as determined by the post-hoc Tukey test (considering p ≤ 0.05).
Water 15 02143 g001
Water 15 02143 g002 550
Figure 2. Effects of Cipro on oxidative stress markers in Desmodesmus subspicatus cells exposed to water contaminated with Cipro at increasing concentrations (Control, 1, 10, and 100 µg L−1), with or without prior treatment using Egeria densa or Salvinia molesta plants. (A) Catalase activity; (B) Hydrogen peroxide concentration; and (C) Malondialdehyde concentration (lipid peroxidation). The values are represented as the mean ± standard error of four replicates. Lowercase letters indicate significant differences in Cipro concentrations within the same treatment system, while uppercase letters indicate significant differences between treatment systems within the same Cipro concentration, as determined by the post-hoc Tukey test (considering p ≤ 0.05).
Figure 2. Effects of Cipro on oxidative stress markers in Desmodesmus subspicatus cells exposed to water contaminated with Cipro at increasing concentrations (Control, 1, 10, and 100 µg L−1), with or without prior treatment using Egeria densa or Salvinia molesta plants. (A) Catalase activity; (B) Hydrogen peroxide concentration; and (C) Malondialdehyde concentration (lipid peroxidation). The values are represented as the mean ± standard error of four replicates. Lowercase letters indicate significant differences in Cipro concentrations within the same treatment system, while uppercase letters indicate significant differences between treatment systems within the same Cipro concentration, as determined by the post-hoc Tukey test (considering p ≤ 0.05).
Water 15 02143 g002
Table
Table 1. Ciprofloxacin concentration and natural degradation in water and phytoremediation efficiency of Salvinia molesta and Egeria densa (means values ± standard error of four replicates).
Table 1. Ciprofloxacin concentration and natural degradation in water and phytoremediation efficiency of Salvinia molesta and Egeria densa (means values ± standard error of four replicates).
SystemTreatments
(µg L−1)		Cipro Concentration in Water (µg L−1)Degradation
(%)		Phytoremediation Efficiency (%)
Initial (T0)96 h96 h96 h
Natural degradation
(No plants)		0n.dn.dn.d-
11.03 ± 0.05 Aa0.98 ± 0.04 Aa2.40 ± 1.29 a-
1010.43 ± 0.28 Ab8.80 ± 0.13 Ab*15.44 ± 1.07 b-
100100.63 ± 9.58 Ac74.01 ± 5.81 Ac*21.70 ± 5.48 a
Water treatment
(Salvinia molesta)		0n.dn.d-n.d
11.01 ± 0.04 Aan.d Ba*-97.60 ± 1.29 Aa
1011.76 ± 0.66 Ab0.56 ± 0.03 Bb*-79.67 ± 0.71 Ab
100100.63 ± 9.58 Ac2.47 ± 0.17 Bb* 76.61 ± 3.21 Ab
Water treatment
(Egeria densa)		0n.dn.d-n.d
11.01 ± 0.51 Aa0.17 ± 0.03 C*-81.40 ± 2.71 Ba
1010.81 ± 0.05 Ab2.44 ± 0.26 Bb*-57.96 ± 2.75 Bb
100106.00 ± 3.91 Ac12.08 ± 1.33 Cb* 66.60 ± 3.01 Bb
Notes: Capital letters indicate significant differences between systems within the same Cipro concentration (p < 0.05); lowercase letters indicate significant differences between Cipro concentrations within the same system (p < 0.05); * indicate differences between the time of analysis. Significant differences were calculated by two-way ANOVA followed by the Tukey test. n.d = not detected.
Table
Table 2. F values and results of the two-way ANOVA for the effects of Cipro at various concentrations (Control, 1, 10, 100 µg Cipro L−1) and water treatment systems (No plants, Salvinia molesta, and Egeria densa) on the physiology of Desmodesmus subspicatus cells. The values represent the means of four replicates.
Table 2. F values and results of the two-way ANOVA for the effects of Cipro at various concentrations (Control, 1, 10, 100 µg Cipro L−1) and water treatment systems (No plants, Salvinia molesta, and Egeria densa) on the physiology of Desmodesmus subspicatus cells. The values represent the means of four replicates.
F ValuesD.FPnRespirationDGRIRCATH2O2MDA
Cipro concentration683.12 ***47.00 ***433.15 ***1638.0 ***12.31 ***66.49 ***4.43 *
Systems2146.30 ***66.15 ***812.70 ***4828.0 ***0.1275.46 ***40.27 ***
Cipro × Systems314.26 ***7.03 **96.69 ***562.9 ***0.9214.78 ***7.27 ***
Comparison of means
Systems
Tukey Test, p < 0.05
No plants 3.01 ± 0.93 a2.16 ± 0.51 a−34,750 ± 23,100 a53.56 ± 18.39 a21.73 ± 3.28 a6.34 ± 1.52 a2.32 ± 0.23 a
E. densa 4.94 ± 0.38 b2.91 ± 0.21 b16,118 ± 11,095 b12.78 ± 8.90 b21.98 ± 3.54 a3.90 ± 0.90 b2.04 ± 0.04 b
S. molesta 5.30 ± 0.39 c3.36 ± 0.11 c24,048 ± 11,333 c1.34 ± 0.62 c21.43 ± 3.17 a3.23 ± 0.51 c2.03 ± 0.03 b
Cipro (µg L−1)
Tukey Test, p < 0.05
Control5.62 ± 0.07 a3.55 ± 0.07 a32,435 ± 1925 a0 ± 0 a19.73 ± 0.19 a2.57 ± 0.16 a2.07 ± 0.01 a
14.91 ± 0.80 b2.90 ± 0.34 b5769 ± 2609 b21.08 ± 20.88 b19.82 ± 0.73 ab3.48 ± 0.91 b2.10 ± 0.04 ab
103.99 ± 1.01 c2.66 ± 0.49 c2769 ± 2111 c24.21 ± 22.06 c21.02 ± 1.20 ab5.49 ± 1.80 c2.16 ± 0.14 b
1003.15 ± 0.97 d2.12 ± 0.52 d−33,093 ± 19,752 d45.04 ± 20.78 d26.30 ± 0.50 b6.41 ± 1.23 d2.20 ± 0.16 b
Notes: D.F, degrees of freedom; Respiration (µmol CO2 m2·s−1); Pn, net photosynthesis rate (µmol CO2 m2·s−1); DGR, Daily growth rate (cell day−1); IR, inhibition rate (%); CAT, catalase (nmol H2O2 min mg protein−1); H2O2, hydrogen peroxide (mg protein−1); MDA, lipid peroxidation (nmol min−1 mg protein−1); * Significant p < 0.05; ** significant p < 0.01; *** significant p < 0.001. Treatment means from two-way ANOVA. Lowercase letters indicate significant differences between Cipro concentrations within the same treatment system based on a post-hoc Tukey test (considering p ≤ 0.05).
Table
Table 3. Plants used for phytoremediation of ciprofloxacin, removal efficiency (%), treatment time, ecotoxicity of post-treatment evaluation, and references.
Table 3. Plants used for phytoremediation of ciprofloxacin, removal efficiency (%), treatment time, ecotoxicity of post-treatment evaluation, and references.
PlantsPhytoremediation
Efficiency		Treatment TimeEcotoxicity EvaluationReferences
S. molesta76 to 97%96 hPrevents deleterious effects on microalgae Desmodesmus subspicatusPresent work
E. densa57 to 81%
S. molesta79 to 97%96 hPrevents deleterious effects to catfish Rhamdia quelen and human health[10]
S. molesta63 to 76%96 hNo[12]
S. molesta69 to 93%7 daysNo[12]
E. densa58 to 75%96 hNo[12]
E. densa68 to 90%7 daysNo[12]
Eichhornia crassipesUp to 84%7 DaysNo[37]
Chrysopogon zizanioides94%60 daysNo[65]
Chrysopogon zizanioides97%30 daysNo[66]
Typha latifolia34%7 daysNo[67]
Panicum virgatum10%7 daysNo[67]
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MDPI and ACS Style

Kitamura, R.S.A.; Fusaro, T.; Marques, R.Z.; Brito, J.C.M.; Juneau, P.; Gomes, M.P. The Use of Aquatic Macrophytes as a Nature-Based Solution to Prevent Ciprofloxacin Deleterious Effects on Microalgae. Water 2023, 15, 2143. https://doi.org/10.3390/w15122143

AMA Style

Kitamura RSA, Fusaro T, Marques RZ, Brito JCM, Juneau P, Gomes MP. The Use of Aquatic Macrophytes as a Nature-Based Solution to Prevent Ciprofloxacin Deleterious Effects on Microalgae. Water. 2023; 15(12):2143. https://doi.org/10.3390/w15122143

Chicago/Turabian Style

Kitamura, Rafael Shinji Akiyama, Tayna Fusaro, Raizza Zorman Marques, Julio Cesar Moreira Brito, Philippe Juneau, and Marcelo Pedrosa Gomes. 2023. "The Use of Aquatic Macrophytes as a Nature-Based Solution to Prevent Ciprofloxacin Deleterious Effects on Microalgae" Water 15, no. 12: 2143. https://doi.org/10.3390/w15122143

APA Style

Kitamura, R. S. A., Fusaro, T., Marques, R. Z., Brito, J. C. M., Juneau, P., & Gomes, M. P. (2023). The Use of Aquatic Macrophytes as a Nature-Based Solution to Prevent Ciprofloxacin Deleterious Effects on Microalgae. Water, 15(12), 2143. https://doi.org/10.3390/w15122143

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