The bacterial metallome: composition and stability with specific reference to the anaerobic bacterium Desulfovibrio desulfuricans

Abstract

In bacteria, the intracellular metal content or metallome reflects the metabolic requirements of the cell. When comparing the composition of metals in phytoplankton and bacteria that make up the macronutrients and the trace elements, we have determined that the content of trace elements in both of these microorganisms is markedly similar. The trace metals consisting of transition metals plus zinc are present in a stoichometric molar formula that we have calculated to be as follows: Fe(1)Mn(0.3)Zn(0.26)Cu(0.03)Co(0.03)Mo(0.03). Under conditions of routine cultivation, trace metal homeostasis may be maintained by a series of transporter systems that are energized by the cell. In specific environments where heavy metals are present at toxic levels, some bacteria have developed a detoxification strategy where the metallic ion is reduced outside of the cell. The result of this extracellular metabolism is that the bacterial metallome specific for trace metals is not disrupted. One of the microorganisms that reduces toxic metals outside of the cell is the sulfate-reducing bacterium Desulfovibrio desulfuricans. While D. desulfuricans reduces metals by enzymatic processes involving polyhemic cytochromes c3 and hydrogenases, which are all present inside the cell; we report the presence of chain B cytochrome c nitrite reductase, NrfA, in the outer membrane fraction of D. desulfuricans ATCC 27774 and discuss its activity as a metal reductase.

The nonconservative property of dissolved molybdenum in the western Taiwan Strait: Relevance of submarine groundwater discharges and biological utilization

“…In particular, phytoplankton and heterotrophs both require Mo as involving in metabolic activities such as nitrate assimilation [e.g., Howarth and Cole , ; Glass et al ., ], and consequently contain high levels of cellular Mo: ∼5.3 µmol/L in phytoplankton cells [ Ho et al ., ] and 53 µmol/L in bacterial cells [ Barton et al ., ] respectively. As the Mo levels in these biological cells are far higher than in seawater (105 nmol/L) [ Collier , ], the high abundances of phytoplankton and bacteria (higher than 10 µg/L) might consume a large quantity of dissolved Mo, and even lead to a net removal of dissolved Mo out of the water column.…”

The nonconservative property of dissolved molybdenum in the western Taiwan Strait: Relevance of submarine groundwater discharges and biological utilization

“…In particular, phytoplankton and heterotrophs both require Mo as involving in metabolic activities such as nitrate assimilation [e.g., Howarth and Cole , ; Glass et al ., ], and consequently contain high levels of cellular Mo: ∼5.3 µmol/L in phytoplankton cells [ Ho et al ., ] and 53 µmol/L in bacterial cells [ Barton et al ., ] respectively. As the Mo levels in these biological cells are far higher than in seawater (105 nmol/L) [ Collier , ], the high abundances of phytoplankton and bacteria (higher than 10 µg/L) might consume a large quantity of dissolved Mo, and even lead to a net removal of dissolved Mo out of the water column.…”

Toward an Internally Consistent Model for Hg(II) Chemical Speciation Calculations in Bacterium–Natural Organic Matter–Low Molecular Mass Thiol Systems

“…Total organic carbon (TOC) content accounted for 51 and 41% of the membrane mass of Geobacter and ND132, respectively, which is in agreement with a previous study. 42 Sulfur K-edge XANES spectra ( Figure S1 and Table S2 ) of whole cell and membrane samples demonstrated a high dominance of Org-S RED , representing the sum of reduced organic S functionalities organic disulfide (RSSR), monosulfide (RSR), and thiol (RSH) that cannot be separated by this methodology. Notably, our membrane samples are expected to include both outer and inner membrane structures.…”

“…Given the limited Hg EXAFS data for this bacterium, our estimate rests on the assumption that the concentration of Mem-R II S tot made up 5% of Mem-RS tot also for ND132 (as determined for Geobacter membranes). If the total S accounts for ∼1% of bacterial cell mass (dry weight), 42 Mem-RS tot will account for 55% of total S and for 62% of Org-S RED (as determined by S K-edge XANES) in membranes of Geobacter ; whereas for ND132 Mem-RS tot accounts for 48% of total S and 72% of Org-S RED .…”

Transcriptome ofGeobacter uraniireducensgrowing in uranium-contaminated subsurface sediments

“…A more plausible function for NrfA and NrfH in G. uraniireducens grown under these conditions is that they are involved in electron transfer to Fe(III) oxides in the sediment. It has been proposed that NrfA is important for dissimilatory metal reduction in two other metalreducing species, Desulfovibrio desulfuricans and Shewanella oneidensis (Barton et al, 2007;Shi et al, 2007).…”

The nonconservative property of dissolved molybdenum in the western Taiwan Strait: Relevance of submarine groundwater discharges and biological utilization

“…In particular, phytoplankton and heterotrophs both require Mo as involving in metabolic activities such as nitrate assimilation [e.g., Howarth and Cole , ; Glass et al ., ], and consequently contain high levels of cellular Mo: ∼5.3 µmol/L in phytoplankton cells [ Ho et al ., ] and 53 µmol/L in bacterial cells [ Barton et al ., ] respectively. As the Mo levels in these biological cells are far higher than in seawater (105 nmol/L) [ Collier , ], the high abundances of phytoplankton and bacteria (higher than 10 µg/L) might consume a large quantity of dissolved Mo, and even lead to a net removal of dissolved Mo out of the water column.…”

Toward an Internally Consistent Model for Hg(II) Chemical Speciation Calculations in Bacterium–Natural Organic Matter–Low Molecular Mass Thiol Systems

“…Total organic carbon (TOC) content accounted for 51 and 41% of the membrane mass of Geobacter and ND132, respectively, which is in agreement with a previous study. 42 Sulfur K-edge XANES spectra ( Figure S1 and Table S2 ) of whole cell and membrane samples demonstrated a high dominance of Org-S RED , representing the sum of reduced organic S functionalities organic disulfide (RSSR), monosulfide (RSR), and thiol (RSH) that cannot be separated by this methodology. Notably, our membrane samples are expected to include both outer and inner membrane structures.…”

“…Given the limited Hg EXAFS data for this bacterium, our estimate rests on the assumption that the concentration of Mem-R II S tot made up 5% of Mem-RS tot also for ND132 (as determined for Geobacter membranes). If the total S accounts for ∼1% of bacterial cell mass (dry weight), 42 Mem-RS tot will account for 55% of total S and for 62% of Org-S RED (as determined by S K-edge XANES) in membranes of Geobacter ; whereas for ND132 Mem-RS tot accounts for 48% of total S and 72% of Org-S RED .…”

Transcriptome ofGeobacter uraniireducensgrowing in uranium-contaminated subsurface sediments

“…A more plausible function for NrfA and NrfH in G. uraniireducens grown under these conditions is that they are involved in electron transfer to Fe(III) oxides in the sediment. It has been proposed that NrfA is important for dissimilatory metal reduction in two other metalreducing species, Desulfovibrio desulfuricans and Shewanella oneidensis (Barton et al, 2007;Shi et al, 2007).…”

The nonconservative property of dissolved molybdenum in the western Taiwan Strait: Relevance of submarine groundwater discharges and biological utilization

“…In particular, phytoplankton and heterotrophs both require Mo as involving in metabolic activities such as nitrate assimilation [e.g., Howarth and Cole , ; Glass et al ., ], and consequently contain high levels of cellular Mo: ∼5.3 µmol/L in phytoplankton cells [ Ho et al ., ] and 53 µmol/L in bacterial cells [ Barton et al ., ] respectively. As the Mo levels in these biological cells are far higher than in seawater (105 nmol/L) [ Collier , ], the high abundances of phytoplankton and bacteria (higher than 10 µg/L) might consume a large quantity of dissolved Mo, and even lead to a net removal of dissolved Mo out of the water column.…”

Toward an Internally Consistent Model for Hg(II) Chemical Speciation Calculations in Bacterium–Natural Organic Matter–Low Molecular Mass Thiol Systems

“…Total organic carbon (TOC) content accounted for 51 and 41% of the membrane mass of Geobacter and ND132, respectively, which is in agreement with a previous study. 42 Sulfur K-edge XANES spectra ( Figure S1 and Table S2 ) of whole cell and membrane samples demonstrated a high dominance of Org-S RED , representing the sum of reduced organic S functionalities organic disulfide (RSSR), monosulfide (RSR), and thiol (RSH) that cannot be separated by this methodology. Notably, our membrane samples are expected to include both outer and inner membrane structures.…”

“…Given the limited Hg EXAFS data for this bacterium, our estimate rests on the assumption that the concentration of Mem-R II S tot made up 5% of Mem-RS tot also for ND132 (as determined for Geobacter membranes). If the total S accounts for ∼1% of bacterial cell mass (dry weight), 42 Mem-RS tot will account for 55% of total S and for 62% of Org-S RED (as determined by S K-edge XANES) in membranes of Geobacter ; whereas for ND132 Mem-RS tot accounts for 48% of total S and 72% of Org-S RED .…”

Transcriptome ofGeobacter uraniireducensgrowing in uranium-contaminated subsurface sediments

“…A more plausible function for NrfA and NrfH in G. uraniireducens grown under these conditions is that they are involved in electron transfer to Fe(III) oxides in the sediment. It has been proposed that NrfA is important for dissimilatory metal reduction in two other metalreducing species, Desulfovibrio desulfuricans and Shewanella oneidensis (Barton et al, 2007;Shi et al, 2007).…”