Desulfobulbus propionicus

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Desulfobulbus propionicus
Scientific classification
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Phylum:
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Genus:
Species:
D. propionicus
Binomial name
Desulfobulbus propionicus
Pagani et al. 2011 [1]
Type strain
1pr3T (DSM 2032, ATCC 33891, VKM B-1956) [1]

Desulfobulbus propionicus is a Gram-negative, anaerobic chemoorganotroph. [1] [2] Three separate strains have been identified: 1pr3T, 2pr4, and 3pr10. [2] It is also the first pure culture example of successful disproportionation of elemental sulfur to sulfate and sulfide. [3] Desulfobulbus propionicus has the potential to produce free energy (in the form of electrons) and chemical products. [4]

Contents

Discovery

Desulfobulbus propionicus was discovered in 1982 by Friedrich Widdel and Norbert Pfenning. [2] Desulfobulbuspropionicus was isolated from samples taken from anaerobic mud in a village ditch, pond, and marine mud flat in Germany. [2] All three strains were isolated using the agar shake dilution method on a basal medium with added sulfate, mineral salts, iron, trace elements, bicarbonate, sulfide, and seven vitamins. [2]

StrainGeographical Location [2] Habitat Type [2]
1pr3TLindhort, GermanyFreshwater ditch mud
2pr4Hannover, GermanyFreshwater pond mud
3pr10Jadebusen, Germany (North Sea)Marine mud flat

Etymology

The genus Desulfobulbus can be derived from the Latin words -de meaning from, -sulfo meaning sulfur, and -bulbus meaning onion shaped literally meaning onion-shaped sulfate reducer. [2] The species name propionicus is derived from the organisms electron donor propionate. [2]

Taxonomic and phylogenetic description

Desulfobulbus propionicus possesses three strains: 1pr3T, 2pr4, and 3pr10. [2] Similarly, all three strains are Gram-negative, sulfur-reducers with the ability to grow exclusively on lactate or pyruvate without any external electron or carbon sources. [2] What separates 1pr3T from its sister strains is its ability to reduce sulfite and thiosulfate to hydrogen sulfide (H2S); reduce nitrate to ammonia; lastly, its presence of cytochrome types b- and c-. [2] Furthermore, strain 1pr3T differentiated from the others in shape (1pr3T possesses pointed ends compared to ovoid or ellipsoidal shaped ends), motility (1pr3T lacks motility, whereas the others possess flagella), and the presence of fimbriae (2pr4 and 3pr10 strains do not). [2]

In terms of the genus Desulfobulbus, the closest relatives of D. propionicus are D. elongatus with an identity of 96.9%, followed by D. rhabdoformis, and then D. mediterraneus and D. japonicas with equal relation respective to the phylogenetic tree constructed using 16S rRNA sequences. [1]

Characterization

Morphology

Desulfobulbus propionicus is a Gram-negative, ellipsoidal to lemon-shaped bacteria, with an average length of 1.0 to 1.3μm and a width of 1.8 to 2.0μm. [1] D. propionicus functions as an anaerobic chemoorganotroph. [1] The three strains differ in shape, motility, and presence of fimbriae. [2]

StrainShapeMotilityFimbriae
1pr3TLemon-shapedNon-motile+
2pr4OvoidSingle polar flagella-
3pr10EllipsoidalSingle polar flagella-

Metabolism

Desulfobulbus propionicus is an anaerobic chemoorganotroph. [1] D. propionicus uses the methylmalony-CoA pathway to ferment 3 moles of pyruvate to 2 moles of acetate and 1 mole of propionate. [1] Desulfobulbuspropionicus utilizes propionate, lactate, pyruvate, and alcohols from the environment as not only electron sources, but for carbon sources as well. [2] Hydrogen gas (H2) is only utilized as an electron donor in the presence of carbon dioxide and acetate. [2] As assumed by its name, Desulfobulbuspropionicus reduces sulfate, sulfite, and thiosulfate to hydrogen sulfide (H2S), but does not reduce elemental sulfur, malate, and fumarate. [2] When sulfate is absent ethanol is fermented to propionate and acetate. [1] In the absence of an electron acceptor, D. propionicus produces sulfate and sulfide from elemental sulfur and water. [3] Also, Desulfobulbus propionicus strains 1pr3T and 3pr10 can only grow in defined minimal media with the addition of a vitamin 4-aminobenzoic acid, whereas strain 2pr4 does not show this additional requirement. [1] [2] Furthermore, the 2pr4 strain is the only of the three to show growth with butyrate as an electron donor and carbon source, however, the growth is slow compared to other substrates. [2]

Genome

Of the three strains within Desulfobulbus propionicus, 1pr3T is the only to have its genome completely sequenced. [1] It was sequenced in 2011 by Pagani et al. [1] Strain 1pr3T was found to encompass a genome size of 3,851,869 bp, with a G-C content of 58.93%. [1] Pagani et al. predicted 3,408 genes in the genome of 1pr3T, with 3,351 genes that encode proteins. [1] The genome contains 57 RNA genes and two rRNA operons. [1] Furthermore, there is 68 pseudo genes which makes up 2.0% of the total genome size. [1]

Ecology

Desulfobulbus propionicus inhabits anaerobic freshwaters and marine sediments. [1] Among the three strains, they differ in: temperature ranges, optimal temperature, pH range, optimal pH, and NaCl concentration requirements (1pr3T and 2pr4 show slowed growth above a NaCl concentration of 15 g/L, and 3pr10 shows no growth below 15 g/L). [1] [2]

StrainTemperate Range (°C) [2] Temperature Optimum (°C) [2] pH Range [2] pH Optimum [2] NaCl Concentration Requirement (g/L) [2]
1pr3T10 - 43396.0 - 8.67.2<15
2pr410 - 36306.6 - 8.17.2<15
3pr1015 - 36296.6 - 8.17.4>15

Application

Desulfobulbus propionicus can serve as a biocatalyst in microbial electrosynthesis. [4] Microbial electrosynthesis is the usage of electrons by microorganism to reduce carbon dioxide to organic molecules. [4] Desulfobulbus propionicus, when present at the anode, oxidizes elemental sulfur to sulfate, which creates free electrons in the process. [4] The free electrons flow to the organism located at the cathode. [4] The microbe present at the cathode utilizes the electron energy transferred from Desulfobulbus propionicus to create organic matter (e.g. acetate) by reducing carbon dioxide. [4] The use of microbial electrosynthesis has potential to aid in the production and waste maintenance of industrial chemicals and energy production. [4]

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References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 Pagani, Ioanna; Lapidus, Alla; Nolan, Matt; Lucas, Susan; Hammon, Nancy; Deshpande, Shweta; Cheng, Jan-Fang; Chertkov, Olga; Davenport, Karen; Tapia, Roxane; Han, Cliff; Goodwin, Lynne; Pitluck, Sam; Liolios, Konstantinos; Mavromatis, Konstantinos; Ivanova, Natalia; Mikhailova, Natalia; Pati, Amrita; Chen, Amy; Palaniappan, Krishna; Land, Miriam; Hauser, Loren; Chang, Yun-Juan; Jeffries, Cynthia D.; Detter, John C.; Brambilla, Evelyne; Kannan, K. Palani; Ngatchou Djao, Olivier D.; Rohde, Manfred; Pukall, Rüdiger; Spring, Stefan; Göker, Markus; Sikorski, Johannes; Woyke, Tanja; Bristow, James; Eisen, Jonathan A.; Markowitz, Victor; Hugenholtz, Philip; Kyrpides, Nikos C.; Klenk, Hans-Peter (2011). "Complete genome sequence of Desulfobulbus propionicus type strain (1pr3T)". Standards in Genomic Sciences. 4 (1): 100–110. doi:10.4056/sigs.1613929. PMC   3072085 . PMID   21475592.
  2. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 Widdel, F.; Pfenning, N. (1982). "Studies on Dissimilatory Sulfate-Reducing Bacteria that Decompose Fatty Acids II. Incomplete Oxidation of Propionate byDesulfobulbuspropionicusgen. nov., sp. nov". Arch Microbiol. 131 (4): 360–365. doi:10.1007/BF00411187. S2CID   52801829.
  3. 1 2 Lovely, Derek R.; Phillips, Elizabeth J. P. (1994). "Novel processes for anae- robic sulfate production from elemental sulfur by sulfate-reducing bacteria". Applied and Environmental Microbiology. 60 (7): 2394–2399. doi:10.1128/AEM.60.7.2394-2399.1994. PMC   201662 . PMID   16349323.
  4. 1 2 3 4 5 6 7 Gong, Yanming; Ebrahim, Ali; Feist, Adam M.; Embree, Mallory; Zhang, Tian; Lovely, Derek; Zengler, Karsten (2013). "Sulfide-Driven Microbial Electrosynthesis". Environmental Science & Technology. 47 (1): 568–573. Bibcode:2013EnST...47..568G. doi:10.1021/es303837j. PMID   23252645.

Further reading