Elsevier

Science of The Total Environment

Volume 627, 15 June 2018, Pages 600-612
Science of The Total Environment

Shift in the microbial community composition of surface water and sediment along an urban river

https://doi.org/10.1016/j.scitotenv.2018.01.203Get rights and content

Highlights

  • Microbial community in the urban river exhibited spatial variations due to the joint influence of chemical variables

  • The microbial OTUs richness decreased in the urban area

  • TP, NO3- and metals (Zn, Fe) were the most determining factors impacting the surface water microbial compositions

  • Higher abundance of genes associated with xenobiotic metabolism were observed in the urban surface water and sediments

Abstract

Urban rivers represent a unique ecosystem in which pollution occurs regularly, leading to significantly altered of chemical and biological characteristics of the surface water and sediments. However, the impact of urbanization on the diversity and structure of the river microbial community has not been well documented. As a major tributary of the Yangtze River, the Jialing River flows through many cities. Here, a comprehensive analysis of the spatial microbial distribution in the surface water and sediments in the Nanchong section of Jialing River and its two urban branches was conducted using 16S rRNA gene-based Illumina MiSeq sequencing. The results revealed distinct differences in surface water bacterial composition along the river with a differential distribution of Proteobacteria, Cyanobacteria, Actinobacteria, Bacteroidetes and Acidobacteria (P < 0.05). The bacterial diversity in sediments was significantly higher than their corresponding water samples. Additionally, archaeal communities showed obvious spatial variability in the surface water. The construction of the hydropower station resulted in increased Cyanobacteria abundance in the upstream (32.2%) compared to its downstream (10.3%). Several taxonomic groups of potential fecal indicator bacteria, like Flavobacteria and Bacteroidia, showed an increasing trend in the urban water. PICRUSt metabolic inference analysis revealed a growing number of genes associated with xenobiotic metabolism and nitrogen metabolism in the urban water, indicating that urban discharges might act as the dominant selective force to alter the microbial communities. Redundancy analysis suggested that the microbial community structure was influenced by several environmental factors. TP (P < 0.01) and NO3 (P < 0.05), and metals (Zn, Fe) (P < 0.05) were the most significant drivers determining the microbial community composition in the urban river. These results highlight that river microbial communities exhibit spatial variation in urban areas due to the joint influence of chemical variables associated with sewage discharging and construction of hydropower stations.

Introduction

Rivers or streams flowing through cities always serve as an important sink for waste materials, urban sewage, and storm water run-off. They are also the main source of drinking or industrial water in cities, especially those along the river. Microorganisms inhabiting these ecosystems are one of the crucial players in the biogeochemical cycling of organic matter and nutrients, biodegradation and biotransformation of pollutants, and the recovery and maintenance of ecosystem health and balance (Bai et al., 2014; Kirchman, 1994; Ruiz-González et al., 2015). Although there has been an increasing awareness of water quality and great efforts are being taken to ensure greater sustainability of urban rivers, the accelerating development of cities, commonly in developing countries, inevitably leads to an increase in river deterioration (Suthar et al., 2010) due to high-load discharge and water front construction. Meanwhile, the water microbial properties, particularly the diversity and community structure, could be susceptibly influenced by the spatial variability of the physicochemical and biotic parameters, which can be used as an indicator of environmental conditions (Kostanjsek et al., 2005; Lundgaard et al., 2017; Tiquia, 2010). Most previous laboratory and field studies assessing the impact of urban human activity on surface water and sediments have focused on physicochemical indexes such as heavy metals (Vink et al., 1999; Zheng et al., 2008), hydrocarbons (Yunker et al., 2002) or nutrients (Howarth et al., 2000), and algal characters (Biggs, 2000; Flynn et al., 2013). The in-depth understanding of microbial community diversity in the flowing urban river is still lacking, and is less explored than that of marine or lake ecosystems (Zinger et al., 2012).

It is well-understood that microbial communities are taxonomically distinct at different spatial and temporal scales in river systems (Garcia-Armisen et al., 2014; Savio et al., 2015; Zhi et al., 2015). Urban rivers are rather spatially heterogeneous ecosystems that are mainly influenced by the terrestrial environment. Sewage from the residential areas containing organic and inorganic pollutants notably alters the basic parameters of freshwater, such as pH, temperature, dissolved oxygen content, and light penetration, which could further reshape the bacterial community structure (Garcia-Armisen et al., 2014; Lindström et al., 2005; Mark Ibekwe et al., 2012). The sewage system seems to be an eutrophic environment for stimulating the growth of microorganisms which are likely to be physiologically adapted to this environment. In addition, sewage also introduces microbiological contamination to the river which can have a key impact on the diversity and function of the bacterial community (Drury et al., 2013). To some degree, the spatial distribution of river bacterial communities is also associated with the landscape topography and hydrology (Crump et al., 2007; Lindström and Bergström, 2004). The variations in valley width, hydrologic connections, and flow can directly influence the water residence time and water dilution capacity. These factors are related to the balance process between the bacteria from terrestrial or sewage source, and indigenous communities, and the stabilization of the communities by predation or competition (Crump et al., 2007; Lozupone and Knight, 2007; Read et al., 2015; Székely et al., 2013), which might indirectly or directly affect the microbial community function. As a result, it is essential to understand the microbial communities in the context of their spatial distribution and microbial diversity in a river to monitor the ecosystem health and function. Recently, a growing number of nations have highlighted the development of small hydropower resources (Karki, 2007; Li et al., 2009; Yüksel, 2007). The construction of hydropower stations could exert a significant influence on altering the upstream and downstream water quality (Zhang et al., 2005). These changes can greatly affect the microbial communities in the aquatic system (Sekiguchi et al., 2002; Yan et al., 2015). Several studies have described the impact of hydropower stations on phytoplankton (Sow et al., 2016; Ye et al., 2006; Zhou et al., 2011) and other related environmental changes (Zhang et al., 2005). However, there exists little data regarding their effects on microorganisms. Therefore, an attempt to determine the shift in microbial communities caused by hydropower projects has also been emphasized in the present study.

We hypothesized that addition of high nutrient elements from anthropogenic sources associated with urbanization is an important impetus for altering the microbial communities in the surface water and sediment of urban rivers. In the current study, the Jialing River (Nanchong section), which is the second longest tributary of the Yangtze River impacted by urbanization and a small hydropower station, was chosen as a model to gain insight into the variation of bacterial communities in the urban river. We performed 16S rRNA gene-based high-throughput sequencing on the microbial communities of eight surface water samples (two of which were collected from the urban branches) and three representative sediments. The objectives of the study are as follows: (i) to study the spatial variations in bacterial communities along the urban river; (ii) to reveal the main environmental factors leading to the altered dynamics change of microbial communities; and (iii) to identify the response of microbial communities to urban discharge and the construction of a hydropower station in terms of microbial composition and metabolic prediction analysis.

Section snippets

Description of sampling sites

The Jialing River is the second longest tributary of the YangtZe River in China, and stretches over 1120 km from Qinling Mountain to Chong Qing city (Zhang et al., 2008). Nanchong is located in the low reach of the Jialing River, and the river runs through Nanchong city. The flow direction throughout Nanchong City is from the north to the south. The area is highly urbanized with a population of over 7.6 million. Jialing River is the main source of drinking and household water, and also the main

Physicochemical properties of water and sediment samples

The physicochemical characteristics of the water and sediment samples collected from each sampling site are shown in Table 1. Temperature and pH ranged from 25.0 to 28.0 °C and 7.91 to 8.22 in all water samples, respectively. Significant differences in water NO3 and NO2 content among samples were observed (P < 0.05). The hydropower station built between the 2W and 3W did not affect the chemical characters measured in this study. The NO3and TP contents in branch 5BW were higher than those in

Discussion

There is a large degree of variation in the freshwater bacterial community in terms of taxonomic composition and spatial distribution among or within different rivers (Bai et al., 2014; Garcia-Armisen et al., 2014; Ibekwe et al., 2016; Ouattara et al., 2014; Ruiz-González et al., 2015), how and where the shift of microbial communities occurs in a certain urban river remains largely unexplored. The shifts in aquatic and sediment bacterial communities were determined by Illumina Miseq sequencing

Conclusion

In conclusion, our study demonstrates the spatial shift in microbial communities of freshwater and sediments in an integral urban river, shaped by environmental variables like TP, NO3, DO, metals (Fe, Zn) and a hydropower station. We also demonstrate significant differences in the bacterial and archaeal community composition between the branches and the main river within the same district. The construction of the hydropower station led to the high abundance of Cyanobacteria in the upstream

Acknowledgments

This work was financially supported by the National Science Foundation of China (41606142) and the Fundamental Research Funds of China West Normal University (463140 and 412554). We thank Tao Hou for the sample collection, and Mingli Liao, Xiao Xu for their assistance in chemical analysis. We are grateful to the two anonymous reviewers for the great comments that improved the manuscript greatly.

References (103)

  • Y. Tian et al.

    PAHs contamination and bacterial communities in mangrove surface sediments of the Jiulong River Estuary, China

    Mar. Pollut. Bull.

    (2008)
  • S.M. Tiquia

    Metabolic diversity of the heterotrophic microorganisms and potential link to pollution of the Rouge River

    J. Environ. Pollut.

    (2010)
  • R. Vink et al.

    Development of the heavy metal pollution trends in several European rivers: an analysis of point and diffuse sources

    Water Sci. Technol.

    (1999)
  • N. Wéry et al.

    Behaviour of pathogenic and indicator bacteria during urban wastewater treatment and sludge composting, as revealed by quantitative PCR

    J. Water Res.

    (2008)
  • P. Withers et al.

    Delivery and cycling of phosphorus in rivers: a review

    Sci. Total Environ.

    (2008)
  • M. Yunker et al.

    Sources and significance of alkane and PAH hydrocarbons in Canadian arctic rivers

    Estuar. Coast. Shelf Sci.

    (2002)
  • N. Zheng et al.

    Characterization of heavy metal concentrations in the sediments of three freshwater rivers in Huludao City, Northeast China

    J. Environ. Pollut.

    (2008)
  • Y. Bai et al.

    Using high-throughput sequencing to assess the impacts of treated and untreatewastewater discharge on prokaryotic communities in an urban river

    Appl. Environ. Microbiol.

    (2014)
  • H.A. Barton et al.

    Molecular phylogenetic analysis of a bacterial community in an oligotrophic cave environment

    Geomicrobiol J.

    (2004)
  • R. Benveniste et al.

    Aminoglycoside antibiotic-inactivating enzymes in actinomycetes similar to those present in clinical isolates of antibiotic-resistant bacteria

    PNAS

    (1973)
  • B.J. Biggs

    Eutrophication of streams and rivers: dissolved nutrient-chlorophyll relationships for benthic algae

    J. N. Am. Benthol. Soc.

    (2000)
  • D. Blankenberg et al.

    Galaxy: a web-based genome analysis tool for experimentalists

    Curr. Protoc. Mol. Biol.

    (2010)
  • M. Candela et al.

    High taxonomic level fingerprint of the human intestinal microbiota by ligase detection reaction - universal array approach

    BMC Microbiol.

    (2010)
  • Z. Cao et al.

    Distribution and ecosystem risk assessment of polycyclic aromatic hydrocarbons in the Luan River, China

    Ecotoxicology

    (2010)
  • J.G. Caporaso et al.

    PyNAST: a flexible tool for aligning sequences to a template alignment

    Bioinformatics

    (2010)
  • J.G. Caporaso et al.

    QIIME allows analysis of high-throughput community sequencing data

    Nat. Methods

    (2010)
  • V. Cattoir et al.

    Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp

    Emerg. Infect. Dis.

    (2008)
  • A. Chao

    Nonparametric estimation of the number of classes in a population

    Scand. J. Stat.

    (1984)
  • A. Chao et al.

    Estimating the number of classes via sample coverage

    J. Am. Stat. Assoc.

    (1992)
  • K. Clarke et al.

    Primer v6: User Manual/Tutorial Plymouth UK

    (2006)
  • B.C. Crump et al.

    Biogeography of bacterioplankton in lakes and streams of an arctic tundra catchment

    J. Ecol.

    (2007)
  • S.E. Dowd et al.

    Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP)

    BMC Microbiol.

    (2008)
  • B. Drury et al.

    Wastewater treatment effluent reduces the abundance and diversity of benthic bacterial communities in urban and suburban rivers

    Appl. Environ. Microbiol.

    (2013)
  • R.C. Edgar

    Search and clustering orders of magnitude faster than BLAST

    Bioinformatics

    (2010)
  • K.P. Feris et al.

    Seasonal dynamics of shallow-hyporheic-zone microbial community structure along a heavy-metal contamination gradient

    Appl. Environ. Microbiol.

    (2004)
  • J.G. Ferry et al.

    Methanospirillum, a new genus of methanogenic bacteria, and characterization of Methanospirillum hungatii sp. nov

    Int. J. Syst. Evol. Microbiol.

    (1974)
  • N. Fierer et al.

    Toward an ecological classification of soil bacteria

    J. Ecol.

    (2007)
  • H.M. Galvão et al.

    Ecological tools for the management of cyanobacteria blooms in the Guadiana River watershed, Southwest Iberia

  • T. Garcia-Armisen et al.

    Seasonal variations and resilience of bacterial communities in a sewage polluted urban river

    PLoS One

    (2014)
  • J. Goecks et al.

    Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences

    Genome Biol.

    (2010)
  • M. Goodfellow et al.

    Ecology of actinomycetes

    Annu. Rev. Microbiol.

    (1983)
  • C.J. Hayden et al.

    Microbial diversity and community structure along a lake elevation gradient in Yosemite National Park, California, USA

    Environ. Microbiol.

    (2016)
  • R.W. Howarth et al.

    Issues in Ecology: Nutrient Pollution of Coastal Rivers, Bays, and Seas

    (2000)
  • T. Jin et al.

    Diversity and quantity of ammonia-oxidizing archaea and bacteria in sediment of the Pearl River Estuary, China

    J. Appl. Microbiol. Biotechnol.

    (2011)
  • J.-H. Kang et al.

    Bisphenol A degradation by bacteria isolated from river water

    Arch. Environ. Contam. Toxicol.

    (2002)
  • J.-H. Kang et al.

    Bisphenol A in the aquatic environment and its endocrine-disruptive effects on aquatic organisms

    Crit. Rev. Toxicol.

    (2007)
  • M.M. Kansole et al.

    Microcystin-LR biodegradation by Bacillus sp.: reaction rates and possible genes involved in the degradation

    Water

    (2016)
  • S.K. Karki

    Implications of Small Hydropower Plants in Power Sector Development: A Case of Nepal

    (2007)
  • D.L. Kirchman

    The uptake of inorganic nutrients by heterotrophic bacteria

    J. Microb. Ecol.

    (1994)
  • D.L. Kirchman et al.

    Changes in bacterial activity and community structure in response to dissolved organic matter in the Hudson River, New York

    Aquat. Microb. Ecol.

    (2004)
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