Abstract
Our demand for electronic goods and fossil fuels has challenged our ecosystem with contaminating amounts of heavy metals, causing numerous water sources to become polluted. To counter heavy-metal waste, industry has relied on a family of physicochemical processes, with chemical precipitation being one of the most commonly used. However, the disadvantages of chemical precipitation are vast, including the generation of secondary waste, technical handling of chemicals and need for complex infrastructures. To circumvent these limitations, biological processes to naturally manage waste have been sought. Here, we show that yeast can act as a biological alternative to traditional chemical precipitation by controlling naturally occurring production of hydrogen sulfide (H2S). Sulfide production was harnessed by controlling the sulfate assimilation pathway, where strategic knockouts and culture conditions generated H2S from 0 to over 1,000 ppm (~30 mM). These sulfide-producing yeasts were able to remove mercury, lead and copper from real-world samples taken from the Athabasca oil sands. More so, yeast surface display of biomineralization peptides helped control for size distribution and crystallinity of precipitated metal sulfide nanoparticles. Altogether, this yeast-based platform not only removes heavy metals but also offers a platform for metal re-extraction through precipitation of metal sulfide nanoparticles.
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Acknowledgements
We thank the Koch Institute Facilities, Center for Material Science Facilities (CMSE), the Whitehead Keck Microscopy Facility, as well as Y. Zhang (CMSE) and N. Watson (Keck) for assisting in TEM sample prep and imaging. We acknowledge the Amon Lab for helpful discussions and advice in setting up basic yeast experiments, specifically C. Brennan and S. Morrill. We also thank N. Eze for insightful discussions and paper editing. This work was supported by the Amar G. Bose Research Grant (G.L.S. and A.M.B.) and the NSF Graduate Fellowship (G.L.S.). Partial support for this research was provided by a core center grant P30-ES002109 from the National Institute of Environmental Health Sciences, National Institutes of Health.
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G.L.S., E.E.R. and A.M.B. conceived the study and designed experiments; G.L.S. performed and E.E.R. helped with experiments; G.L.S. analysed the data and assembled figures; G.L.S., E.E.R. and A.M.B. wrote the manuscript.
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Extended data
Extended Data Fig. 1 Measuring yeast H2S production.
Illustrations left of the images represent H2S detection columns with tick marks indicating the level of sulfide measured in ppm. a, Sulfide detection using 200 pm columns for mutants ΔCYS4, ΔHOM2, ΔMET17, and ΔHM217. b, Sulfide detection using 60 ppm columns for ΔMET17 in cultures of YPD, CSM, and CSM with the addition (+) of methionine (M) or cysteine (C). c, Sulfide detection using 2000 ppm columns for ΔMET17 in CSM cultures lacking (-) methionine or cysteine, or both.
Extended Data Fig. 2 Strain, culture density (OD600), and media composition effects on metal precipitation.
a, Precipitation of copper, zinc, cadmium, lead, and mercury with mutants ΔCYS4, ΔHOM2, ΔMET17, and ΔHM217, and WT as a control, in CSM. b, Effects of removing methionine (M) and/or cysteine (C) from CMS on precipitation efficacy using ΔMET17. Columns represent removal of M while rows represent removal of C from CSM. 1X stands for 100% removal (that is 0.2X = 20% and 0.5X=50%). Annotated values per cell grid represent the percent cadmium removed and standard error. c, Optimal culture density (marked within grey bounds) was determined by titrating cultures of ΔMET17 at different OD600 with copper, zinc, cadmium, lead, and mercury. Metal color coding matches those used in the main text. For all data, the mean ±s.d. of three replicates were taken for each data point.
Extended Data Fig. 3 Elemental mapping of precipitated metal sulfide particles.
a, Elemental mapping of HRTEM images of cadmium sulfide nanoparticles deposited on the cell wall of ΔMET17. Cadmium was false colored as red, sulfide as blue. Scale bars represent 50 nm. b, Elemental dispersive X-ray (EDX) spectroscopy was performed on purified precipitated copper, cadmium, lead, mercury, and zinc sulfide particles under TEM. Elemental Kα peaks were colored and highlighted as areas under the curve for qualitative comparisons. Metal color coding of spectral plots match those used in the main text.
Supplementary information
Supplementary Information
Supplementary Figs. 1–11 and Tables 1 and 3.
Supplementary Table
Supplementary Table 2.
Source data
Source Data Fig. 1
Growth curve and sulfur production values for several strains at various time points
Source Data Fig. 2
Metal removal of Cu, Zn, Cd, Pb, and Hg with respects to media composition in YPD, CSM, CSM-M, and CSM-C
Source Data Fig. 3
Metal concentrations at different rounds of metal removal taken from the Athabasca oil sands
Source Data Fig. 4
Measured sizes of metal sulfide particles examined under TEM
Source Data Fig. 5
Excitation and emission spectra of several purified metal sulfide nanoparticles
Source Data Extended Data Fig. 2
Effects on strain and culture density on metal precipitation efficiency
Source Data Extended Data Fig. 3
Raw EDX signal of purified metal sulfide nanoparticles examined under TEM
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Sun, G.L., Reynolds, E.E. & Belcher, A.M. Using yeast to sustainably remediate and extract heavy metals from waste waters. Nat Sustain 3, 303–311 (2020). https://doi.org/10.1038/s41893-020-0478-9
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DOI: https://doi.org/10.1038/s41893-020-0478-9
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