Metagenomic insight into the distribution of metal resistance genes within cascade reservoir waters: Synergic impacts of geographic variation and anthropogenic pollution

https://doi.org/10.1016/j.envres.2022.114682Get rights and content

Highlights

  • Metal pollution level is a prerequisite regulating MRGs abundance in reservoir water.

  • Geographic variation had stronger impact on MRGs composition than metal pollution.

  • Reservoir operation time, storage size and regulation mode affected MRGs abundance.

  • Reservoir MRGs distribution was internally affected by relevant microbial community.

Abstract

Metal resistance genes (MRGs) are potential bio-indicators to diagnose contamination stress on riverine ecosystems. Within reservoir systems, river damming weakens hydrodynamic condition and enriches metal contaminants. But, little is known about the synergic impacts of geographic variation and anthropogenic pollution on MRGs. In this study, the abundance, composition and microbes of MRGs in four cascade reservoirs along the Jinsha River, southwestern China were investigated via high-throughput metagenomics. The results showed significant enrichment of chromium, cadmium and lead in Ludila and Xiluodu reservoirs with moderate ecological risks based on the criteria of drinking water quality and aquatic life protection. Nevertheless, at watershed scale, these metals played little role in up-regulating MRGs abundance owing to the limited toxic stress on microbes. Accordingly, geographic variation showed stronger impacts on MRGs composition than metals as revealed by the distance-decay relationship (Pearson correlation, rgeo = 0.24–0.57, rmetal = 0.10–0.41) and co-occurrence network (Node degree to MRGs subtype, ngeo = 180, nmetal = 6). River damming, as an artificial isolation of geographic space, significantly affected MRGs composition. The longer operation history, smaller storage capacity and higher regulation frequency caused the higher dissimilarity of MRGs composition between the reservoir's upstream and downstream areas. In conclusion, the metal pollution level is a prerequisite regulating MRGs; while under the lowly-polluted conditions, geographic variation had stronger impacts on MRGs than metal pollution via altered assembly of microbial communities. This study provides an important guidance for the future environmental management and ecological protection of river-reservoir ecosystems.

Introduction

Because of rapid development of industrialization and urbanization, metal contamination has been aggravated in numerous rivers via excessive discharge of industrial wastewater and domestic sewage from medicine, agriculture, aquaculture, mining and refining (Yuan et al., 2019). Microbes, ubiquitous in riverine ecosystems, have been widely applied as biological indicators to diagnose metal pollution owing to its high environmental sensitivity, convenient field sampling and low economic cost (Tang et al., 2019; Yuan et al., 2022). Recent advances in high-throughput metagenomics enable in-depth coverage of microbial gene pools containing various metal resistance genes (MRGs), to reveal microbial resistance mechanism and survival strategy under metal-polluted conditions in a culture-independent manner (Reddy and Dubey, 2019; Yang et al., 2019). As a result, the determination of MRGs have notable potentials in future environmental monitoring and assessment, from which government policymakers and environmental managers would obtain a clear understanding on how riverine microbial ecosystems are affected by metal pollutants (Chen et al., 2015).

The MRGs are ancient and ubiquitous in natural environments (Jenkins and Stekel, 2010; D'Costa et al., 2011). Since 2.4 billion years ago, the Great Oxidation Event made metals bioavailable, which exerts a notable selective pressure on microorganisms and generates diverse profiles of MRGs (Fru et al., 2016). The MRGs could protect microbial cells from metal toxicity through various resistance mechanisms, including intra-/extra-cellular sequestration, active transport efflux pump, permeability barrier exclusion and so on (Bruins et al., 2000; Argudin et al., 2019). For example, the copper (Cu) and arsenic (As) contamination from acid mine drainage caused elevated abundances of corresponding MRGs, such as ars genes encoding arsenate reduction and arsenite methylation (arsB, arsC, arsM and arsR genes) and cop genes encoding ATP-dependent Cu transporter (copA, copB, copR and copS genes) in riverine sediments (Zhang et al., 2019). These MRGs can not only diagnose metal contamination status, but also reveal biological processes in response to corresponding pollutant, which is relatively difficult for microbial community related bio-indicators reflecting only characterization of composition shifts (Pal et al., 2014, 2015). Recently, accumulating evidences have demonstrated that metal pollution could up-regulate MRGs abundance in riverine water and sediment media through the activation of intrinsic MRGs and/or acquisition of exogenous MRGs (Xie et al., 2019; Zhang et al., 2019). Accordingly, the MRGs have been employed to diagnose metal pollution stress on riverine ecosystem under anthropogenic disturbances (Li et al., 2021).

Dam, as a typical hydraulic structure, is widely applied for hydropower generation in numerous large rivers (Timpe and Kaplan, 2017). After the dam construction, the water impoundment in front of dam could form a large reservoir, which modifies natural flow regime of water, sediment, nutrient and biota transport (Yuan et al., 2019; Chen et al., 2020). Moreover, the long hydraulic retention time resulted by river damming could accelerate the accumulation of various metal pollutants in reservoirs (Wang et al., 2018a). For example, in the Three Gorges Reservoir in China, high concentrations of lead (Pb) and As were enriched in water column due to the contamination input from surrounding industrial discharge and gasoline combustion (Gao et al., 2016). These metal pollutants could cause significant impacts on reservoir microbial diversity, community composition and nutrient cycling function (Liu et al., 2018; Yang et al., 2022; Yuan et al., 2022). Further investigation on MRGs, therefore, is essential to indicate microbial resistance mechanisms and diagnose metal pollution impacts.

However, according to existing researches, numerous reservoirs exhibit low enrichment of metals after river damming, for example, the low concentrations of Cu, Zn, Pb and Cd within the Iron Gate Reservoir water in Serbia, because of limited anthropogenic contamination (Vukovic et al., 2014). In aquatic environments, these metals at low concentrations are generally regarded as micropollutants, which posed relatively weak ecological influences (Walaszek et al., 2018). Nevertheless, it is still essential to reveal the impact of reservoirs on MRGs even under lowly-polluted conditions, which is of significance as background references for future researches on MRGs when metal contamination is significantly aggravated. Generally, the river damming changes aquatic physicochemical properties and deposits large amounts of suspended particles, spontaneously altering microbial communities (Wang et al., 2018b, 2020). Thus, the MRGs relevant microbes, as a subgroup of total microbial taxa, may also be affected. Recent studies have emphasized that geographic variation could shape microbial community and subsequently affect MRGs distribution in water, sediment and biofilm media (Song et al., 2019; Yang et al., 2019). In this study, the river fragmentation caused by dam constructions could be regarded as the artificial isolation of geographic space (Nilsson et al., 2005). The geographical location, operation history and storage capacity are the main factors determining the impact extents of dam reservoirs on riverine ecosystems (Poff and Hart, 2002). But, it is unknown whether these factors affect MRGs distribution within reservoirs.

The Jinsha River basin in China, due to its notable hydropower resource, has planned a cascade of 24 dam reservoirs along the mainstream (Wang et al., 2015). Of these cascade dams, eight have been constructed, significantly affecting riverine hydrology, aquatic environments and microbial ecosystems (Chen et al., 2020). In this study, four representative reservoirs, including the Ahai (AH), Ludila (LDL), Guanyinyan (GYY) and Xiluodu (XLD) ones, have been selected to investigate the synergic impacts of geographic variation and anthropogenic pollution on the abundance, composition and microbes of MRGs. According to previous studies (Zhang et al., 2019; Wang et al., 2020), we hypothesized that (i) the enriched metal pollution in reservoirs will up-regulate MRGs abundance; (ii) the metals will present stronger impacts on MRGs composition than geographic variation; and (iii) the changes of MRGs relevant microbial community will internally affect MRGs distribution.

Section snippets

Study area and field sampling

The Jinsha River located in southwestern China is an important water source for the Yangtze River. Since 2010, a cascade of dams have been constructed and successively put into operation (Wang et al., 2015). To investigate their influences on MRGs, the AH, LDL, GYY and XLD reservoirs were selected. Detailed information about the operation history, storage capacity and regulation frequency was shown in Supplementary Material Table S1. The field sampling was conducted during December in 2017

Metal concentration and water quality assessment

The concentration ranges of six metals in the Jinsha River water were as follows: 2.46–3.27 μg L−1 for As, 9.20–15.23 μg L−1 for Cu, 0.66–3.49 μg L−1 for Ni, 3.83–22.51 μg L−1 for Cr, 0.05–1.24 μg L−1 for Cd and 5.98–34.95 μg L−1 for Pb (Fig. S1). Results of one-way ANOVA showed notably higher concentrations of Cd, Cr, Ni and Pb in the LDL.U, Cd and Pb in the GYY.U, as well as As, Cd and Cr in the XLD.U than those in the downstream areas of corresponding reservoirs (p < 0.05). However, for the

Reservoir metal pollution played little role in up-regulating MRGs abundance

River damming, as a physical barrier in numerous large rivers, significantly decreases water flow velocity and increases hydraulic retention time (HRT), which allows the enrichment of metal pollutants within reservoirs (Gao et al., 2016; Wang et al., 2018a). In this study, the concentrations of Cd, Cr, Ni and Pb in the LDL reservoir, Cd and Pb in the GYY reservoir, and As, Cd and Cr in the XLD reservoir were significantly higher in upstream areas than those in downstream areas. These metal

Conclusion

In this study, the metals Pb, Cd and Cr in the upstream areas of LDL and XLD reservoir posed potential ecological impacts. Nevertheless, the pollution levels were generally too low to up-regulate MRGs abundance. Compared with metals, the geography played a more important role in influencing MRGs composition. Moreover, the artificial isolation of river damming exhibited certain impacts on MRGs composition. Among four individual reservoirs, the MRGs composition similarity between reservoir

Credit author statement

P. Wang: Conceptualization, Methodology, Writing – review & editing. Q. Yuan: Methodology, Investigation, Writing – original draft & Visualization. X. Wang: Investigation, Writing – review & editing. B. Hu: Investigation. C. Wang: 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.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 92047201; No. 92047303; No. 42007149) and the World-Class Universities (Disciplines) and Characteristic Development Guidance Funds for the Central Universities.

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