Diversity of bacteria and archaea in the groundwater contaminated by chlorinated solvents undergoing natural attenuation

https://doi.org/10.1016/j.envres.2020.109457Get rights and content

Highlights

  • The alpha diversity of archaeal community was more sensitive to CS contamination than that of bacterial community.

  • The ORP, DO, temperature and methane concentration were major drivers of bacterial and archaeal community composition.

  • Both indigenous bacterial and archaeal community compositions are capable of withstanding elevated CS contamination.

Abstract

Chlorinated solvents (CS)-contaminated groundwater poses serious risks to the environment and public health. Microorganisms play a vital role in efficient remediation of CS. In this study, the microbial community (bacterial and archaeal) composition of three CS-contaminated groundwater wells located at an abandoned chemical factory which covers three orders of magnitude in concentration (0.02–16.15 mg/L) were investigated via 16S rRNA gene high-throughput sequencing. The results indicated that Proteobacteria and Thaumarchaeota were the most abundant bacterial and archaeal groups at the phylum level in groundwater, respectively. The major bacterial genera (Flavobacterium sp., Mycobacterium sp. and unclassified Parcubacteria taxa, etc.) and archaeal genera (Thaumarchaeota Group C3, Miscellaneous Crenarchaeotic Group and Miscellaneous Euryarchaeotic Group, etc.) might be involved in the dechlorination processes. In addition, Pearson's correlation analyses showed that alpha diversity of the bacterial community was not significantly correlated with CS concentration, while alpha diversity of archaeal community greatly decreased with the increased contamination of CS. Moreover, partial Mantel test indicated that oxidation-reduction potential, dissolved oxygen, temperature and methane concentration were major drivers of bacterial and archaeal community composition, whereas CS concentration had no significant impact, indicating that both indigenous bacterial and archaeal community compositions are capable of withstanding elevated CS contamination. This study improves our understanding of how the natural microbial community responds to high CS-contaminated groundwater.

Introduction

Chlorinated solvents (CS), such as trichloroethylene (TCE) and tetrachloroethylene (PCE), chloroform and 1,1,1-trichloroethane are used for a variety of commercial and industrial purposes, including dry cleaning, metal cleaning, degreasing, automotive aerosols, printing, paper and textile industries, paint removal, furniture industry (Mortan et al., 2017). Contamination of groundwater with CS is frequently observed in industrial areas as a result of improper handling or accidental leakages. In addition, CS can be released into the environment during production, storage, transport and use processes (Bhatt et al., 2007). Currently, CS are the most frequently detected organic contaminants worldwide (Bhattacharjee and Ghoshal, 2018). As most CS are known or suspected human carcinogens or mutagens (Brisson et al., 2012; Houde et al., 2015), these compounds are designated as priority pollutants by the U.S. Environmental Protection Agency (EPA). Therefore, it is necessary to understand their behavior in the environment for their control and remediation.

Over the past several years, natural attenuation has become increasingly accepted as a remediation strategy for chlorinated solvents in groundwater (Kawabe and Komai, 2019; Scow and Hicks, 2005; Wright et al., 2017). The term “natural attenuation” refers to naturally-occurring processes in soil and groundwater which reduce the mass, toxicity, mobility, volume, or concentration of contaminants without human intervention. These processes include physical, chemical and biological transformations (Mulligan and Yong, 2004). Under conditions found in the majority of groundwater, biodegradation is believed to be the major process for the oxidation or reduction of contaminants. A variety of microorganisms able to utilize CS have been reported, including the polychlorinated aliphatic alkanes-dehalogenating bacterium Dehalogenimonas lykanthroporepellens (Moe et al., 2009), chlorinated alkane dehalogenating bacterium Dehalogenimonas alkenigignens (Bowman et al., 2013), dichloromethane-degrading bacterium Candidatus Dichloromethanomonas elyunquensis (Kleindienst et al., 2017), chloroanilines-dehalogenating Dehalococcoides mccartyi strain CBDB1 and Dehalobacter strain 14DCB1 (Zhang et al., 2017), chlorinated alkane-respiring bacterium Dehalogenimonas formicexedens (Key et al., 2017), etc. As only a minor proportion of environmental microorganisms can be cultivated, the majority of bacterial strains involved in CS biotransformation cannot be fully described using culture dependent methods. In addition, complete dichlorination of highly substituted CS such as TCE and TeCA to nontoxic ethylene involves a mixed consortium of organisms (Manchester et al., 2012; Mortan et al., 2017). In the past two decades, the biotransformation of CS by indigenous microbial community has been well documented. For example, in the early 1990s, a total of 104 (94 bacterial and 10 archaeal) sequence types were determined by using the restriction fragment length polymorphisms (RFLP) and clone library to investigate the microbial communities associated with an aquifer contaminated with hydrocarbons and chlorinated solvents (Dojka et al., 1998). Later, the community composition of microbial cultures for chlorinated ethene-degrading was studied by using PCR-denaturing gradient gel electrophoresis (PCR-DGGE) and quantitative PCR method (Duhamel and Edwards, 2006), the results showed that Dehalococcoides populations were the dominant phylotypes. Recently, studies on the microbial communities associated with the dechlorination process have been remarkably promoted by the 16S rRNA gene amplicon sequencing approach with metagenomic sequencing (Brisson et al., 2012; David et al., 2015; Delgado et al., 2017; Kao et al., 2016; Liu et al., 2018; Simsir et al., 2017; Wright et al., 2017; Yu et al., 2016a). Most of these previous researches were based on data in the laboratory and in pilot field tests, but study in the natural environment could obtain more authentic information on the changes of microbial community composition in the contaminated environments. Wright et al. (2017) reported that dichloromethane degrading organisms, such as the Desulfosporosinus, thrived within the most heavily contaminated groundwater samples. However, to date, the available information about the microbial community involved in CS biotransformation in the in situ environment are still not understood in detail. Additionally, relatively little is known regarding the effect of CS contamination and physio-chemical parameters on the microbial communities at field sites undergoing natural attenuation.

In the present study, CS contaminated groundwater showing natural attenuation was selected. The objectives of our study were 1) to evaluate the microbial community response to CS contamination; 2) to explore the native structure of the bacterial and archaeal communities involved in the CS biotransformation process; and 3) to better understand the relationship between the microbial community and environmental parameters, and their correlation with groundwater contamination.

Section snippets

Sample collection

The contaminated site was located at an abandoned chemical factory in the east of Beijing, China. During its operation, various CS were imported as raw materials or produced as final products, resulting in the site's groundwater pollution. Groundwater samples were taken using a PTFE bailer (Cole-Parmer, Chicago, 1 L, USA) from three wells contaminated with CS, three water samples were taken from each well at three different time points within 24 h. The depth of groundwater samples for wells

Physio-chemical parameters of multiple wells

As shown in Table S1, total CS concentration spanned three orders of magnitude (0.02–16.15 mg/L) with the highest levels detected in BJ12. No distinct differences in measured water chemical parameters were observed between groundwater samples collected in the wells BJ2 and BJ20. However, significant differences were found between BJ12 and the other two wells. There were 4, 11 and 8 different organic chlorinated compounds in BJ2, BJ12 and BJ20, respectively (Table S2), with 1,2-dichlorobenzene

Discussion

Microorganisms play important roles in the self-remediation activity and their compositions that are largely influenced by the external pollutants (Liang et al., 2019). In the present study, the microbial communities of three different wells contaminated with organic CS, with concentrations spanned three orders of magnitude, were studied by using Illumina MiSeq sequencing. Bacteroidetes, Proteobacteria, Actinobacteria and Parcubacteria were found to be the most abundant in all wells. This was

Conclusion

The microbial community (bacterial and archaeal) composition of three different CS-contaminated groundwater wells were analyzed by using high-throughput 16S rRNA gene analysis. The most abundant bacterial phyla in three wells were Bacteroidetes, Proteobacteria, Actinobacteria and Parcubacteria, while Thaumarchaeota, Unclassified Archaeal and Woesearchaeota were the most abundant archaeal phyla. Some genera may be involved in microbial oxidation or reduction of CS were also identified (i.e.

Funding

This study was financially supported by the National Natural Science Foundation of China (Nos. 41977122, 21577007, 31500083 and 31601642), the National Key Research and Development Program of China (No. 2017YFD0800102), and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA23010400).

Author statement

D.C.J., F.S.Z., Y.F.X., and X.M.D. planned and designed the research. X.K., Y.S., Y.X.L., and R.Y.Z. performed experiments and analyzed data. D.C.J. wrote the main manuscript text and all the authors contributed to the revision of the manuscript and approved the version to be published.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relavtionships that could have appeared to influence the work reported in this paper.

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