Strong impact of micropollutants on prokaryotic communities at the horizontal but not vertical scales in a subtropical reservoir, China
Graphical abstract
Introduction
Rivers are an important freshwater resources on Earth that serve the society in a variety of ways (Grill et al., 2019). Hundreds of thousands of dams have been constructed worldwide because of an increasing demand of water for human activities. Besides providing benefits to the society, dams also cause numerous harm to rivers (Fang and Min, 2011), via irregular hydrological conditions (e.g., water flow rate and water residence time) (Nilsson and Berggren, 2006), lowering the water quality (e.g., eutrophication and hypoxia) (Elçi, 2008) and chemical pollution (Fang and Min, 2011). Consequently, the microorganisms inhabiting the rivers are likely to be influenced by such disturbances in the riverine environments. Previous works suggested that prokaryotic communities serve as a good bio-indicator for evaluating the health of aquatic ecosystems (Sun et al., 2012; Zeglin, 2015), provided that they readily respond to the shifting environmental conditions (Hu et al., 2017b; Isabwe et al., 2018; Shen et al., 2018; Sun et al., 2017a; Sun et al., 2017b). In the events of river disturbances, the changes in the prokaryotic communities are not only linked to the changes of water physico-chemical properties such as temperature, salinity, dissolved oxygen (DO) and nutrients etc. (Hu et al., 2017a; Isabwe et al., 2018; Sun et al., 2017a; Sun et al., 2017b) but also to various chemical pollutants (Jeanbille et al., 2016; Sabater et al., 2016; Sun et al., 2012). Several studies have assessed the effects of either physico-chemical factors (Hu et al., 2017b; Isabwe et al., 2018; Sun et al., 2017b; Sun et al., 2017a) or chemical pollutants (Blunt et al., 2018; Jeanbille et al., 2016; Sun et al., 2012) on the diversity and composition of prokaryotic communities. However, little is known about the relative impacts of both of these river disturbances on the assembly of prokaryotic communities, especially, in case of freshwater ecosystems, where the disrupting effects of micropollutants on ecological disturbances have been taken very seriously in the recent years (Richmond et al., 2017).
Micropollutants, such as pharmaceuticals, personal care products, endocrine disrupting compounds and industrial chemicals have raised public concerns due to their pseudo-persistence in environment and potential threats to ecosystem and human health (Liu and Wong, 2013; Yang et al., 2012). Although they commonly occur at low concentrations in the natural environments (Liu and Wong, 2013; Richmond et al., 2017), yet they have implications at sub-lethal concentrations. Some microorganisms are capable of utilizing certain micropollutants as carbon sources, such as triclosan, bisphenol A, ibuprofen (Zhou et al., 2013) and ciprofloxacin (Liao et al., 2016), however, the growth and metabolism of the others may be influenced by the sub-lethal effects of the micropollutants (Richmond et al., 2017). Blunt et al. (2018) reported a relatively higher degradation capabilities of microorganisms in a micropollutant contaminated part of a river than that in its adjacent pristine part (Blunt et al., 2018). Our previous work also suggested that trace micropollutants levels exert relatively greater influence on the co-occurrence of central microbial species than the physico-chemical factors (Hu et al., 2017a). Hence, exploring the relationship among physico-chemical factors, micropollutants and aquatic prokaryotic communities will provide a better understanding of the extent to which these abotic factors affect the prokaryotic community.
Aquatic prokaroytic community composition varies both at seasonal and vertical scales in freshwater ecosystems (Garcia et al., 2013; Salcher et al., 2010; Yu et al., 2015). The vertical variation pattern was put forward as variation in the diversity and composition of the prokaryotic communities due to changes in physico-chemical factors, such as light, temperature, DO, nutrients and chlorophyll-a at different water depths (Salcher et al., 2011; Yang et al., 2015; Yu et al., 2014). The vertical and seasonal variations in the physico-chemical profiles are well documented (Garcia et al., 2013; Morrison et al., 2017; Yang et al., 2015; Yu et al., 2015), however, such variations in the micropollutant distribution are scarcely reported (Aristizabal-Ciro et al., 2017; Deyerling et al., 2016). Likewise, a knowledge gap also exists on the relative importance of micropollutants on the assembly of prokaryotic communities through the water column.
Prokaryotic communities in the aquatic environments can be categorized as particle-associated (PA) and free-living (FL) on the basis of cell size and lifestyle (Riemann and Winding, 2001). Since PA taxa specialize in occupying the unique niches provided by suspended particles (Dang and Lovell, 2016), PA and FL communities usually possess distinct compositions (Yung et al., 2016; Zhao et al., 2017), physiological capabilities and metabolic activities (Grossart et al., 2007). Moreover, due to the biofilm structure, PA communities may be more resistant to environmental stressors, such as disinfectants, biocides and others, than the FL communities (Dang and Lovell, 2016). A recent study has found that antibiotics can enhance the aggregation of specific bacterial taxa with the suspended particles in the drinking water distribution systems (Wang et al., 2018a). These findings raise the possibility that the micropollutants are likely to influence the compositions of PA and FL prokaryotic communities, differently, to some extent. This phenomenon may be addressed in spatial dimensions (e.g., horizontal and vertical scales), provided that the hydrological dynamics may influence the distribution of micropollutants in water bodies. Furthermore, prokaryotic species can be further partitioned into core and satellite groups according to species' occupancy and abundance (Hanski, 1982). In order to model the random distribution (i.e., Poisson distribution) of species, the core-satellite approach uses the dispersion index (i.e., the ratio of variance to mean abundance), rather than setting an artificial cut-off for partitioning of species into ecologically meaningful groups (van der Gast et al., 2011). The core group is composed of non-randomly distributed species, which are abundant and widespread across time and space, while the satellite species are generally randomly distributed and have low abundance and narrow occupancy (Hanski, 1982; van der Gast et al., 2011). The core and satellite groups may have different responses to environmental conditions (Hou et al., 2019; Hu et al., 2017b; Jeanbille et al., 2016). Since abundant core and rare species are both important in term of ecosystem function and responding to environmental disturbances (Campbell et al., 2011; Jacquiod et al., 2018), particularly the former one (Hu et al., 2017b), an in-depth understanding of the micropollutant effects on these ecological meaningful groups is of great significance for predicting the response of prokaryotic communities to future environmental changes.
Here, 16S rRNA gene amplicon sequencing was used to characterize the structure of core/satellite sub-communities within PA and FL size-fractions, and their relationships with the micropollutants and physio-chemical parameters in a subtropical water reservoir were explored. Samples were collected horizontally (surface water) and vertically (depth-profile) from the water body. This sampling strategy allowed us to capture a relatively wide gradient of micropollutants and physico-chemical parameters in different seasons and depths under natural conditions. Specifically, following hypotheses were tested: (i) the micropollutants can significantly predict the variations in the composition of PA and FL prokaryotic communities at both horizontal and vertical scales in the reservoir; (ii) the core groups are more sensitive to physico-chemical factors and micropollutants than their satellite counterparts within PA or FL communities, as the non-randomly distributed taxa are more sensitive to the environmental drivers than the randomly distributed taxa (Barnes et al., 2016; Hou et al., 2019; Hu et al., 2017b); and (iii) prokaryotic taxa from PA and FL size-fractions are expected to have different types of associations with physico-chemical factors and micropollutants, as it is well-known that even for the same taxon, PA and FL taxa have different physiological and metabolic properties (Dang and Lovell, 2016).
Section snippets
Study area and sample collection
Minjiang River is the largest river in Fujian Province, China (Fig. 1), that serves as water resource for residential, industrial, and agricultural activities of roughly half of its inhabitants (Chen et al., 2011). Shuikou Water Reservoir (SWR) is located in the midstream of Minjiang River, resulting from Shuikou Dam that was built for hydroelectric generation. A decrease in the water quality of SWR was reported, due to floating-cage fish farming in the upstream area (Zhang et al., 2019) and
Physico-chemical properties and micropollutants of SWR
Majority of the physico-chemical variables either at surface water (horizontal scale) or across depth (vertical scale) varied significantly among seasons (Friedman's test, P < 0.05). Moreover, only 6 out of 15 physico-chemical variables showed significant variation across depth (Fig. 3A and C, Table S1). A total of 22 micropollutants were detected across all the samples (Qian Sun, unpublished data), where 17 micropollutants occurred in >30% of all the samples and were included in further
Stronger impact of micropollutants at horizontal than vertical scales on both PA and FL communities
This study represents the first ever account on the relative contribution of water quality variables (i.e., physico-chemicals) and chemical stressors (i.e., micropollutants) in shaping the prokaryotic community assemblages in horizontal (surface water) as well as vertical (depth-profile) dimensions in a freshwater environment. As hypothesized, the micropollutants were found to explain a significantly unique portion of variation in the composition of ecologically meaningful groups (i.e., core
Conclusions
Our study demonstrated that water physico-chemical factors and micropollutants had strong joint effects on both core and satellite prokaryotic assemblages from PA or FL fractions in a subtropical water reservoir, China. The micropollutants demonstrated a larger independent impact on core sub-communities than their satellite counterparts. However, the responses of the prokaryotic assemblages to the micropollutants were different from the horizontal (surface water) and vertical (depth-profile)
CRediT authorship contribution statement
Bob Adyari: Software, Formal analysis, Data curation, Writing - original draft, Visualization. Dandan Shen: Writing - review & editing. Shuang Li: Investigation. Lanping Zhang: Investigation. Azhar Rashid: Investigation, Data curation, Writing - review & editing. Qian Sun: Methodology, Data curation. Anyi Hu: Conceptualization, Methodology, Software, Validation, Writing - review & editing, Supervision, Project administration, Funding acquisition. Nengwang Chen: Investigation, Methodology,
Declaration of competing interest
The authors declare that they have no competing interests.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31870475, 31470539 and U1805244) and the Joint project of Chinese Academy of Sciences and Industrial Technology Research Institute (CAS-ITRI201802). AR was supported by PIFI CAS (2017VEB0008). BA was supported by CAS-TWAS president PhD fellowship programme. The postdoctoral fellowship of DS was funded by the Leibniz Institute for Baltic Sea Research (IOW) in Germany.
References (81)
- et al.
Monitoring and mass balance analysis of endocrine disrupting compounds and their transformation products in an anaerobic-anoxic-oxic wastewater treatment system in Xiamen, China
Chemosphere
(2018) - et al.
Pharmaceuticals in the environment: biodegradation and effects on natural microbial communities. A review
J. Pharm. Biomed. Anal.
(2015) - et al.
Association between degradation of pharmaceuticals and endocrine-disrupting compounds and microbial communities along a treated wastewater effluent gradient in Lake Mead
Sci. Total Environ.
(2018) - et al.
Phosphorus export during storm events from a human perturbed watershed, southeast China: implications for coastal ecology
Estuar. Coast. Shelf Sci.
(2015) - et al.
Prokaryotic footprints in urban water ecosystems: a case study of urban landscape ponds in a coastal city, China
Environ. Pollut.
(2018) - et al.
Community assembly processes underlying phytoplankton and bacterioplankton across a hydrologic change in a human-impacted river
Sci. Total Environ.
(2018) - et al.
Long-term industrial metal contamination unexpectedly shaped diversity and activity response of sediment microbiome
J. Hazard. Mater.
(2018) - et al.
Refinement of biodegradation tests methodologies and the proposed utility of new microbial ecology techniques
Ecotoxicol. Environ. Saf.
(2015) - et al.
Pharmaceuticals and personal care products (PPCPs): a review on environmental contamination in China
Environ. Int.
(2013) - et al.
Pharmaceuticals and personal care products in a mesoscale subtropical watershed and their application as sewage markers
J. Hazard. Mater.
(2014)
The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology
Curr. Opin. Microbiol.
Biodegradation of sulfamethoxazole and other sulfonamides by Achromobacter denitrificans PR1
J. Hazard. Mater.
Shared effects of organic microcontaminants and environmental stressors on biofilms and invertebrates in impaired rivers
Environ. Pollut.
Bacterial communities are sensitive indicators of contaminant stress
Mar. Pollut. Bull.
Regularized generalized canonical correlation analysis for multiblock or multigroup data analysis
Eur. J. Oper. Res.
Quantifying the importance of the rare biosphere for microbial community response to organic pollutants in a freshwater ecosystem
Appl. Environ. Microbiol.
Sulfadiazine/ciprofloxacin promote opportunistic pathogens occurrence in bulk water of drinking water distribution systems
Environ. Pollut.
Monitoring, mass balance and fate of pharmaceuticals and personal care products in seven wastewater treatment plants in Xiamen City, China
J. Hazard. Mater.
Removal of selected endocrine disrupting chemicals (EDCs) and pharmaceuticals and personal care products (PPCPs) during ferrate(VI) treatment of secondary wastewater effluents
Water Res.
Microbiological effects of sublethal levels of antibiotics
Nat. Rev. Microbiol.
Monitoring pharmaceuticals and personal care products in reservoir water used for drinking water supply
Environ. Sci. Pollut. Res.
Spatio-temporal variation of core and satellite arbuscular mycorrhizal fungus communities in Miscanthus giganteus
Front. Microbiol.
Activity of abundant and rare bacteria in a coastal ocean
Proc. Natl. Acad. Sci.
MixMC: a multivariate statistical framework to gain insight into microbial communities
PLoS One
Class 1 integrons, selected virulence genes, and antibiotic resistance in Escherichia coli isolates from the Minjiang River, Fujian Province, China
Appl. Environ. Microbiol.
Aerobic soil biodegradation of bisphenol (BPA) alternatives bisphenol S and bisphenol AF compared to BPA
Environ. Sci. Technol.
Factors affecting the removal of organic micropollutants from wastewater in conventional treatment plants (CTP) and membrane bioreactors (MBR)
Rev. Environ. Sci. Biotechnol.
Nitrogen enrichment suppresses other environmental drivers and homogenizes salt marsh leaf microbiome
Ecology
Microbial surface colonization and biofilm development in marine environments
Microbiol. Mol. Biol. Rev.
Depth profile of persistent and emerging organic pollutants upstream of the Three Gorges Dam gathered in 2012/2013
Environ. Sci. Pollut. Res.
Antibiotic disturbance affects aquatic microbial community composition and food web interactions but not community resilience
Mol. Ecol.
UPARSE: highly accurate OTU sequences from microbial amplicon reads
Nat. Methods
Effects of thermal stratification and mixing on reservoir water quality
Limnology
Application of MIKE 11 model in the prediction of water pollution accident in the Three Gorges Reservoir
Depth-discrete profiles of bacterial communities reveal pronounced spatio-temporal dynamics related to lake stratification
Environ. Microbiol. Rep.
Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities
ISME J.
Mapping the world’s free-flowing rivers
Nature
Comparison of cell-specific activity between free-living and attached bacteria using isolates and natural assemblages
FEMS Microbiol. Lett.
Dynamics of regional distribution: the core and satellite species hypothesis
Oikos
Deciphering the assembly processes of the key ecological assemblages of microbial communities in thirteen full-scale wastewater treatment plants
Microbes Environ.
Cited by (15)
Network analysis reveals significant joint effects of microplastics and tetracycline on the gut than the gill microbiome of marine medaka
2023, Journal of Hazardous MaterialsSeasonal hydrological dynamics govern lifestyle preference of aquatic antibiotic resistome
2023, Environmental Science and EcotechnologyCitation Excerpt :Water samples (500–1000 mL) were filtered through 3 μm and 0.22 μm filters to collect DNA of PA and FL fractions, respectively. DNA from a total of 70 samples from various depths (18 for April, August, and January and 16 for November) representing both PA and FL fractions were extracted by using a FastDNA SPIN kit for soil (Obiogene-MP Biomedicals, Irvine, CA, USA) following the manufacturer's protocol [14]. Subsequently, samples were analyzed via HT-qPCR (Wafergen SmartChip Real-time PCR system) with a total of 296 primer sets representing 285 ARGs, ten MGEs (eight transposase genes and two integrons), and a 16S rRNA gene (as internal control).
Continuous antibiotic attenuation in algal membrane photobioreactor: Performance and kinetics
2022, Journal of Hazardous MaterialsDomestic wastewater causes nitrate pollution in an agricultural watershed, China
2022, Science of the Total EnvironmentCitation Excerpt :The 16S rRNA gene amplicon sequencing data were submitted into the NCBI Short Reads Archive (SRA) database with BioProject number PRJNA686226. The 16S rRNA gene sequence data were processed by using two pipelines, LotuS (Hildebrand et al., 2014) and QIIME v1.9.1 (Caporaso et al., 2010) as described previously (Adyari et al., 2020). In brief, the paired-end reads were quality trimmed, merged, and clustered into operational taxonomic units (OTUs) with a threshold of ≥97% similarity (Hildebrand et al., 2014).
Spatial autocorrelation and temporal variation of contaminants of emerging concern in a typical urbanizing river
2022, Water ResearchCitation Excerpt :CECs are frequently detected in various environmental systems, including surface water (Sun et al., 2016b), drinking water (Qiao et al., 2011), wastewater, sludge, and suspended solids (Y. Y. Wang et al., 2018). Great attention has been paid to CECs due to their potential negative effects on the health of humans and other organisms (Brausch and Rand, 2011; Kim et al., 2009), including endocrine disruption (Subedi et al., 2015), the spread of antibiotic resistance genes (Schoenfuss et al., 2016), and ecological disruption (Adyari et al., 2020; Hu et al., 2020, 2017), such as altering ecological interactions and processes or altering relationships among organisms (Richmond et al., 2017). River water is an important source of drinking water.