Desulfuromonas acetoxidans

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Classification

FIGURE 1. hylogenetic tree based on 16s rRNA. Modified by adding a red box around desulfuromonas acetoxidans. Source: http://www.sciencedirect.com/science/article/pii/S0964830510001721 P

Higher order taxa

Kingdom: Bacteria

Phylum: Proteobacteria

Class: Deltaproteobacteria

Order: Desulfuromonadales

Family: Desulfuromonadaceae

Genus: Desulfuromonas [7]



Species

NCBI: Taxonomy

Species: Acetoxidans [7]




Description and significance

Desulfuromonas acetoxidans was first described in 1976 by N. Pfennig and H. Biebl [10]. The name has a Latin root, meaning “single-celled organism that reduces sulphur (Desulfuromonas) and oxidizes acetate (acetoxidans)” [6, 10]. It was first described as a sulphur reducing bacteria capable of anaerobically reducing sulphur to sulphide [10]. However, it was later discovered to also possess the ability to perform dissimilatory Fe(III) reduction coupled with the oxidation of organic compounds [11].

Desulfuromonas acetoxidans is a rod-shaped, Gram negative bacterium that is predominantly found in marine sediments [10], though able to survive in fresh water environments [13]. The species is a strict anaerobe that uses a variety of electron donors, such as acetate, ethanol, propanol and butanol, to yield energy [10].

Desulfuromonas acetoxidans is part of the Desulfuromonas genus, which has a characteristic of being able to reduce sulphur through the conversion of elemental sulphur into sulphide [10]. D. acetoxidans is the first species described within the Desulfuromonas genus, and it is also the first marine microorganism ever described to support growth through Fe(III) or Mn(IV) reduction coupled to the oxidation of organic compounds [11].

As the first marine organism ever described to perform the oxidation of organic material coupled with reduction of Fe(III) or Mn(IV), D. acetoxidans has served as a model organism for the mechanism of Fe(III) or Mn(IV) oxidation of organic compounds [11].


Genome structure

The genome sequence of D. acetoxidans was completed in 2007 with funding from the United states Department of Energy Joint Genome Institute [5]. The sequence is available online [7], though a formal description of the genome sequence has not been published in a peer-reviewed scientific journal. Its genome is 3.8Mb in length, and codes for 3234 putative genes [7]. A recent study has shown that the genome contains a very large number of genes coding for c-type cytochromes with multiple heme cofactors [1]. Studies have found that the genome of D. acetoxidans codes for 47 possible multiheme cytochrome proteins [3]. A heme cofactor is a prosthetic group found on proteins that have diverse function [5]. In the case of c-type cytochrome, the heme cofactors function as both electron acceptors and electron donors [5]. The large percentage of genes coding for c-type cytochromes have been found to correlate with the ability of D. acetoxidans to reduce Fe(III) through the dissimilatory pathway [2]. In a study done by Aubert et al. (date, i.e. 2007), the genes that coded for the c-type cytochromes were inserted into the genome of the closely related Desulfovibrio desulfuricans, which is unable to reduce metals [3]. The transformed D. desulfuricans produced the c-type cytochromes and exhibited metal reductase activities [3]. This shows that the c-type cytochrome is vital in the reduction of Fe(III) or Mn(IV) in D. acetoxidans. The mechanistic details concerning how these multiheme cytochromes work are still being studied, but C7 cytochrome is proposed to possess metal reductase activity [2].


Cell structure, metabolism and life cycle

FIGURE 2: Electron Microscopy of Desulfuromonas acetoxidans that clearly shows the flagellum at the lateral side of cell body. Source: http://garciajeanlouis9051.perso.neuf.fr/aaBXIII4_O4_5.html
FIGURE 3. A figure visualizing the differences between Gram positive and Gram negative cell walls. Source: http://water.me.vccs.edu/courses/env108/Lesson5_print.htm


D.acetoxidans has the following characteristics: i) dimensions of 0.4 - 0.7μm in width and 1 - 4μm in length, ii) a single flagellum on the lateral side of the rod-shaped bacteria and even though it possesses a flagellum, most strains were not motile (figure 2.) [10]. Its cell envelope resembles those of other gram negative bacteria, with an outer membrane separated from the cytoplasmic membrane by a thin layer of peptidoglycan (figure 3.) [10]. D. acetoxidans have been found to be non-sporulating, free living bacterium that divides via binary fission [10].


D. acetoxidans possesses a complex metabolism, and energy for metabolism comes from a variety of redox reactions. They are chemoorganotrophs that respire anaerobically, using acetate, ethanol or propanol as carbon sources and electron donors in the presence of ~0.2mM bicarbonate [10]. These organic carbon sources are completely oxidized to CO2 [6, 10]. When D. acetoxidans is reducing sulphuric compounds, either elemental sulphur or disulfide bonds within compounds such as malate or fumarate serve as electron acceptors and are reduced to H2S and sulfhydryl-groups, respectively[10].


D. acetoxidans, when present in different media, has different cytochromes that are present as the dominant type, but there is one type (C7 cytochrome) that is always present, suggesting that this cytochrome plays a key role in metabolism [2]. Studies have also shown that cytochrome C7 plays a role as an electron-transfer protein in the sulphur reduction, as well as in reduction of Fe(III) and Mn(IV) [2].




Ecology

FIGURE 4: Original figure: Schematic diagram showing the mutualism between Green sulfur bacteria and Desulfuromonas acetoxidans.


Desulfuromonas acetoxidans is found primarily in anoxic marine sediment, and rarely found in freshwater sediments [13]. It is able to grow in a pH-range of 6.5 to 8.5, but its optimum pH between 7.2 and 7.5 [10]. D. acetoxidans has an optimum growth temperature of ~30。C, but it can grow in temperature ranging from 25。C to 35。C [10]. In some environments, D. acetoxidans grows syntrophically with green sulphur bacteria [4, 8]. Their relationship is mutualistic in that the green sulphur bacteria presents dissolved and readily metabolizable form of sulphur which is used by D. acetoxidans (refer to figure). The sulphur is oxidized by D. acetoxidans to sulphur, which the green sulphur bacteria can use, this is shown schematically by Figure 4 [4, 12].


The species has biogeochemical significance as it plays a role in the carbon and sulphur cycles [8]. In carbon contaminant-filled sediments, the environment usually quickly becomes anaerobic. As the environment becomes increasingly anoxic, Fe(III) becomes the most abundant and favourable electron acceptor for organic matter oxidation [8]. D. acetoxidans’ ability to perform dissimilatory Fe(III) reduction can be coupled with the oxidation of organic contaminants, effectively removing them from the environment [8]. Recent studies are focused on the dissimilatory Fe(III) reduction aspect of D. acetoxidans rather than the sulphur reduction, since Fe(III) reduction signifies the production of electricity through the degradation of organic materials. This has been applied to the creation of microbial fuel cells, providing enough electricity to power basic electronic equipments [9].



References

[1] Alves, A. S., Paquete, C. M., Fonseca, B. M., and Louro, R. O. “Exploration of the ‘cytochrome’ of Desulfuromonas acetoxidans, a Marine Bacterium Capable of Powering Microbial Fuel Cells.” Metallomics, 2011, 3. p. 349–353. DOI: 10.1039/c0mt00084a

[2] Assfalg, M., Bertini, I., Bruschi, M., Michel, C., and Turano, P. “The Metal Reductase Activity of Some Multiheme Cytochromes c: NMR Structural Characterization of the Reduction of Chromium(VI) to Chromium(III) by Cytochrome C7.” PNAS. 2002, DOI:10.1073.

[3] Aubert, C., Lojou, E., Bianco, P., Rousset, M., Durand, M., Bruschi, M., and Dolla, A. “The Desulfuromonas acetoxidans Triheme Cytochrome C7 Produced in Desulfovibrio desulfuricans Retains Its Metal Reductase Activity.” Appl. Environ. Microbiol. 1998, 64(4):1308.

[4] Biebl. H., Pfennig, N. “Growth Yields of Green Sulfur Bacteria in Mixed Cultures with Sulfur and Sulfate Reducing Bacteria.” Arch. Microbiol. 1978. 117, p. 9 -16.

[5] Dumont, M. E., Cardillo, T. S., Hayes, M. K. and Sherman, F. “Role of cytochrome c heme lyase in mitochondrial import and accumulation of cytochrome c in Saccharomyces cerevisiae.” Mol Cell Biol. 1991 November; 11(11): 5487–5496. PMCID: PMC361918.

[6] Gebhard , N. A., Thauer, R. K., Linder, D., Kaulfers, P., Pfennig, N. “Mechanism of acetate oxidation to CO2 with elemental sulfur in Desulfuromonas acetoxidans.” Arch Microbiol (1985) 141:392-98.

[7] Gillespie, J. J., Wattam, A. R., Cammer, S. A., Gabbard, J., Shukla, M. P., Dalay, O., Driscoll, T., Hix, D., Mane, S. P., Mao, C., Nordberg, E. K., Scott, M., Schulman, J. R., Snyder, E. E., Sullivan, D. E. Wang, C., Warren, A., Williams, K. P., Xue, T., Yoo, H. S., Zhang, C., Zhang, Y., Will, R., Kenyon, R.W. and Sobral B. W. (2011). “PATRIC: The Comprehensive Bacterial Bioinformatics Resource with a Focus on Human Pathogenic Species” Infect. Immun 79 (11): 4286-98. doi:10.1128/IAI.00207-11. PMID21896772.PMC3257917.

[8] Lovley, D. R. “ Dissimilatory Metal Reduction: from Early Life to Bioremediation.” ASM News. 2002, 68(5). p. 231-37

[9] Lovley, D. R. “Microbial Energizers: Fuel Cells That Keep on Going.” Microbe. 2006, 1(6). p. 323-29.

[10] Pfennig, N., and Biebl, H.. “Desulfuromonas acetoxidans gen. nov. and sp. nov., a new anaerobic, sulfur-reducing, acetate-oxidizing bacterium.” Arch. Microbiol0., 1976, 110:3-12

[11] Roden, E. R., Lovley, D. R. “Dissimilatory Fe(III) Reduction by the Marine Microorganism Desulfuromonas acetoxidans.” Applied and Environmental Microbiology. 1993, 59(3). p. 734-42.

[12] Warthmann, R., Cypionka, H., Pfennig, N. “Photoproduction of H2 from acetate by syntrophic cocultures of green sulfur bacteria and sulfur-reducing bacteria.” Arch Microbiol (1992), 157: 343-48.

[13] Vandieken, V., Mußmann, B., Niemann, H., Jørgensen, B. B. “Desulfuromonas svalbardensis sp. nov. and Desulfuromusa ferrireducens sp. nov., psychrophilic, Fe(III)-reducing bacteria isolated from Arctic sediments, Svalbard.” International Journal of Systematic and Evolutionary Microbiology (2006), 56: 1133–1139 DOI 10.1099.