Desulfovibrio vulgaris: Difference between revisions

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Desulfovibrio species are characterized by contain desulfoviridin. This genus can grow easily on a sulfate-lactate medium in the absence of oxygen as a result of metabolic evolutionary traits that have been since studied and isolated by biotechnicians.  
Desulfovibrio species are characterized by contain desulfoviridin. This genus can grow easily on a sulfate-lactate medium in the absence of oxygen as a result of metabolic evolutionary traits that have been since studied and isolated by biotechnicians.  


Desulfovibrio vulgaris Hildenborough is a model organism for studying the energy metabolism of sulfate-reducing bacteria and for understanding the related economic impacts, including bio-corrosion of metal infrastructure and bioremediation of toxic metal ions. It is also known as the “petroleum pest” since it is known to cause a lot of damage to equipment used for drilling and storing oil. What makes this sulfate-reducing bacteria unique is that it can cause the enzymatic reduction of Cr(VI) into a nontoxic form. Furthermore it makes use of hydrogenase activity and cytochrome c3 as the reductase. What separates this reducer is that it can function in high concentration of toxicity as well as in the presence of nickelous chloride, zinc chloride, magnesium sulfate, vanadyl sulfate, and many more (4).
Desulfovibrio vulgaris Hildenborough is a model organism for studying the energy metabolism of sulfate-reducing bacteria and for understanding the related economic impacts, including bio-corrosion of metal infrastructure and bioremediation of toxic metal ions. It is also known as the “petroleum pest” since it is known to cause a lot of damage to equipment used in drilling for and storing oil. What makes this sulfate-reducing bacteria unique is that it can cause the enzymatic reduction of Cr(VI) into a nontoxic form. Furthermore it makes use of hydrogenase activity and cytochrome c3 as the reductase. What separates this reducer is that it can function in high concentration of toxicity as well as in the presence of nickelous chloride, zinc chloride, magnesium sulfate, vanadyl sulfate, and many more (4).


[[Image:Desulfovibrio.jpg]]
[[Image:Dvulgaris.jpg]]
Image from Virtual Institute for Micobial Stress and Survival (vimss.lbl.gov)


==Genome structure==
==Genome structure==
Describe the size and content of the genome. How many chromosomes?  Circular or linear?  Other interesting features?  What is known about its sequence?
Desulfovibrio vulgaris has a genome that is 3,570,858 base pairs in length. The chromosome has a 64.2% guanine and cytosine concentration. Remarkably, the chromosome has 1,894 similar to known protein coding genes in a predicted 3,395 total coding sequences. These genes code for an intricate network of c-type cytochromes that connect multiple periplasmic hydrogenases and formate dehydrogenases (4). Additionally, the sequencing showed the presence of a phosphotransferase system (PTS) similar to those found in other Gram (-) and Gram (+) bacteria that suggest D. vulgaris may have the potential to use mannose type sugars. However evidence that this bacterium uses sugars has not yet been confirmed even though the presence of most of the necessary proteins has been confirmed. In the strain D. vulgaris Hildenborough many proteins were found that are used in glycolysis. The list below does the protein and the gene it is coded from.
Does it have any plasmids?  Are they important to the organism's lifestyle?
 
 
Glucose phosphate isomerase (pgi)
Phosphofructokinase (pfkA)
Fructose bisphosphate aldolase (fba)
Triose phosphate isomerase (tpiA)
Glyceraldehydes-3-phosphate dehydrogenase (gap-1, gap-2)
3-Phosphoglycerate kinase (pgk)
Phosphoglycerate mutase (gpm ,gpmA)
Enolase (eno)
Pyruvate kinase (pyk)
 
The genome sequencing illustrates the possibility of hydrogenases and cytochromes that remove the hydrogens from metals (3). This is substantiated by the presence of genes coding for 27 methyl-accepting chemotaxis proteins that include proteins DcrA and DcrH that sense gradients of oxic/anoxic interfaces (3).
 
Another component of the genome that is being researched are the genes that code for proteins that reduce oxygen are found on the same chromosome. These genes are superoxide reductase (Sor), rubredoxin (Rub), and rubredoxin:oxygen oxidoreductase (Roo) (9).


==Cell structure and metabolism==
==Cell structure and metabolism==
Describe any interesting features and/or cell structures; how it gains energy; what important molecules it produces.
D. Vulgaris is a Gram (-) bacterium that shares many similar characteristics of other Gram (-) bacteria. It has a cell wall enclosing a unique periplasmic space. This periplasmic space is home to a novel network of cytochrome c heme proteins, membrane bound and unbound hydrogenases that allows for the remarkable adaptive abilities of D. vulgaris. This bacteria has an uncanny ability to reduce the highly soluble and toxic Cr(VI) to the less toxic and less soluble Cr(III). Using H2, Cr(VI) can be reduced with cytochrome c3 as the primary reductase (4).
 
When only inorganic chemicals for growth, energy is derived from oxidative phosphorylation by reducing sulfate to sulfide by oxidizing hydrogen (4). There are different types of hydrogenases but by deleting any of them does diminish the chemolithotrophic growth. The electrons generated were stored in the periplasm in multiheme c3-type cytochromes. There are apparently three additional cytochromes (8). According to recent research suggests that the periplasm acts like a capacitor. The electrons can be used to reduce metal ions. This research suggests that tetraheme cytochromes are also involved with reducing metal ions. Sulfur is the final electron acceptor in the cytoplasm.
 
Another metabolic pathway is the incomplete-oxidation of sulfate that leads to acetic acid as the end product. D. vulgaris does have the ability to ferment pyruvate using oxidoreductases, but the thermodynamics of lactate oxidation to pyruvate costs energy (6). It has been postulated that the way this bacteria generates the energy is through something termed “hydrogen cycling” (10). This is aided by two membrane-bound hydrogenases (12). It is important to note that the D. vulgaris has the enzymes necessary for proper break down of hexose sugars, but it has not been yet verified.
 
One of the most fascinating features of this primarily sulfate reducing bacteria is that it contains an alternate pathway to accept electrons. This bacteria has a periplasmic nitrite reductase with two sub-units containing multiple c¬-type heme binding sites (7). This has led to speculation on the ability of D. vulgaris using oxygen as an electron acceptor. There is genomic evidence of oxidases that could protect the bacteria against oxygenic environments. The periplasmic space as iron superoxide dismutase and plasmid-encoded catalase (12).
 
==Ecology and Biotechnology==
Sulfur-reducing bacteria have been known to corrode oil wells, other drilling equipment, and sewers. D. vulgaris is no different, but its unique ability has the potential to of removing Cr(VI) contamination in water and soil (4). Current research places D. vulgaris above the next candidate for treating contamination, Enterobacter cloacoe. Heavy metals inhibit the E. cloacoe but they do not impede D. vulgaris. This bacterium was tested at 50mM of sulfate and did not have its ability to reduce impeded. This experiment was furthered by testing the effects of other metals at a concentration of 100µM (6). Another advantage is that D. vulgaris does not require a high nutrient medium; in fact it can make do with a fairly simple mineral medium. Using H2 as an electron donor does not leave organic compounds as a by-product of decontamination, this is especially important to those who are responsible for cleaning environmental contaminations (12).
 
A strain of this bacterium called D. vulgaris subsp. vulgaris ATCC 29579 is being tested to remove harmful, damaging deposits on stone monuments (7). This black crust formation is the result of a humid climate, pollution, and an area that does is unexposed to rain. Calcite is converted into gypsum and collectively with the smog and other particles, the black crust is formed (7).
 


==Ecology==
Describe any interactions with other organisms (included eukaryotes), contributions to the environment, effect on environment, etc.


==Pathology==
How does this organism cause disease?  Human, animal, plant hosts?  Virulence factors, as well as patient symptoms.


==Application to Biotechnology==
Does this organism produce any useful compounds or enzymes?  What are they and how are they used?


==Current Research==
==Current Research==


Enter summaries of the most recent research here--at least three required
Researchers have a lot to learn about the D. vulgaris. There is still much to be learned on the PTS system that brings in mannose as well as the purpose of the glycolytic enzymes if there still isn’t evidence that the bacteria breaks down hexose sugars (5). Additionally, there is research being done to find a way to mimic the function of cytochrome c3 to treat Cr(IV) wastes. Researchers are trying to be able to harness the resilience of D. vulgaris to high metal toxicity in order to clear up contaminations thoroughly. They also are designing strains that can tolerate more oxygen rich environments.
 
Additional research is trying to better understand the function of the rubredoxin:oxygen oxidoreductase (Roo) gene (8). It is apparent that this gene does allow for the oxidation of oxygen. However in fully aerobic conditions, this gene and its counterparts were inactivated. Some speculate that the Roo gene may in fact nitric oxide reductase (11). This gene works in concert with other genes in order to keep the wild type alive in environments with a low percent of oxygen. By actually turning off some of the genes, the bacteria become more tolerant to oxygen rich environments (9). This is very important to scientists whom are genetically engineering D. vulgaris to but used to decontaminate or clean in oxygen rich environments.
 
Other research that has more applicable purposes is the continuing research done to create strains of D. vulgaris that can withstand aerobic conditions in order to be used as the primary method of removing black crust (7). While maintaining such monuments, is important to leave only the stone and remove all the small particles in a homogenous manner and that is what the current research is stressing.


==References==
==References==
[Sample reference] [http://ijs.sgmjournals.org/cgi/reprint/50/2/489 Takai, K., Sugai, A., Itoh, T., and Horikoshi, K. "''Palaeococcus ferrophilus'' gen. nov., sp. nov., a barophilic, hyperthermophilic archaeon from a deep-sea hydrothermal vent chimney". ''International Journal of Systematic and Evolutionary Microbiology''. 2000. Volume 50. p. 489-500.]
 
1. "Bacteria Genomes - DESULFOVIBRIO VULGARIS." EMBL-EBI. European Bioinformatics Institute. 27 Aug 2007 <http://www.ebi.ac.uk/2can/genomes/bacteria/Desulfovibrio_vulgaris.html>.
 
 
2. Heidelberg, John, Rekha Seshadri, Shelley, and Haveman. "the genome sequence of the Anaerobic, Sulfate-reducing Bacterium Desulfovibrio vulgaris Hildenborough." Nature Biotechnology . 22(2004): 554-559.
 
 
3. Postgate , AuthorR, & Campbell, Leon (1966 ). Classification of DesulJovibrio Species, the . BACTERIOLOGICAL REVIEWS. 30, 23-27.
 
 
4. Lovley, Derek, and Elizabeth Phillips. "Reduction of Chromate by Desulfovibrio vulgaris and its c3 Cytochrome." Applied and Environmental Microbiology 60(1994): 726-728.
 
 
5. Santana, Margarida and Martine Crasnier-Mednansky. "The Adaptive Genome of Desulfovibrio vulgaris Hildenborough." FEMS Microbiology Letter 27 APR 2006 127-133. 26 AUG 2007
 
 
6. Hemme, Christopher, and Judy Wall. "Genomic Insights into Gene Regulation of Desulfovibrio vulgaris Hildenborough." OMICS A Journal of Integrative Biology 8(2004): 43-55.
 
 
7. Francesca, Cappitelli, Lucia Toniolo, Antonio Sansonetti, and Davide Gulotta. "Advantages of Using Microbial Technology over Traditional Chemical Technology in Removal of Black Crusts from Stone Surfaces of Historical Monuments." Applied and Environmental Microbiology, September 2007. 73(2007): 5671-5675.
 
 
8. deMaré, Frank, Donald M. Kurtz Jr, and Pär Nordlund. "The structure of Desulfovibrio vulgaris rubrerythrin reveals a unique combination of rubredoxin-like FeS4 and ferritin-like diiron domains." Nature Structural Biology 3(1996): 539 - 546.
 
 
9. Lumppio, Heather, Neeta V. Shenvi, and Anne O. Summers. "Rubrerythrin and Rubredoxin Oxidoreductase in Desulfovibrio vulgaris: a Novel Oxidative Stress Protection System." Journal of Bacteriology 183(2001): 101-108.
 
 
10. Bender, Kelly, Huei-Che Bill Yen, Christopher L. Hemme, and Zamin Yang. "Analysis of a Ferric Uptake Regulator (Fur) Mutant of Desulfovibrio vulgaris Hildenborough." Applied and Environmental Microbiology, September 2007. 73(2007): 5389-5400.
 
 
 
11. Wildschut, Janine, R. Michael Lang, and Johanna K. Voordouw. "Rubredoxin:Oxygen Oxidoreductase Enhances Survival of Desulfovibrio vulgaris Hildenborough under Microaerophilic Conditions." Journal of Bacteriology 188(2006): 6253-6260.
 
 
12. Caffrey, Sean, Hyung-Soo Park, Johanna K. Voordouw, and Zhili He. "Function of Periplasmic Hydrogenases in the Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough." Journal of Bacteriology. 189(2007): 6159-6167.
 
 
 
 


Edited by student of [mailto:ralarsen@ucsd.edu Rachel Larsen]
Edited by student of [mailto:ralarsen@ucsd.edu Rachel Larsen]

Latest revision as of 03:17, 20 August 2010

This student page has not been curated.

A Microbial Biorealm page on the genus Desulfovibrio vulgaris

Classification

Higher order taxa

Cellular organism: Bacteria (Domain): Proteobacteria(Phylum): delta/epsilon subdivisions (Sub-phylum): Deltaproteobacteria (Class): Desulfovibrionales (Order): Desulfovibrionaceae (Family) [Others may be used. Use NCBI link to find]

Species

NCBI: Taxonomy

Desulfovibrio (Genus): Desulfovibrio vulgaris (Species)

Description and significance

Desulfovibrio vulgaris is a Gram-negative , anaerobic, non-spore forming, curved rod-shaped bacteria, that can be found in soil, animal intestines and feces, and fresh and salt water. (1) It is able to thrive in many of these environments as a result of cellular modifications as well as metabolic enhancements that has allowed this species to live in terrestrial and aquatic habitats. Sulfur-reducing bacteria (SRB), such as D. vulgaris are generally found in anoxic sub-surfaces like areas formed from microbial decomposition as well as sediments and bottom waters. (5). D. vulgaris Hildenborough was discovered in clay soil near Hildenborough, Kent, United Kingdom in forests and grazing fields. Many of the bacteria found in the rhizosphere where roots from plants releasing organic material (6).

The strain many researchers use come from Hildenborough, UK that was first isolated in 1946 from clay. The carbon sources it can use are acetate, pyruvate, formate, and certain primary alcohols (2,3). Desulfovibrio oxidize their energy sources to acetate, excreting this as their end product.

Desulfovibrio species are characterized by contain desulfoviridin. This genus can grow easily on a sulfate-lactate medium in the absence of oxygen as a result of metabolic evolutionary traits that have been since studied and isolated by biotechnicians.

Desulfovibrio vulgaris Hildenborough is a model organism for studying the energy metabolism of sulfate-reducing bacteria and for understanding the related economic impacts, including bio-corrosion of metal infrastructure and bioremediation of toxic metal ions. It is also known as the “petroleum pest” since it is known to cause a lot of damage to equipment used in drilling for and storing oil. What makes this sulfate-reducing bacteria unique is that it can cause the enzymatic reduction of Cr(VI) into a nontoxic form. Furthermore it makes use of hydrogenase activity and cytochrome c3 as the reductase. What separates this reducer is that it can function in high concentration of toxicity as well as in the presence of nickelous chloride, zinc chloride, magnesium sulfate, vanadyl sulfate, and many more (4).

Dvulgaris.jpg Image from Virtual Institute for Micobial Stress and Survival (vimss.lbl.gov)

Genome structure

Desulfovibrio vulgaris has a genome that is 3,570,858 base pairs in length. The chromosome has a 64.2% guanine and cytosine concentration. Remarkably, the chromosome has 1,894 similar to known protein coding genes in a predicted 3,395 total coding sequences. These genes code for an intricate network of c-type cytochromes that connect multiple periplasmic hydrogenases and formate dehydrogenases (4). Additionally, the sequencing showed the presence of a phosphotransferase system (PTS) similar to those found in other Gram (-) and Gram (+) bacteria that suggest D. vulgaris may have the potential to use mannose type sugars. However evidence that this bacterium uses sugars has not yet been confirmed even though the presence of most of the necessary proteins has been confirmed. In the strain D. vulgaris Hildenborough many proteins were found that are used in glycolysis. The list below does the protein and the gene it is coded from.


Glucose phosphate isomerase (pgi) Phosphofructokinase (pfkA) Fructose bisphosphate aldolase (fba) Triose phosphate isomerase (tpiA) Glyceraldehydes-3-phosphate dehydrogenase (gap-1, gap-2) 3-Phosphoglycerate kinase (pgk) Phosphoglycerate mutase (gpm ,gpmA) Enolase (eno) Pyruvate kinase (pyk)

The genome sequencing illustrates the possibility of hydrogenases and cytochromes that remove the hydrogens from metals (3). This is substantiated by the presence of genes coding for 27 methyl-accepting chemotaxis proteins that include proteins DcrA and DcrH that sense gradients of oxic/anoxic interfaces (3).

Another component of the genome that is being researched are the genes that code for proteins that reduce oxygen are found on the same chromosome. These genes are superoxide reductase (Sor), rubredoxin (Rub), and rubredoxin:oxygen oxidoreductase (Roo) (9).

Cell structure and metabolism

D. Vulgaris is a Gram (-) bacterium that shares many similar characteristics of other Gram (-) bacteria. It has a cell wall enclosing a unique periplasmic space. This periplasmic space is home to a novel network of cytochrome c heme proteins, membrane bound and unbound hydrogenases that allows for the remarkable adaptive abilities of D. vulgaris. This bacteria has an uncanny ability to reduce the highly soluble and toxic Cr(VI) to the less toxic and less soluble Cr(III). Using H2, Cr(VI) can be reduced with cytochrome c3 as the primary reductase (4).

When only inorganic chemicals for growth, energy is derived from oxidative phosphorylation by reducing sulfate to sulfide by oxidizing hydrogen (4). There are different types of hydrogenases but by deleting any of them does diminish the chemolithotrophic growth. The electrons generated were stored in the periplasm in multiheme c3-type cytochromes. There are apparently three additional cytochromes (8). According to recent research suggests that the periplasm acts like a capacitor. The electrons can be used to reduce metal ions. This research suggests that tetraheme cytochromes are also involved with reducing metal ions. Sulfur is the final electron acceptor in the cytoplasm.

Another metabolic pathway is the incomplete-oxidation of sulfate that leads to acetic acid as the end product. D. vulgaris does have the ability to ferment pyruvate using oxidoreductases, but the thermodynamics of lactate oxidation to pyruvate costs energy (6). It has been postulated that the way this bacteria generates the energy is through something termed “hydrogen cycling” (10). This is aided by two membrane-bound hydrogenases (12). It is important to note that the D. vulgaris has the enzymes necessary for proper break down of hexose sugars, but it has not been yet verified.

One of the most fascinating features of this primarily sulfate reducing bacteria is that it contains an alternate pathway to accept electrons. This bacteria has a periplasmic nitrite reductase with two sub-units containing multiple c¬-type heme binding sites (7). This has led to speculation on the ability of D. vulgaris using oxygen as an electron acceptor. There is genomic evidence of oxidases that could protect the bacteria against oxygenic environments. The periplasmic space as iron superoxide dismutase and plasmid-encoded catalase (12).

Ecology and Biotechnology

Sulfur-reducing bacteria have been known to corrode oil wells, other drilling equipment, and sewers. D. vulgaris is no different, but its unique ability has the potential to of removing Cr(VI) contamination in water and soil (4). Current research places D. vulgaris above the next candidate for treating contamination, Enterobacter cloacoe. Heavy metals inhibit the E. cloacoe but they do not impede D. vulgaris. This bacterium was tested at 50mM of sulfate and did not have its ability to reduce impeded. This experiment was furthered by testing the effects of other metals at a concentration of 100µM (6). Another advantage is that D. vulgaris does not require a high nutrient medium; in fact it can make do with a fairly simple mineral medium. Using H2 as an electron donor does not leave organic compounds as a by-product of decontamination, this is especially important to those who are responsible for cleaning environmental contaminations (12).

A strain of this bacterium called D. vulgaris subsp. vulgaris ATCC 29579 is being tested to remove harmful, damaging deposits on stone monuments (7). This black crust formation is the result of a humid climate, pollution, and an area that does is unexposed to rain. Calcite is converted into gypsum and collectively with the smog and other particles, the black crust is formed (7).



Current Research

Researchers have a lot to learn about the D. vulgaris. There is still much to be learned on the PTS system that brings in mannose as well as the purpose of the glycolytic enzymes if there still isn’t evidence that the bacteria breaks down hexose sugars (5). Additionally, there is research being done to find a way to mimic the function of cytochrome c3 to treat Cr(IV) wastes. Researchers are trying to be able to harness the resilience of D. vulgaris to high metal toxicity in order to clear up contaminations thoroughly. They also are designing strains that can tolerate more oxygen rich environments.

Additional research is trying to better understand the function of the rubredoxin:oxygen oxidoreductase (Roo) gene (8). It is apparent that this gene does allow for the oxidation of oxygen. However in fully aerobic conditions, this gene and its counterparts were inactivated. Some speculate that the Roo gene may in fact nitric oxide reductase (11). This gene works in concert with other genes in order to keep the wild type alive in environments with a low percent of oxygen. By actually turning off some of the genes, the bacteria become more tolerant to oxygen rich environments (9). This is very important to scientists whom are genetically engineering D. vulgaris to but used to decontaminate or clean in oxygen rich environments.

Other research that has more applicable purposes is the continuing research done to create strains of D. vulgaris that can withstand aerobic conditions in order to be used as the primary method of removing black crust (7). While maintaining such monuments, is important to leave only the stone and remove all the small particles in a homogenous manner and that is what the current research is stressing.

References

1. "Bacteria Genomes - DESULFOVIBRIO VULGARIS." EMBL-EBI. European Bioinformatics Institute. 27 Aug 2007 <http://www.ebi.ac.uk/2can/genomes/bacteria/Desulfovibrio_vulgaris.html>.


2. Heidelberg, John, Rekha Seshadri, Shelley, and Haveman. "the genome sequence of the Anaerobic, Sulfate-reducing Bacterium Desulfovibrio vulgaris Hildenborough." Nature Biotechnology . 22(2004): 554-559.


3. Postgate , AuthorR, & Campbell, Leon (1966 ). Classification of DesulJovibrio Species, the . BACTERIOLOGICAL REVIEWS. 30, 23-27.


4. Lovley, Derek, and Elizabeth Phillips. "Reduction of Chromate by Desulfovibrio vulgaris and its c3 Cytochrome." Applied and Environmental Microbiology 60(1994): 726-728.


5. Santana, Margarida and Martine Crasnier-Mednansky. "The Adaptive Genome of Desulfovibrio vulgaris Hildenborough." FEMS Microbiology Letter 27 APR 2006 127-133. 26 AUG 2007


6. Hemme, Christopher, and Judy Wall. "Genomic Insights into Gene Regulation of Desulfovibrio vulgaris Hildenborough." OMICS A Journal of Integrative Biology 8(2004): 43-55.


7. Francesca, Cappitelli, Lucia Toniolo, Antonio Sansonetti, and Davide Gulotta. "Advantages of Using Microbial Technology over Traditional Chemical Technology in Removal of Black Crusts from Stone Surfaces of Historical Monuments." Applied and Environmental Microbiology, September 2007. 73(2007): 5671-5675.


8. deMaré, Frank, Donald M. Kurtz Jr, and Pär Nordlund. "The structure of Desulfovibrio vulgaris rubrerythrin reveals a unique combination of rubredoxin-like FeS4 and ferritin-like diiron domains." Nature Structural Biology 3(1996): 539 - 546.


9. Lumppio, Heather, Neeta V. Shenvi, and Anne O. Summers. "Rubrerythrin and Rubredoxin Oxidoreductase in Desulfovibrio vulgaris: a Novel Oxidative Stress Protection System." Journal of Bacteriology 183(2001): 101-108.


10. Bender, Kelly, Huei-Che Bill Yen, Christopher L. Hemme, and Zamin Yang. "Analysis of a Ferric Uptake Regulator (Fur) Mutant of Desulfovibrio vulgaris Hildenborough." Applied and Environmental Microbiology, September 2007. 73(2007): 5389-5400.


11. Wildschut, Janine, R. Michael Lang, and Johanna K. Voordouw. "Rubredoxin:Oxygen Oxidoreductase Enhances Survival of Desulfovibrio vulgaris Hildenborough under Microaerophilic Conditions." Journal of Bacteriology 188(2006): 6253-6260.


12. Caffrey, Sean, Hyung-Soo Park, Johanna K. Voordouw, and Zhili He. "Function of Periplasmic Hydrogenases in the Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough." Journal of Bacteriology. 189(2007): 6159-6167.



Edited by student of Rachel Larsen