Thiosulfate oxidation by Thiomicrospira thermophila: Metabolic flexibility in response to ambient geochemistry
Abstract
Previous studies of the stoichiometry of thiosulfate oxidation by colorless sulfur bacteria have failed to demonstrate mass balance of sulfur, indicating that unidentified oxidized products must be present. Here the reaction stoichiometry and kinetics under variable pH conditions during the growth of Thiomicrospira thermophila strain EPR85, isolated from diffuse hydrothermal fluids at the East Pacific Rise, is presented. At pH 8.0, thiosulfate was stoichiometrically converted to sulfate. At lower pH, the products of thiosulfate oxidation were extracellular elemental sulfur and sulfate. Here, we were able to replicate previous experiments and identify the missing sulfur as tetrathionate, consistent with previous reports of the activity of thiosulfate dehydrogenase. Tetrathionate was formed under slightly acidic conditions. Genomic DNA from T. thermophila strain EPR85 contains genes homologous to those in the Sox pathway (soxAXYZBCDL), as well as rhodanese and thiosulfate dehydrogenase. No other sulfur oxidizing bacteria containing sox(CD)2 genes have been reported to produce extracellular elemental sulfur. If the apparent modified Sox pathway we observed in T. thermophila is present in marine Thiobacillus and Thiomicrospira species, production of extracellular elemental sulfur may be biogeochemically important in marine sulfur cycling.
- Authors:
-
- Washington Univ., St. Louis, MO (United States)
- Carnegie Inst. of Washington, Washington, DC (United States)
- Argonne National Lab. (ANL), Lemont, IL (United States); The Univ. of Chicago, Chicago, IL (United States)
- Rutgers Univ., New Brunswick, NJ (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
- OSTI Identifier:
- 1339997
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 18; Journal Issue: 9; Journal ID: ISSN 1462-2912
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES
Citation Formats
Houghton, J. L., Foustoukos, D. I., Flynn, T. M., Vetriani, C., Bradley, Alexander S., and Fike, D. A. Thiosulfate oxidation by Thiomicrospira thermophila: Metabolic flexibility in response to ambient geochemistry. United States: N. p., 2016.
Web. doi:10.1111/1462-2920.13232.
Houghton, J. L., Foustoukos, D. I., Flynn, T. M., Vetriani, C., Bradley, Alexander S., & Fike, D. A. Thiosulfate oxidation by Thiomicrospira thermophila: Metabolic flexibility in response to ambient geochemistry. United States. https://doi.org/10.1111/1462-2920.13232
Houghton, J. L., Foustoukos, D. I., Flynn, T. M., Vetriani, C., Bradley, Alexander S., and Fike, D. A. Mon .
"Thiosulfate oxidation by Thiomicrospira thermophila: Metabolic flexibility in response to ambient geochemistry". United States. https://doi.org/10.1111/1462-2920.13232. https://www.osti.gov/servlets/purl/1339997.
@article{osti_1339997,
title = {Thiosulfate oxidation by Thiomicrospira thermophila: Metabolic flexibility in response to ambient geochemistry},
author = {Houghton, J. L. and Foustoukos, D. I. and Flynn, T. M. and Vetriani, C. and Bradley, Alexander S. and Fike, D. A.},
abstractNote = {Previous studies of the stoichiometry of thiosulfate oxidation by colorless sulfur bacteria have failed to demonstrate mass balance of sulfur, indicating that unidentified oxidized products must be present. Here the reaction stoichiometry and kinetics under variable pH conditions during the growth of Thiomicrospira thermophila strain EPR85, isolated from diffuse hydrothermal fluids at the East Pacific Rise, is presented. At pH 8.0, thiosulfate was stoichiometrically converted to sulfate. At lower pH, the products of thiosulfate oxidation were extracellular elemental sulfur and sulfate. Here, we were able to replicate previous experiments and identify the missing sulfur as tetrathionate, consistent with previous reports of the activity of thiosulfate dehydrogenase. Tetrathionate was formed under slightly acidic conditions. Genomic DNA from T. thermophila strain EPR85 contains genes homologous to those in the Sox pathway (soxAXYZBCDL), as well as rhodanese and thiosulfate dehydrogenase. No other sulfur oxidizing bacteria containing sox(CD)2 genes have been reported to produce extracellular elemental sulfur. If the apparent modified Sox pathway we observed in T. thermophila is present in marine Thiobacillus and Thiomicrospira species, production of extracellular elemental sulfur may be biogeochemically important in marine sulfur cycling.},
doi = {10.1111/1462-2920.13232},
journal = {Environmental Microbiology},
number = 9,
volume = 18,
place = {United States},
year = {Mon Mar 21 00:00:00 EDT 2016},
month = {Mon Mar 21 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
QUAST: quality assessment tool for genome assemblies
journal, February 2013
- Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay
- Bioinformatics, Vol. 29, Issue 8
Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption
journal, April 2003
- Huber, Julie A.; Butterfield, David A.; Baross, John A.
- FEMS Microbiology Ecology, Vol. 43, Issue 3
Properties and Role of Sulphite: Cytochrome c Oxidoreductase Purified from Thiobacillus versutus (A2)
journal, July 1984
- Lu, W. -P.; Kelly, D. P.
- Microbiology, Vol. 130, Issue 7
Oxidation of reduced inorganic sulphur compounds by acidophilic thiobacilli
journal, June 1990
- Pronk, J. T.; Meulenberg, R.; Hazeu, W.
- FEMS Microbiology Letters, Vol. 75, Issue 2-3
Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters
journal, May 1969
- Cline, Joel D.
- Limnology and Oceanography, Vol. 14, Issue 3, p. 454-458
Dissimilatory sulphite reductase from Archaeoglobus fulgidus: physico-chemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes
journal, August 1993
- Dahl, C.; Kredich, N. M.; Deutzmann, R.
- Journal of General Microbiology, Vol. 139, Issue 8
Thiomicrospira thermophila sp. nov., a novel microaerobic, thermotolerant, sulfur-oxidizing chemolithomixotroph isolated from a deep-sea hydrothermal fumarole in the TOTO caldera, Mariana Arc, Western Pacific
journal, November 2004
- Takai, K.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 6
Manganese, iron and sulfur cycling in a coastal marine sediment, Aarhus bay, Denmark
journal, December 1994
- Thamdrup, Bo; Fossing, Henrik; Jørgensen, Bo Barker
- Geochimica et Cosmochimica Acta, Vol. 58, Issue 23
Mechanisms and Evolution of Oxidative Sulfur Metabolism in Green Sulfur Bacteria
journal, January 2011
- Gregersen, Lea H.; Bryant, Donald A.; Frigaard, Niels-Ulrik
- Frontiers in Microbiology, Vol. 2
Identification of 16S Ribosomal DNA-Defined Bacterial Populations at a Shallow Submarine Hydrothermal Vent near Milos Island (Greece)
journal, July 2000
- Sievert, S. M.; Kuever, J.; Muyzer, G.
- Applied and Environmental Microbiology, Vol. 66, Issue 7
Seasonal dynamics of elemental sulfur in two coastal sediments
journal, September 1982
- Troelsen, Henning; Jørgensen, Bo Barker
- Estuarine, Coastal and Shelf Science, Vol. 15, Issue 3
Evidence for two pathways of thiosulfate oxidation in Starkeya novella (formerly Thiobacillus novellus )
journal, March 2001
- Kappler, Ulrike; Friedrich, Cornelius G.; Trüper, Hans G.
- Archives of Microbiology, Vol. 175, Issue 2
Interaction between Sox proteins of two physiologically distinct bacteria and a new protein involved in thiosulfate oxidation
journal, March 2009
- Welte, Cornelia; Hafner, Swetlana; Krätzer, Christian
- FEBS Letters, Vol. 583, Issue 8
Purification and Properties of Thiosulfate Reductase from Desulfovibrio vulgaris, Miyazaki F1
journal, April 1985
- Aketagawa, Jun; Kobayashi, Kunihiko; Ishimoto, Makoto
- The Journal of Biochemistry, Vol. 97, Issue 4
Quantitative measurement of sulphur formation by steady-state and transient-state continuous cultures of autotrophic Thiobacillus species
journal, March 1996
- Stefess, G. C.; Torremans, R. A. M.; de Schrijver, R.
- Applied Microbiology and Biotechnology, Vol. 45, Issue 1-2
Salinisphaera hydrothermalis sp. nov., a mesophilic, halotolerant, facultatively autotrophic, thiosulfate-oxidizing gammaproteobacterium from deep-sea hydrothermal vents, and emended description of the genus Salinisphaera
journal, June 2009
- Crespo-Medina, M.; Chatziefthimiou, A.; Cruz-Matos, R.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 6
The Genera Thiobacillus and Thiomicrospira
book, January 1981
- Kuenen, J. Gijs; Tuovinen, Olli H.
- The Prokaryotes
Active Site Structural Features for Chemically Modified Forms of Rhodanese
journal, August 1996
- Gliubich, Francesca; Gazerro, Marialuisa; Zanotti, Giuseppe
- Journal of Biological Chemistry, Vol. 271, Issue 35
Increased species diversity and extended habitat range of sulfur-oxidizing Thiomicrospira spp.
journal, January 1997
- Brinkhoff, T.; Muyzer, G.
- Applied and environmental microbiology, Vol. 63, Issue 10
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
Metagenomic Comparison of Two Thiomicrospira Lineages Inhabiting Contrasting Deep-Sea Hydrothermal Environments
journal, October 2010
- Brazelton, William J.; Baross, John A.
- PLoS ONE, Vol. 5, Issue 10
A novel membrane-bound flavocytochrome c sulfide dehydrogenase from the colourless sulfur bacterium Thiobacillus sp. W5
journal, April 1997
- Visser, J. M.; de Jong, Govardus A. H.; Robertson, L. A.
- Archives of Microbiology, Vol. 167, Issue 5
Microbial Interactions among Aerobic and Anaerobic Sulfur-Oxidizing Bacteria
book, January 1985
- Kuenen, J. Gijs; Robertson, Lesley A.; Van Gemerden, Hans
- Advances in Microbial Ecology
A Cryptic Sulfur Cycle in Oxygen-Minimum-Zone Waters off the Chilean Coast
journal, November 2010
- Canfield, D. E.; Stewart, F. J.; Thamdrup, B.
- Science, Vol. 330, Issue 6009
Release LTPs104 of the All-Species Living Tree
journal, May 2011
- Munoz, Raúl; Yarza, Pablo; Ludwig, Wolfgang
- Systematic and Applied Microbiology, Vol. 34, Issue 3
Characterization of a new type of sulfite dehydrogenase from Paracoccus pantotrophus GB17
journal, November 1999
- Quentmeier, Armin; Kraft, Regine; Kostka, Susanne
- Archives of Microbiology, Vol. 173, Issue 2
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes
journal, May 2012
- Pruesse, Elmar; Peplies, Jörg; Glöckner, Frank Oliver
- Bioinformatics, Vol. 28, Issue 14
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012
- Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
- Nucleic Acids Research, Vol. 41, Issue D1
Identification and sequence analysis of the soxB gene essential for sulfur oxidation of Paracoccus denitrificans GB17.
journal, October 1994
- Wodara, C.; Kostka, S.; Egert, M.
- Journal of Bacteriology, Vol. 176, Issue 20
ARB: a software environment for sequence data
journal, February 2004
- Ludwig, W.
- Nucleic Acids Research, Vol. 32, Issue 4
A Thiosulfate Shunt in the Sulfur Cycle of Marine Sediments
journal, July 1990
- Jorgensen, B. B.
- Science, Vol. 249, Issue 4965
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012
- Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
- Journal of Computational Biology, Vol. 19, Issue 5
Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur
journal, July 1998
- Pott, A. S.; Dahl, C.
- Microbiology, Vol. 144, Issue 7
Insights into the Genome of Large Sulfur Bacteria Revealed by Analysis of Single Filaments
journal, August 2007
- Mußmann, Marc; Hu, Fen Z.; Richter, Michael
- PLoS Biology, Vol. 5, Issue 9
Properties of the thiosulphate-oxidizing multi-enzyme system from Thiobacillus versutus
journal, April 1985
- Lu, Wei-Ping; Swoboda, B. E. P.; Kelly, D. P.
- Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 828, Issue 2
Cloning and characterization of sulfite dehydrogenase, two c-type cytochromes, and a flavoprotein of Paracoccus denitrificans GB17: essential role of sulfite dehydrogenase in lithotrophic sulfur oxidation.
journal, August 1997
- Wodara, C.; Bardischewsky, F.; Friedrich, C. G.
- Journal of Bacteriology, Vol. 179, Issue 16
Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum
journal, June 1998
- Reinartz, Michael; Tschäpe, Jürgen; Brüser, Thomas
- Archives of Microbiology, Vol. 170, Issue 1
The Genome of Deep-Sea Vent Chemolithoautotroph Thiomicrospira crunogena XCL-2
journal, November 2006
- Scott, Kathleen M.; Sievert, Stefan M.; Abril, Fereniki N.
- PLoS Biology, Vol. 4, Issue 12
Thiosulfate dehydrogenase: a widespread unusual acidophilic c -type cytochrome : Thiosulfate dehydrogenase
journal, July 2012
- Denkmann, Kevin; Grein, Fabian; Zigann, Renate
- Environmental Microbiology, Vol. 14, Issue 10
Thiosulphate Metabolism and Rhodanese in Chromatium sp. strain D
journal, March 1966
- Smith, A. J.; Lascelles, J.
- Journal of General Microbiology, Vol. 42, Issue 3
Mechanism for the Formation of Elemental Sulfur from Aqueous Sulfide in Chemical and Microbiological Desulfurization Processes
journal, January 1996
- Steudel, Ralf
- Industrial & Engineering Chemistry Research, Vol. 35, Issue 4
The All-Species Living Tree project: A 16S rRNA-based phylogenetic tree of all sequenced type strains
journal, September 2008
- Yarza, Pablo; Richter, Michael; Peplies, Jörg
- Systematic and Applied Microbiology, Vol. 31, Issue 4
Bacterial sulfite dehydrogenases in organotrophic metabolism: separation and identification in Cupriavidus necator H16 and in Delftia acidovorans SPH-1
journal, January 2008
- Denger, Karin; Weinitschke, Sonja; Smits, Theo H. M.
- Microbiology, Vol. 154, Issue 1
Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum
journal, September 2006
- Hensen, Daniela; Sperling, Detlef; Trüper, Hans G.
- Molecular Microbiology, Vol. 62, Issue 3
The in situ pH of hydrothermal fluids at mid-ocean ridges
journal, August 2005
- Ding, Kang; Seyfried, William E.; Zhang, Zhong
- Earth and Planetary Science Letters, Vol. 237, Issue 1-2
The genetic basis of tetrathionate respiration in Salmonella typhimurium
journal, April 1999
- Hensel, Michael; Hinsley, Andrew P.; Nikolaus, Thomas
- Molecular Microbiology, Vol. 32, Issue 2
Sulfur-mediated electron shuttling during bacterial iron reduction
journal, May 2014
- Flynn, T. M.; O'Loughlin, E. J.; Mishra, B.
- Science, Vol. 344, Issue 6187
The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium
journal, October 1994
- Chen, Z.; Koh, M.; Van Driessche, G.
- Science, Vol. 266, Issue 5184
Engineering Hydrogen Sulfide Production and Cadmium Removal by Expression of the Thiosulfate Reductase Gene (phsABC) from Salmonella enterica Serovar Typhimurium in Escherichia coli
journal, September 2000
- Bang, Sang-Weon; Clark, Douglas S.; Keasling, Jay D.
- Applied and Environmental Microbiology, Vol. 66, Issue 9
Involvement of Intermediate Sulfur Species in Biological Reduction of Elemental Sulfur under Acidic, Hydrothermal Conditions
journal, January 2013
- Boyd, Eric S.; Druschel, Gregory K.
- Applied and Environmental Microbiology, Vol. 79, Issue 6
The relationship between structure and function for the sulfite reductases
journal, December 1996
- Crane, Brian R.; Getzoff, Elizabeth D.
- Current Opinion in Structural Biology, Vol. 6, Issue 6
Dissolved carbon species in associated diffuse and focused flow hydrothermal vents at the Main Endeavour Field, Juan de Fuca Ridge: Phase equilibria and kinetic constraints: CARBON SPECIES IN MEF VENT FLUIDS
journal, October 2009
- Foustoukos, Dionysis I.; Pester, Nicholas J.; Ding, Kang
- Geochemistry, Geophysics, Geosystems, Vol. 10, Issue 10
Novel Genes Coding for Lithotrophic Sulfur Oxidation of Paracoccus pantotrophus GB17
journal, September 2000
- Friedrich, C. G.; Quentmeier, A.; Bardischewsky, F.
- Journal of Bacteriology, Vol. 182, Issue 17
Oxidation of Reduced Inorganic Sulfur Compounds by Bacteria: Emergence of a Common Mechanism?
journal, July 2001
- Friedrich, C. G.; Rother, D.; Bardischewsky, F.
- Applied and Environmental Microbiology, Vol. 67, Issue 7
pH-Dependent metabolism of thiosulfate and sulfur globules in the chemolithotrophic marine bacterium Thiomicrospira crunogena
journal, August 1990
- Javor, Barbara J.; Wilmot, David B.; Vetter, Russell D.
- Archives of Microbiology, Vol. 154, Issue 3
Pathways and Microbiology of Thiosulfate Transformations and Sulfate Reduction in a Marine Sediment (Kattegat, Denmark) †
journal, January 1991
- Jørgensen, Bo Barker; Bak, Friedhelm
- Applied and Environmental Microbiology, Vol. 57, Issue 3
Microbial Stress-Response Physiology and its Implications for Ecosystem Function
journal, June 2007
- Schimel, Joshua; Balser, Teri C.; Wallenstein, Matthew
- Ecology, Vol. 88, Issue 6
Oxidation of reduced sulphur compounds by intact cells of Thiobacillus acidophilus
journal, January 1992
- Meulenberg, Rogier; Pronk, Jack T.; Hazeu, Wim
- Archives of Microbiology, Vol. 157, Issue 2
Microbial community structure and global trace gases
journal, October 1998
- Schimel, Joshua P.; Gulledge, Jay.
- Global Change Biology, Vol. 4, Issue 7
Rhodanese as a thioredoxin oxidase
journal, April 2000
- Nandi, Dhirendra L.; Horowitz, Paul M.; Westley, John
- The International Journal of Biochemistry & Cell Biology, Vol. 32, Issue 4
The SoxYZ Complex Carries Sulfur Cycle Intermediates on a Peptide Swinging Arm
journal, May 2007
- Sauvé, Véronique; Bruno, Stefano; Berks, Ben C.
- Journal of Biological Chemistry, Vol. 282, Issue 32
The sulfide affinity of phototrophic bacteria in relation to the location of elemental sulfur
journal, November 1984
- Van Gemerden, Hans
- Archives of Microbiology, Vol. 139, Issue 4
Structural Basis for the Oxidation of Protein-bound Sulfur by the Sulfur Cycle Molybdohemo-Enzyme Sulfane Dehydrogenase SoxCD
journal, December 2010
- Zander, Ulrich; Faust, Annette; Klink, Björn U.
- Journal of Biological Chemistry, Vol. 286, Issue 10
Analysis of immune, microbiota and metabolome maturation in infants in a clinical trial of Lactobacillus paracasei CBA L74-fermented formula
journal, June 2020
- Roggero, Paola; Liotto, Nadia; Pozzi, Chiara
- Nature Communications, Vol. 11, Issue 1
Mutations in virus-derived small RNAs
journal, June 2020
- Nigam, Deepti; LaTourrette, Katherine; Garcia-Ruiz, Hernan
- Scientific Reports, Vol. 10, Issue 1
Works referencing / citing this record:
Microbial functional genes elucidate environmental drivers of biofilm metabolism in glacier-fed streams
journal, October 2017
- Ren, Ze; Gao, Hongkai; Elser, James J.
- Scientific Reports, Vol. 7, Issue 1
Thiomicrorhabdus streamers and sulfur cycling in perennial hypersaline cold springs in the Canadian high Arctic
journal, January 2020
- Magnuson, Elisse; Mykytczuk, Nadia C. S.; Pellerin, Andre
- Environmental Microbiology
The effect of O 2 and pressure on thiosulfate oxidation by Thiomicrospira thermophila
journal, June 2019
- Houghton, Jennifer L.; Foustoukos, Dionysis I.; Fike, David A.
- Geobiology, Vol. 17, Issue 5
The influence of Antarctic subglacial volcanism on the global iron cycle during the Last Glacial Maximum
journal, June 2017
- Frisia, Silvia; Weyrich, Laura S.; Hellstrom, John
- Nature Communications, Vol. 8, Issue 1
Microbial functional genes elucidate environmental drivers of biofilm metabolism in glacier-fed streams
journal, October 2017
- Ren, Ze; Gao, Hongkai; Elser, James J.
- Scientific Reports, Vol. 7, Issue 1
Tetrathionate and Elemental Sulfur Shape the Isotope Composition of Sulfate in Acid Mine Drainage
journal, August 2017
- Balci, Nurgul; Brunner, Benjamin; Turchyn, Alexandra V.
- Frontiers in Microbiology, Vol. 8
Sulfur Metabolism of Hydrogenovibrio thermophilus Strain S5 and Its Adaptations to Deep-Sea Hydrothermal Vent Environment
journal, December 2017
- Jiang, Lijing; Lyu, Jie; Shao, Zongze
- Frontiers in Microbiology, Vol. 8