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Title: Mechanisms of Hg(II) uptake and methylation in methylating bacteria

Abstract

The goal of this project was to understand the critical factors which control the availability and transport of Hg(II) into cells, a first step in the production of the neurotoxin, methylmercury. Specifically, this research focused on understanding the mechanism of bacterial mercury uptake and how mercury speciation affects the specificity and kinetics of mercury transport. Our research has shown that Hg(II) uptake in three different iron and sulfate-reducing proteobacteria occurs by the following mechanism (1) : Hg(II) uptake is an active transport process requiring energy, (2) it is dependent upon the structure of the Hg binding ligand, and (3) it is mediated by a heavy metal transporter such as one which transports the essential metal, Zn(II). In order to determine whether this mechanism extends to more diverse phylogenetic groups, we have begun examining Hg(II) uptake and bioavailability in two representative Hg methylating strains within the Firmicutes. These organisms have remarkably different membrane structures distinct from the Proteobacteria. Our results show low uptake rates in these two species of Firmicutes relative to the previously characterized Proteobacteria. This may explain the low methylation rates and yields observed in these organisms. Most surprisingly, however, these organisms appear to take up Hg(II) passively, asmore » the addition of a protonophore failed to reduce Hg(II) uptake in these organisms. This is quite different to what has been observed previously for the Proteobacteria and suggests a different mechanism for Hg(II) uptake in the Firmicutes. We are continuing to understand and describe Hg(II) uptake in these organisms. A manuscript is expected to be submitted on this research in June 2016.« less

Authors:
 [1]
  1. Princeton Univ., NJ (United States). Geosciences Dept.
Publication Date:
Research Org.:
Princeton Univ., NJ (United States)
Sponsoring Org.:
USDOE Savannah River Operations Office (SRO)
OSTI Identifier:
1328868
Report Number(s):
DOE-Princeton-06849
DOE Contract Number:
SC0006849
Resource Type:
Technical Report
Resource Relation:
Related Information: Manuscripts Published: Szczuka, F. M. M. Morel, and J. K. Schaefer. 2015. The effect of thiols, zinc, and redox conditions on Hg uptake in Shewanella oneidensis. Environ. Sci. Technol. 49: 7432-7438.J. K. Schaefer, A. Szczuka, and F. M. M. Morel. 2014. Effect of divalent metals on Hg(II) uptake and methylation by bacteria. Environ. Sci. Technol. 48: 3007-3013.J. K. Schaefer, R.-M. Kronberg, F. M. M. Morel, U. Skyllberg. 2014. Detection of a key Hg methylation gene, hgcA, in wetland soil. Environ. Microbiol. Rep. 6: 441-447.J. K. Schaefer, S. S. Rocks, W. Zheng, L. Liang, B. Gu, and F. M. M. Morel. 2011. Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria. Proc. Nat. Acad. Sci. 108: 8714-8719.Manuscripts In Preparation:S. Janssen and J. K. Schaefer. Mercury uptake and methylation in firmicutes. Submission planned to ES&T Lett.
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 12 MANAGEMENT OF RADIOACTIVE AND NON-RADIOACTIVE WASTES FROM NUCLEAR FACILITIES; Mercury; methylmercury; bioaccumulation

Citation Formats

Morel, Francois M. M. Mechanisms of Hg(II) uptake and methylation in methylating bacteria. United States: N. p., 2016. Web.
Morel, Francois M. M. Mechanisms of Hg(II) uptake and methylation in methylating bacteria. United States.
Morel, Francois M. M. Fri . "Mechanisms of Hg(II) uptake and methylation in methylating bacteria". United States. doi:. https://www.osti.gov/servlets/purl/1328868.
@article{osti_1328868,
title = {Mechanisms of Hg(II) uptake and methylation in methylating bacteria},
author = {Morel, Francois M. M.},
abstractNote = {The goal of this project was to understand the critical factors which control the availability and transport of Hg(II) into cells, a first step in the production of the neurotoxin, methylmercury. Specifically, this research focused on understanding the mechanism of bacterial mercury uptake and how mercury speciation affects the specificity and kinetics of mercury transport. Our research has shown that Hg(II) uptake in three different iron and sulfate-reducing proteobacteria occurs by the following mechanism (1) : Hg(II) uptake is an active transport process requiring energy, (2) it is dependent upon the structure of the Hg binding ligand, and (3) it is mediated by a heavy metal transporter such as one which transports the essential metal, Zn(II). In order to determine whether this mechanism extends to more diverse phylogenetic groups, we have begun examining Hg(II) uptake and bioavailability in two representative Hg methylating strains within the Firmicutes. These organisms have remarkably different membrane structures distinct from the Proteobacteria. Our results show low uptake rates in these two species of Firmicutes relative to the previously characterized Proteobacteria. This may explain the low methylation rates and yields observed in these organisms. Most surprisingly, however, these organisms appear to take up Hg(II) passively, as the addition of a protonophore failed to reduce Hg(II) uptake in these organisms. This is quite different to what has been observed previously for the Proteobacteria and suggests a different mechanism for Hg(II) uptake in the Firmicutes. We are continuing to understand and describe Hg(II) uptake in these organisms. A manuscript is expected to be submitted on this research in June 2016.},
doi = {},
journal = {},
number = ,
volume = ,
place = {United States},
year = {Fri Oct 14 00:00:00 EDT 2016},
month = {Fri Oct 14 00:00:00 EDT 2016}
}

Technical Report:

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  • Cited by 23
  • The formation of methylmercury (MeHg), which is biomagnified in aquatic food chains and poses a risk to human health, is effected by some iron- and sulfate-reducing bacteria (FeRB and SRB) in anaerobic environments. However, very little is known regarding the mechanism of uptake of inorganic Hg by these organisms, in part because of the inherent difficulty in measuring the intracellular Hg concentration. By using the FeRB Geobacter sulfurreducens and the SRB Desulfovibrio desulfuricans ND132 as model organisms, we demonstrate that Hg(II) uptake occurs by active transport. We also establish that Hg(II) uptake by G. sulfurreducens is highly dependent on themore » characteristics of the thiols that bind Hg(II) in the external medium, with some thiols promoting uptake and methylation and others inhibiting both. The Hg(II) uptake system of D. desulfuricans has a higher affinity than that of G. sulfurreducens and promotes Hg methylation in the presence of stronger complexing thiols. We observed a tight coupling between Hg methylation and MeHg export from the cell, suggesting that these two processes may serve to avoid the build up and toxicity of cellular Hg. Our results bring up the question of whether cellular Hg uptake is specific for Hg(II) or accidental, occurring via some essential metal importer. Our data also point at Hg(II) complexation by thiols as an important factor controlling Hg methylation in anaerobic environments.« less
  • Elemental mercury, Hg(0) is a contaminant at many DOE sites, especially at Oak Ridge National Laboratory (ORNL) where the spread of spilled Hg and its effects on microbial populations have been monitored for decades. To explore the microbial interactions with Hg, we have devised a global proteomic approach capable of directly detecting Hg-adducts of proteins. This technique developed in the facultative anaerobe, Escherichia coli, allows us to identify the proteins most vulnerable to acute exposure to organomercurials phenyl- and ethyl-mercury (as surrogates for the highly neurotoxic methyl-Hg) (Polacco, et al, 2011). We have found >300 such proteins in all metabolicmore » functional groups and cellular compartments; most are highly conserved and can serve as markers for acute Hg exposure (Zink, et al. 2016, in preparation). We have also discovered that acute Hg exposure severely disrupts thiol, iron and redox homeostases, and electrolyte balance (LaVoie, et al., 2015) Thus, we proposed to bring these techniques to bear on the central problem of identifying the cellular proteins involved in bacterial uptake and methylation of mercury and its release from the cell.« less
  • The source of carbonate in marine molluscan shell formation was investigated in the immature queen conch, 8trombus gigas, using Na/sup 14/CO/sub 3/ as a source of inorganic carbonate and /sup 14/C-L-alanine, L-serine, and L - glutamic acid as organic sources. The uptake of the labeled compounds, and of / sup 45/Ca as CaCl/sub 2/, was determined as related to the physical activity of the animal. Results indicate that the conch can utilize many substances dissolved in the sea water environment as a source of carbonate and that the site of absorption is not limited to the gut wall. The rolemore » of marine bacterin in biological calcification in the sea was also investigated. Results are reported from studies of surface binding of Ca and Mg by the cell envelope of Pseudomonas piscicida, a bacteria found in shallow water marine sediments. Calcium-45 and / sup 14/C-alanine were used as tracers. It was concluded that at least two mechanisms are directly involved in the uptake of Ca and Mg by P. piscicida from sea water and that as the cells age increased amounts of CaCO/sub 3/ are deposited but MgCO/sub 3/ deposition remains relatively static. (C.H.)« less