The effect of carbon-based copper nanocomposites on Microcystis aeruginosa and the movability of antibiotic resistance genes in urban water
Graphical abstract
Introduction
The bloom of Microcystis aeruginosa (M. aeruginosa), the dominant species in harmful algal blooms (HABs), and the spread of antibiotic resistance genes (ARGs) in various freshwater ecosystems have caused widespread public concern (Jiang et al., 2021; Zhao et al., 2021a). HABs can contribute to ARG spread in aquatic environments (Wang et al., 2020b). ARGs are widely spread in edaphic and aquatic ecosystems; mainly, the aquatic environment is one of the ideal media for organisms to acquire and spread ARGs (Li et al., 2020). Humans and animals discharge ARGs into the environment via intestinal bacteria. The spread of ARGs mediated by horizontal gene transfer (HGT) in the environmental medium is aggravated (Lu et al., 2020). The ARGs, frequently located on mobile genetic elements (MGEs), are a kind of genetic material that can be transferred same species or be transferred from one species to another (Frost et al., 2005). Plasmids, transposons, integrons, and integrative and conjugative elements (ICEs), which are mobile genetic elements, comprise all MGEs with self-replication, integration, and conjugation abilities (Burrus and Waldor, 2004). These MGEs are closely related to the HGT of ARGs (Wozniak &Waldor, 2010). The aquatic environment is rich in microorganism diversity; therefore, aquatic ecosystems are often considered an essential ARG reservoir (Chen et al., 2019b).
Our previous study found that the abundance of ARGs in wastewater was closely related to the quantity of M. aeruginosa. Simultaneously, carbon-based copper nanocomposites (CCN) had the broad-spectrum killing ability of harmful microorganisms in aquatic environments (Kang et al., 2009). Thus, to further control the harmful cyanobacteria and spread of ARGs in the environment, the effects of CCN on M. aeruginosa and ARGs associated with MGEs should be investigated and explained. Moreover, the HGT of ARGs will lead to increased hosts and promote the dissemination of ARGs (Ma et al., 2017). Therefore, it is important to estimate the hosts of ARGs when the CCN is presented.
The traditional method for cyanobacteria removal is spraying copper sulfate (CuSO4) (Jiang et al., 2020). However, the CCN is an ideal nanomaterial that can effectively control the growth of harmful microorganisms, and its effects on M. aeruginosa control are better than those of CuSO4. Furthermore, the removal efficiency of M. aeruginosa is about six times that of physical removal methods (Cruces et al., 2021). Traditionally, methods to evaluate the mobility and HGT of ARGs in natural water were DNA sequencing and comparison (Nielsen et al., 1998). However, microbial genome sequencing and genomics rely on traditional clonal cultures; early gene sequencing of environmental sample cloned specific genes to produce a profile of diversity in a biological sample. These work demonstrated that the vast majority of microbial biodiversity had been missed by traditional cultivation methods (Hugenholtz et al., 1998). Therefore, the traditional techniques still cannot meet complex environmental samples’ analysis needs, especially when some exogenous substances are present (Chen et al., 2019b). With the rapid development of metagenomic sequencing, because of its strong ability to decipher the hidden ARGs of environmental samples, metagenomics provides an efficient approach for learning the ARGs that can revolutionize understanding of almost the entire ARG characters (Marco, 2011). Many previous studies on metagenomics focused on the abundance of ARGs (Yang et al., 2019), disregarding the relationship between ARGs and MGEs.
Moreover, most previous studies focused on the M. aeruginosa removal by nanomaterials, such as carbon nanotubes and graphene oxide (Wu et al., 2020; Yousefi et al., 2020), with little emphasis on the effects of nanomaterials on ARGs and their HGT. Little is known about the effect of CCN on the removal of M. aeruginosa, relations between ARGs and MGEs, and changes in the hosts of ARGs in urban water. Currently, the proliferation of M. aeruginosa and contamination of ARGs are the two major challenges in the removal of pollutants from urban water (Everett et al., 2017; Ye et al., 2018). Whether the CCN, which can remove harmful cyanobacteria and spectroscopically kill harmful microorganisms, affects the co-removal of M. aeruginosa and ARGs in natural water is still unclear.
In this study, the urban water of Jinhui Harbor in Haiwan Town, Fengxian District, Shanghai, was used to set different concentrations of CCN treatment systems at different concentrations of 0, 10, 20, 40, and 60 mg/L according to a previous study (Zhao et al., 2021b). Metagenomic sequencing was employed to investigate the ARGs and their mobility in a photobioreactor. The microbial diversity, live/dead algal cell ratio and zeta potential, coverage of ARG-carrying contigs (ACCs), distribution of ARGs in plasmids and chromosomes, co-occurrence of ARGs with MGEs, environmental factors affecting ACCs, and effect of CCN on the potential host variation of ARGs were detected and analyzed to explain the characters of CCN affecting M. aeruginosa and ARGs in urban aquatic environments.
Section snippets
Sample collection and experiment design
A total of six representative samples were collected, and the sampling sites were all located at the confluence of two streams. The detailed characteristics of the sampling sites are presented in Table S1. The samples were collected from the Jinhui Harbor of the river network in Haiwan Town, Fengxian District, Shanghai (Fig. 1). Sampling points are mostly located at the intersection of the main river and its tributaries. These intersections include urban landscapes, factories, houses, farms,
Impacts of CCN on microbial communities
Microbial diversity is one of the primary indicators to investigate the effect of the exogenous addition of CCN on microorganisms in aquatic environments (Zinger et al., 2012). In this study, the microbial diversity of each sample was tested and analyzed at the domain, phylum, and species levels via 16S high-throughput sequencing (Cao et al., 2018). A total of 311585 sequences were sequenced, and all sequences were divided into OTUs according to different similarity levels, and bioinformatic
Conclusions
The appropriate concentration of CCN could effectively promote flocculation of Microcystis aeruginosa in urban water and the CCN can also inhibit the HGT of ARGs. The HGT potential of ARGs mediated by plasmids and MGEs was higher in the urban water without CCN. The 20 mg/L of CCN significantly decreased the ARGs proportions which mediated by plasmids. This concentration of CCN weakened the movability potential of ARGs mediated by MGEs such as plasmids, 41 bacterial categories were identified as
Ethical approval
This research does not involve ethical issues.
Consent to participate
This research does not involve ethical issues.
Consent to publish
All authors confirm that this paper has not been published before in any form.
Authors contributions
Xiyan Ji: Conceptualization, Methodology, Supervision, Funding acquisition. Yunchao Tang: Validation, Formal analysis, Investigation, Data Curation, Writing - Original Draft. Jing Ye: Review & Editing. Shichao Wu: Data Curation, Formal analysis. Meifang Hou: Supervision, Conceptualization, Review & Editing. Saihua Huang: Conceptualization, Review & Editing. Rui Wang: Visualization and Analysis.
Availability of data and materials
The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.
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.
Acknowledgments
This work were financially sponsored by Shanghai Sailing Program (20YF1447700), National Natural Science Foundation of China (32001201), Collaborative Innovation Fund of Shanghai Institute of Tehnology, The Natural Science Foundation of Guangdong Province (No. 2021A1515012221), Qingyuan Science and Technology Plan Project (2020KJJH012). We sincerely thanked River Chief Office of Fengxian District Bay Tourism Area, Shanghai, China for the help of water sample collection map.
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2022, Science of the Total EnvironmentCitation Excerpt :Pseudonocardia and Cephaloticoccus were found to be hosts for ARGs (Shen et al., 2020), both of them were observed in sludge samples with μm-MPs in present study. And on MPs surface, ARGs were found to be correlated with genus Niveispirillum and Prosthecobacter, which were also found to be hosts for ARGs in aquatic environments (Ji et al., 2022). The particle size of MPs affected the taxa linkages between ARGs and microbes in wastewater treatment systems, and mm-MPs resulted in higher taxa linkages than μm-MPs.