Phytoremediation of pharmaceutical-contaminated wastewater: Insights into rhizobacterial dynamics related to pollutant degradation mechanisms during plant life cycle
Graphical abstract
Introduction
Pharmaceuticals, which are the typical emerging pollutants widely detected in water and soil environments, are mainly emitted to the environment through municipal wastewater (Aus der Beek et al., 2016). For example, ibuprofen (IBP) that is found at the maximum concentrations of 373.1 μg L−1 and 95.0 μg L−1 in the influent and effluent waters of wastewater treatment plants (WWTPs), respectively, is one of the most frequently detected pharmaceuticals in the environment (Aus der Beek et al., 2016; Gao et al., 2016). Due to the environmental risks of pharmaceuticals, it is of a great concern to remove pharmaceuticals from wastewater (Aus der Beek et al., 2016; Li et al., 2019).
Phytoremediation technologies (e.g. constructed wetlands) are regarded as one of the alternative secondary wastewater treatment or the wastewater polishing treatment processes for pharmaceutical removal from wastewater, especially showing a promising application in the decentralized wastewater treatment systems (Li et al., 2014b; Madikizela et al., 2018). To further enhance the removal efficiency of pharmaceuticals during phytoremediation of wastewater, it requires an in-depth understanding on the degradation mechanisms of pharmaceuticals. However, available research works mainly focus on the uptake of pharmaceuticals from wastewater by plant roots (Madikizela et al., 2018) and the translocation, accumulation and metabolism processes of pharmaceuticals in plant tissues (Klampfl, 2019). To date, there are few reports on the dynamics of rhizosphere microbiome related to pharmaceutical removal mechanisms during the phytoremediation of pharmaceutical-contained wastewater (Li et al., 2016b; Nguyen et al., 2019).
Rhizosphere, the thin zone surrounding plant roots, is a hotspot for numerous organisms (microorganisms and invertebrates) and is recognized as one of the most complex ecosystems on Earth (Mendes et al., 2013; Philippot et al., 2013; Sasse et al., 2018). Within the rhizosphere, there exist intricate and dynamic interactions between plant roots and microorganisms (such as bacteria, archaea, fungi, oomycetes and viruses) (Mendes et al., 2013; Philippot et al., 2013). The rhizosphere bacteria that play a positive role in acquisition for nutrients, defense against pests and disease, and tolerance to abiotic stress are referred to as the plant-growth-promoting rhizobacteria (PGPR) (Huang et al., 2014; Vacheron et al., 2013). It has been noted that the PGPR are pivotal for plant growth, health, productivity and functioning (Huang et al., 2014; Vacheron et al., 2013).
Generally, plants could induce a rhizosphere effect, so that rhizosphere microbiome is distinctly different from that of the bulk environment (Sasse et al., 2018). In detail, distinct rhizosphere microbiome is associated with plant species and genotype, plant developmental stage, root morphology, root exudation, soil properties, abiotic and biotic stress, and several other factors (Philippot et al., 2013; Sasse et al., 2018; Zhalnina et al., 2018). In the case of a specific plant in a given environment, the plant’s rhizosphere microbiome is not a static but rather a dynamic system with variations during plant growth, i.e., exerting a selection on rhizosphere beneficial microorganisms (e.g. PGPR) at different developmental stages (Philippot et al., 2013; Sasse et al., 2018; York et al., 2016).
The succession of rhizosphere microbiome during plant life cycle has been well illustrated for some plants such as oat (Shi et al., 2015), arabidopsis (Chaparro et al., 2014), and maize (Li et al., 2014a). Furthermore, a growing number of studies have reported the shifts in community composition and functional activities of rhizosphere microbiome under abiotic stresses such as salinity, heavy metal and organic pollutants (Feng et al., 2019; Mark Ibekwe et al., 2017; Rajkumar et al., 2012). Nevertheless, in the research field of phytoremediation, for the case of pharmaceuticals in wastewater which is a kind of abiotic stress to plants (Aus der Beek et al., 2016; Bartrons and Penuelas, 2017), there are knowledge gaps on the dynamic variations of rhizosphere microbiome over the course of plant life cycle.
In this study, ibuprofen (IBP) was selected as the target pharmaceutical, which belongs to the key pharmceuticals with high environmental risks in the aquatic environment (Li et al., 2019; Wang et al., 2016). The study focused on the removal of IBP from wastewater in microcosm-scale constructed wetlands using Typha angustifolia in order to reveal the potential biodegradation mechanisms of IBP associated with rhizosphere microbiome (e.g. the PCPR). The diversity, community and function variations of rhizobacteria during the developmental course of Typha angustifolia were investigated. In addition, the correlations between the environmental factors (physicochemical properties of interstitial water), OTU (operational taxonomic unit) abundances, and rhizosphere samples (bacterial communities) were evaluated.
Section snippets
Chemicals
Ibuprofen (≥98%, IBP) that was injected into the feed water (synthetic municipal wastewater) and its isotopic compound ibuprofen-d3 (≥98%, IBP-d3) that was used for the internal standard calibration of liquid chromatography-tandem mass spectrometry were purchased from Sigma-Aldrich (USA). The synthetic municipal wastewater was prepared with glucose (anhydrous), potassium dihydrogen phosphate (≥98%), ammonium sulfate (≥99%), magnesium sulfate heptahydrate (≥99%), calcium chloride dehydrate
Wetland performance
The physicochemical characteristics of feed water and interstitial water of the IBP-stressed and control wetlands are presented in Table 1. During the five developmental stages of Typha angutsitfolia, it was observed that the temperature, DO, pH and conductivity of interstitial water were not significantly different between the two types of wetlands and were in the range of 29–31 °C, 1–2 mg L−1, 6–7 and 470–670 μS cm−1, respectively.
In both wetlands, the removal efficiencies of COD and NH4+-N
Conclusions
This study investigated the dynamics of rhizosphere bacteria in microcosm-scale constructed wetlands during the development of Typha angustifolia (i.e. from seedling, vegetative, bolting, mature, to senescent stages) for the treatment of pharmaceutical (IBP) contaminated wastewater.
By comparing with the control wetlands (free of IBP), it was found that plant growth promoted pollutant removal in wetlands with the best performance at the bolting or mature stage, and the presence of IBP in feed
CRediT authorship contribution statement
Yifei Li: Conceptualization, Investigation, Formal analysis, Writing - original draft. Jie Lian: Formal analysis. Bing Wu: Writing - review & editing. Hua Zou: Resources, Writing - review & editing. Soon Keat Tan: Resources, Writing - review & editing.
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.
Acknowledgements
This study was financially funded by Natural Science Foundation of Jiangsu Province, China (No. BK20180632) and Innovative and Entrepreneurial Foundation of Jiangsu Province, China (No. 1126010241180210) (supported by the Government of Jiangsu Province). The authors gratefully acknowledge the assistance and support from Nanyang Technological University, Singapore.
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