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Salinity determines performance, functional populations, and microbial ecology in consortia attenuating organohalide pollutants

The ISME Journal volume 17, pages 660–670 (2023)Cite this article

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Abstract

Organohalide pollutants are prevalent in coastal regions due to extensive intervention by anthropogenic activities, threatening public health and ecosystems. Gradients in salinity are a natural feature of coasts, but their impacts on the environmental fate of organohalides and the underlying microbial communities remain poorly understood. Here we report the effects of salinity on microbial reductive dechlorination of tetrachloroethene (PCE) and polychlorinated biphenyls (PCBs) in consortia derived from distinct environments (freshwater and marine sediments). Marine-derived microcosms exhibited higher halotolerance during PCE and PCB dechlorination, and a halotolerant dechlorinating culture was enriched from these microcosms. The organohalide-respiring bacteria (OHRB) responsible for PCE and PCB dechlorination in marine microcosms shifted from Dehalococcoides to Dehalobium when salinity increased. Broadly, lower microbial diversity, simpler co-occurrence networks, and more deterministic microbial community assemblages were observed under higher salinity. Separately, we observed that inhibition of dechlorination by high salinity could be attributed to suppressed viability of Dehalococcoides rather than reduced provision of substrates by syntrophic microorganisms. Additionally, the high activity of PCE dechlorinating reductive dehalogenases (RDases) in in vitro tests under high salinity suggests that high salinity likely disrupted cellular components other than RDases in Dehalococcoides. Genomic analyses indicated that the capability of Dehalobium to perform dehalogenation under high salinity was likely owing to the presence of genes associated with halotolerance in its genomes. Collectively, these mechanistic and ecological insights contribute to understanding the fate and bioremediation of organohalide pollutants in environments with changing salinity.

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Fig. 1: Effects of salinity on microbial reductive dechlorination of PCE and PCBs in microcosms.
Fig. 2: Microbial communities in microcosms under different salinities.
Fig. 3: Influence of salinity on co-occurrence networks and assembly of microbial communities in microcosms.
Fig. 4: Inhibition of high salinity on growth of organohalide-respiring bacteria in microcosms.
Fig. 5: Influence of salinity on PCE dechlorination and cell growth in the pure cultures of Dehalococcoides.
Fig. 6: In vitro dechlorination of PCE under different salinities.
Fig. 7: Dechlorination activity and cell abundance of organohalide-respiring bacteria during subculturing of the halotolerant dechlorinating culture F.
Fig. 8: Genes related to halotolerance in different subcultures revealed by metagenomic sequencing.

Data availability

The 16 S rRNA gene amplicon sequencing and metagenomic sequencing data are archived at National Center for Biotechnology Information under accession number PRJNA836174.

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Acknowledgements

This study was supported by the Ministry of Education, Singapore under Academic Research Fund Tier 2 under project No.: MOE-00003301 and Tier 1 under Project No.: R-302-000-239-114.

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Authors and Affiliations

  1. Department of Civil and Environmental Engineering, National University of Singapore, Singapore, 117576, Singapore

    Guofang Xu, Xuejie Zhao, Siyan Zhao, Matthew J. Rogers & Jianzhong He

  2. NUS Graduate School - Integrative Sciences and Engineering Programme (ISEP), National University of Singapore, Singapore, 119077, Singapore

    Guofang Xu & Jianzhong He

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GX and JH designed the study. GX and XZ performed the experiments. GX and MR analyzed the data. GX wrote the manuscript with the help of SZ. GX, SZ, MR and JH contributed to the revision and finalization of the manuscript.

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Correspondence to Jianzhong He.

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Xu, G., Zhao, X., Zhao, S. et al. Salinity determines performance, functional populations, and microbial ecology in consortia attenuating organohalide pollutants. ISME J 17, 660–670 (2023). https://doi.org/10.1038/s41396-023-01377-1

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