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Light-independent phytoplankton degradation and detoxification of methylmercury in water

Nature Water volume 1, pages 705–715 (2023)Cite this article

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Abstract

Phytoplankton serves as a key entry point for the trophic transfer and bioaccumulation of the neurotoxin methylmercury (MeHg) in aquatic food webs. However, it is unclear whether and how phytoplankton itself may degrade and metabolize MeHg in the dark. Here, using several strains of the freshwater alga Chlorella vulgaris, the marine diatom Chaetoceros gracilis and two cyanobacteria (or blue-green algae), we report a light-independent pathway of MeHg degradation in water by phytoplankton, rather than its associated bacteria. About 36–85% of MeHg could be degraded intracellularly to inorganic Hg(II) and/or Hg(0) via dark reactions. Endogenic reactive oxygen species, particularly singlet oxygen, were identified as the main driver of MeHg demethylation. Given the increasing incidence of algal blooms in lakes and marine systems globally, these findings underscore the potential roles of phytoplankton demethylation and detoxification of MeHg in aquatic ecosystems and call for improved modelling and assessment of MeHg bioaccumulation and environmental risks.

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Fig. 1: Dark degradation of MeHg by phytoplankton cells and filtrates.
Fig. 2: Hg species distributions during MeHg degradation in the dark.
Fig. 3: Demethylation by phytoplankton cell filtrates and lysates.
Fig. 4: Reactive oxygen species in phytoplankton demethylation.
Fig. 5: Phytoplankton demethylation in natural waters.

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Acknowledgements

We thank X. Yin and Z. Li for technical assistance in experiments and biochemical analyses. This research was supported in part by the Office of Biological and Environmental Research within the Office of Science of the US Department of Energy (DOE), as part of the Critical Interfaces Science Focus Area project at Oak Ridge National Laboratory (ORNL), and by the National Natural Science Foundation of China (12222509 and 42107383) and the Natural Science Foundation of Jiangsu Province (BK20200322). The DOE will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan). ORNL is managed by UT-Battelle, LLC under contract no. DE-AC05-00OR22725 with DOE.

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Author notes

  1. These authors contributed equally: Xujun Liang, Huan Zhong, Alexander Johs, Pei Lei.

Authors and Affiliations

  1. Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA

    Xujun Liang, Alexander Johs, Lijie Zhang, Nali Zhu, Xixiang Yin, Lihong Wang, Jiating Zhao, Eric M. Pierce & Baohua Gu

  2. Department of Biosystems Engineering and Soil Science, University of Tennessee, Knoxville, TN, USA

    Xujun Liang, Jiating Zhao & Baohua Gu

  3. Guangdong Key Laboratory of Environmental Pollution and Health, School of Environment, Jinan University, Guangzhou, China

    Xujun Liang & Eddy Y. Zeng

  4. State Key Laboratory of Pollution Control and Resources Reuse, School of Environment, Nanjing University, Nanjing, China

    Huan Zhong & Jin Zhang

  5. School of Environment, Nanjing Normal University, Nanjing, China

    Pei Lei

  6. Climate and Ecosystem Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Neslihan Taş

  7. Illinois Sustainable Technology Center, Illinois State Water Survey, Champaign, IL, USA

    Linduo Zhao

  8. Key Laboratory for Biomedical Effects of Nanomaterials and Nanosafety, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, China

    Yuxi Gao

  9. Department of Environmental Science, Zhejiang University, Hangzhou, China

    Jiating Zhao

  10. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA

    Dale A. Pelletier

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  1. Xujun Liang
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Contributions

Conceptualization: X.L., J. Zhao., B.G. and H.Z.; investigation and data curation: X.L., H.Z., A.J., P.L., J. Zhang, N.T., L. Zhang, L. Zhao, J. Zhao and B.G.; methodology: X.L., J. Zhao, H.Z., A.J., P.L. and B.G; support: N.Z., X.Y., L.W., E.Y.Z., Y.G., D.A.P. and E.M.P.; writing—original draft: X.L., J. Zhao, A.J. and B.G.; writing—review and editing: all authors; funding: B.G., E.M.P., J. Zhao and H.Z.

Corresponding authors

Correspondence to Jiating Zhao or Baohua Gu.

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Nature Water thanks David Amouroux, Amina Schartup and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended Data Fig. 1 Methylmercury (MeHg) degradation and its degradation products [inorganic Hg(II) and Hg(0)] by Chlorella vulgaris CV395, Chaetoceros gracilis CG2658, Synechocystis sp. PCC6803, and Microcystis sp. 0824.

Methylmercury (MeHg) degradation and its degradation products [inorganic Hg(II) and Hg(0)] by Chlorella vulgaris CV395, Chaetoceros gracilis CG2658, Synechocystis sp. PCC6803, and Microcystis sp. 0824 under dark conditions. The added MeHg concentration was 25 nM, and each Hg species was normalized to the total Hg (THg) at each timepoint. Data are mean ± 1 SD (n = 4, except for zero time points with n =2).

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Extended Data Fig. 2 Changes in dissolved oxygen (a), malondialdehyde (MDA) (b) and cell morphology (c) of Chlorella vulgaris (CV2338, 1×105 cells/mL) during a 5-day incubation period with MeHg (0.05 nM).

For panel (B), CV2338 cells were collected by centrifugation at 4000 rpm and 4 °C for 10 min. Cells were homogenized in 4 mL of PBS (pH 7.8, 4 °C) by an ultrasonic cell disruptor in an ice bath for 5 min. After centrifugation at 4000 rpm for 10 min at 4 °C, the supernatant was used to evaluate the MDA content, as previously described89,90. Data in (a) and (b) are mean ± 1 SD (n = 3).

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Extended Data Fig. 3 Methylmercury (MeHg) degradation under either 24-h dark or 12-h Light+12-h Dark conditions by phytoplankton Chlorella vulgaris CV2338.

Methylmercury (MeHg) degradation under either 24-h dark or 12-h Light + 12-h Dark conditions by phytoplankton Chlorella vulgaris CV2338 at the MeHg concentration of 0.05 nM and CV concentration of 1×105 cells mL−1. Different letters (a and b) denote significant differences among different treatments (one-way ANOVA, p < 0.05). Data are mean ± 1 SD (n = 3).

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Extended Data Fig. 4 (A) Gel electrophoresis analyses of 16S rDNA and (B) PCR-amplified 16S rDNA extracted from Chlorella vulgaris 2338 cell suspensions. (C, D) Scanning electron microscopic (SEM) images of CV2338 cells used in demethylation assays.

(A) Gel electrophoresis analyses of 16S rDNA and (B) PCR-amplified 16S rDNA extracted from Chlorella vulgaris 2338 cell suspensions. (C, D) Scanning electron microscopic (SEM) images of CV2338 cells used in demethylation assays in Figs. 1c, 2b, 3c, d, 5c, d. No visible bands or bacterial contamination were observed in these samples.

Extended Data Fig. 5 Multiple sequence alignment and phylogeny of known and putative flavoprotein oxidoreductase genes.

The sequences of four mercuric reductase (MerA) genes from canonical mer operon variants were aligned with homologs identified in the phytoplankton strains investigated in this study. Residues known to be important for catalysis in mercuric reductase are indicated by red arrows and boxes. The N-terminal sequence region corresponding to the Hg(II)-metallochaperone domain NmerA is shaded in light blue. The level of sequence conservation within the alignment is indicated (darker = higher conservation).

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Extended Data Fig. 6 Evaluation of reactive oxygen species (ROS), including singlet oxygen (1O2), superoxide (O2·−), and hydroxyl (·OH) radicals, on dark degradation of methylmercury (MeHg, 0.05 nM) in the cell lysate of Chlorella vulgaris CV2338.

Evaluation of reactive oxygen species (ROS), including singlet oxygen (1O2), superoxide (O2·−), and hydroxyl (·OH) radicals, on dark degradation of methylmercury (MeHg, 0.05 nM) in the cell lysate of Chlorella vulgaris CV2338 with or without added ROS scavengers. The reaction time was set at 1 h. β-carotene and 2.5-dimethylfuran are used to scavenge 1O. Superoxide dismutase (SOD) is used to scavenge O2·−. Ethyl alcohol is used to scavenge ·OH58. Letters (a and b) denote significant differences among different treatments (one-way ANOVA, p < 0.05). Data are mean ± 1 SD (n = 3 or 4).

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Extended Data Fig. 7 Fluorescence intensity of singlet oxygen signal in Chlorella vulgaris CV2338 cells.

CV2338 cells cultured under various environmental conditions (for example, light/dark) were washed three times with PBS solution and resuspended in PBS solution. PBS solutions without any CV2338 cells were set as blank. Cell suspensions (at approximately 1.5×108 cells mL−1) were reacted with the singlet oxygen fluorescent probe Singlet Oxygen Sensor Green (SOSG) for 30 min and then observed under a confocal laser scanning microscope (Zeiss LSM880 with Airyscan)83,85. Data are mean ± 1 SD (n = 3 or 5).

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Extended Data Fig. 8 Fluorescence signal of singlet oxygen in Chlorella vulgaris CV2338 cell lysates upon ultrasonication and incubation.

CV lysates were reacted with the singlet oxygen fluorescent probe Singlet Oxygen Sensor Green (SOSG) for 30 min83,85. Fluorescence intensities were measured using previously established methods91, with an excitation wavelength of 488 nm and an emission wavelength of 530 nm. Data are mean ± 1 SD (n = 4). Letters (a, b, or c) denote significant differences among different treatments (one-way ANOVA, p < 0.05).

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Extended Data Fig. 9 Methylmercury (MeHg) degradation with added Chlorella vulgaris CV2338 cells in filter-sterilized through 0.2-µm syringe filters or unfiltered Yangshan (YS) lake water-2.

Methylmercury (MeHg) degradation with added Chlorella vulgaris CV2338 cells in filter-sterilized through 0.2-µm syringe filters or unfiltered Yangshan (YS) lake water-2 (sampled on November 2022). Experiments performed at low concentrations of MeHg (0.05 nM) and CV2338 cells (1×105 cells mL−1). Data are mean ± 1 SD (n = 3).

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Extended Data Table 1 Estimated pseudo-first order rate constants (k) for methylmercury (MeHg) degradation by phytoplankton
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Liang, X., Zhong, H., Johs, A. et al. Light-independent phytoplankton degradation and detoxification of methylmercury in water. Nat Water 1, 705–715 (2023). https://doi.org/10.1038/s44221-023-00117-1

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