Resistance and Resilience of Sulfidogenic Communities in the Face of the Specific Inhibitor Perchlorate

Stoeva, Magdalena K.; Nalula, Gilbert; Garcia, Nicholas; Cheng, Yiwei; Engelbrektson, Anna L.; Carlson, Hans K.; Coates, John D.

doi:10.3389/fmicb.2019.00654

Title: Resistance and Resilience of Sulfidogenic Communities in the Face of the Specific Inhibitor Perchlorate

Journal Article · 02 April 2019 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2019.00654 · OSTI ID:1560581

Stoeva, Magdalena K. ^[1]; Nalula, Gilbert ^[2]; Garcia, Nicholas ^[2]; Cheng, Yiwei ^[3]; Engelbrektson, Anna L. ^[1]; Carlson, Hans K. ^[4]; Coates, John D. ^[4]

Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; Energy Biosciences Inst., Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; Energy Biosciences Inst., Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Hydrogen sulfide is a toxic and corrosive gas, produced by the activity of sulfate-reducing microorganisms (SRM). Owing to the environmental, economic and human-health consequences of sulfide, there is interest in developing specific inhibitors of SRM. Recent studies have identified perchlorate as a promising emerging inhibitor. The aim of this work is to quantitatively dissect the inhibitory dynamics of perchlorate. Sulfidogenic mixed continuous-flow systems were treated with perchlorate. SRM number, sulfide production and community structure were monitored pre-, during and post-treatment. The data generated was compared to a simple mathematical model, where SRM growth slows as a result of inhibition. The experimental data supports the interpretation that perchlorate largely acts to suppress SRM growth rates, rendering planktonic SRM increasingly susceptible to wash-out. Surface-attachment was identified as an important parameter preventing SRM wash-out and thus governing inhibitory dynamics. Our study confirmed the lesser depletion of surface-attached SRM as compared to planktonic SRM during perchlorate treatment. Indirect effects of perchlorate (bio-competitive exclusion of SRM by dissimilatory perchlorate-reducing bacteria, DPRB) were also assayed by amending reactors with DPRB. Indeed, low concentrations of perchlorate coupled with DRPB amendment can drive sulfide concentrations to zero. Further, inhibition in a complex community was compared to that in a pure culture, highlighting similarities and differences between the two scenarios. Finally, we quantified susceptibility to perchlorate across SRM in various culture conditions, showing that prediction of complex behavior in continuous systems from batch results is possible. This study thus provides an overview of the sensitivity of sulfidogenic communities to perchlorate, as well as mechanisms underlying these patterns.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1560581

Journal Information:: Frontiers in Microbiology, Vol. 10, Issue APR; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 4 works

Citation information provided by
Web of Science

References (80)

Sulfate‐reducing bacteria Hao, Oliver J.; Chen, Jin M.; Huang, Li Critical Reviews in Environmental Science and Technology, Vol. 26, Issue 2 https://doi.org/10.1080/10643389609388489	journal	May 1996
Sulfate‐reducing bacteria Hao, Oliver J.; Chen, Jin M.; Huang, Li Critical Reviews in Environmental Science and Technology, Vol. 26, Issue 2 https://doi.org/10.1080/10643389609388489	journal	May 1996
UCHIME improves sensitivity and speed of chimera detection Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C. Bioinformatics, Vol. 27, Issue 16 https://doi.org/10.1093/bioinformatics/btr381	journal	June 2011
Attenuating Sulfidogenesis in a Soured Continuous Flow Column System With Perchlorate Treatment Engelbrektson, Anna L.; Cheng, Yiwei; Hubbard, Christopher G. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01575	journal	July 2018
Competitive, Microbially-Mediated Reduction of Nitrate with Sulfide and Aromatic Oil Components in a Low-Temperature, Western Canadian Oil Reservoir Lambo, Adewale J.; Noke, Kim; Larter, Steve R. Environmental Science & Technology, Vol. 42, Issue 23 https://doi.org/10.1021/es801832s	journal	December 2008
Competitive, Microbially-Mediated Reduction of Nitrate with Sulfide and Aromatic Oil Components in a Low-Temperature, Western Canadian Oil Reservoir Lambo, Adewale J.; Noke, Kim; Larter, Steve R. Environmental Science & Technology, Vol. 42, Issue 23 https://doi.org/10.1021/es801832s	journal	December 2008
UCHIME improves sensitivity and speed of chimera detection Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C. Bioinformatics, Vol. 27, Issue 16 https://doi.org/10.1093/bioinformatics/btr381	journal	June 2011
Attenuating Sulfidogenesis in a Soured Continuous Flow Column System With Perchlorate Treatment Engelbrektson, Anna L.; Cheng, Yiwei; Hubbard, Christopher G. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01575	journal	July 2018
Reduction of (per)chlorate by a novel organism isolated from paper mill waste Bruce, Royce A.; Achenbach, Laurie A.; Coates, John D. Environmental Microbiology, Vol. 1, Issue 4, p. 319-329 https://doi.org/10.1046/j.1462-2920.1999.00042.x	journal	August 1999
Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters Cline, Joel D. Limnology and Oceanography, Vol. 14, Issue 3, p. 454-458 https://doi.org/10.4319/lo.1969.14.3.0454	journal	May 1969
Mitigating Sulfidogenesis With Simultaneous Perchlorate and Nitrate Treatments Engelbrektson, Anna; Briseno, Vanessa; Liu, Yi Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02305	journal	October 2018
Metabolic Flexibility of Sulfate-Reducing Bacteria Plugge, Caroline M.; Zhang, Weiwen; Scholten, Johannes C. M. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00081	journal	January 2011
Dethiosulfovibrio russensis sp. nov., Dethosulfovibrio marinus sp. nov. and Dethosulfovibrio acidaminovorans sp. nov., novel anaerobic, thiosulfate- and sulfur-reducing bacteria isolated from 'Thiodendron' sulfur mats in different saline environments. Surkov, A. V.; Dubinina, G. A.; Lysenko, A. M. International Journal of Systematic and Evolutionary Microbiology, Vol. 51, Issue 2 https://doi.org/10.1099/00207713-51-2-327	journal	March 2001
Transcriptomic and proteomic analyses of Desulfovibrio vulgaris biofilms: Carbon and energy flow contribute to the distinct biofilm growth state Clark, Melinda E.; He, Zhili; Redding, Alyssa M. BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-138	journal	January 2012
New Model for Electron Flow for Sulfate Reduction in Desulfovibrio alaskensis G20 Keller, Kimberly L.; Rapp-Giles, Barbara J.; Semkiw, Elizabeth S. Applied and Environmental Microbiology, Vol. 80, Issue 3 https://doi.org/10.1128/AEM.02963-13	journal	November 2013
Reduction of (per)chlorate by a novel organism isolated from paper mill waste Bruce, Royce A.; Achenbach, Laurie A.; Coates, John D. Environmental Microbiology, Vol. 1, Issue 4, p. 319-329 https://doi.org/10.1046/j.1462-2920.1999.00042.x	journal	August 1999
Genetic basis for nitrate resistance in Desulfovibrio strains Korte, Hannah L.; Fels, Samuel R.; Christensen, Geoff A. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00153	journal	April 2014
Assessing microbial competition in a hydrogen-based membrane biofilm reactor (MBfR) using multidimensional modeling: Modeling Competition in a Hydrogen-Based, Membrane Biofilm Reactor Martin, Kelly J.; Picioreanu, Cristian; Nerenberg, Robert Biotechnology and Bioengineering, Vol. 112, Issue 9 https://doi.org/10.1002/bit.25607	journal	July 2015
Reductive precipitation of sulfate and soluble Fe(III) by Desulfovibrio vulgaris: Electron donor regulates intracellular electron flow and nano-FeS crystallization Zhou, Chen; Zhou, Yun; Rittmann, Bruce E. Water Research, Vol. 119 https://doi.org/10.1016/j.watres.2017.04.044	journal	August 2017
Microbial community succession in a bioreactor modeling a souring low-temperature oil reservoir subjected to nitrate injection Callbeck, Cameron M.; Dong, Xiaoli; Chatterjee, Indranil Applied Microbiology and Biotechnology, Vol. 91, Issue 3 https://doi.org/10.1007/s00253-011-3287-2	journal	May 2011
Assessing microbial competition in a hydrogen-based membrane biofilm reactor (MBfR) using multidimensional modeling: Modeling Competition in a Hydrogen-Based, Membrane Biofilm Reactor Martin, Kelly J.; Picioreanu, Cristian; Nerenberg, Robert Biotechnology and Bioengineering, Vol. 112, Issue 9 https://doi.org/10.1002/bit.25607	journal	July 2015
Inhibition of microbial sulfate reduction in a flow-through column system by (per)chlorate treatment Engelbrektson, Anna; Hubbard, Christopher G.; Tom, Lauren M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00315	journal	June 2014
Dethiosulfatibacter aminovorans gen. nov., sp. nov., a novel thiosulfate-reducing bacterium isolated from coastal marine sediment via sulfate-reducing enrichment with Casamino acids Takii, S.; Hanada, S.; Tamaki, H. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 10 https://doi.org/10.1099/ijs.0.64882-0	journal	October 2007
Genetics and Molecular Biology of the Electron Flow for Sulfate Respiration in Desulfovibrio Keller, Kimberly L.; Wall, Judy D. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00135	journal	January 2011
Desulfocurvus vexinensis gen. nov., sp. nov., a sulfate-reducing bacterium isolated from a deep subsurface aquifer Klouche, N.; Basso, O.; Lascourreges, J. -F. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 12 https://doi.org/10.1099/ijs.0.010363-0	journal	July 2009
Detection and Enumeration of Sulphate-Reducing Bacteria in Estuarine Sediments by Competitive PCR Kondo, Ryuji; Nedwell, David B.; Purdy, Kevin J. Geomicrobiology Journal, Vol. 21, Issue 3 https://doi.org/10.1080/01490450490275307	journal	April 2004
Acetate Production from Oil under Sulfate-Reducing Conditions in Bioreactors Injected with Sulfate and Nitrate Callbeck, C. M.; Agrawal, A.; Voordouw, G. Applied and Environmental Microbiology, Vol. 79, Issue 16 https://doi.org/10.1128/AEM.01251-13	journal	June 2013
Spirochaeta perfilievii sp. nov., an oxygen-tolerant, sulfide-oxidizing, sulfur- and thiosulfate-reducing spirochaete isolated from a saline spring Dubinina, G.; Grabovich, M.; Leshcheva, N. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 1 https://doi.org/10.1099/ijs.0.018333-0	journal	February 2010
Sulfide Remediation by Pulsed Injection of Nitrate into a Low Temperature Canadian Heavy Oil Reservoir Voordouw, Gerrit; Grigoryan, Aleksandr A.; Lambo, Adewale Environmental Science & Technology, Vol. 43, Issue 24 https://doi.org/10.1021/es902211j	journal	December 2009
Comparative evaluation of microbial profiles of oral samples obtained at different collection time points and using different methods Omori, Michi; Kato-Kogoe, Nahoko; Sakaguchi, Shoichi Clinical Oral Investigations, Vol. 25, Issue 5 https://doi.org/10.1007/s00784-020-03592-y	journal	September 2020
Microbial perchlorate reduction: rocket-fuelled metabolism Coates, John D.; Achenbach, Laurie A. Nature Reviews Microbiology, Vol. 2, Issue 7 https://doi.org/10.1038/nrmicro926	journal	July 2004
Competitive Inhibition of Sulphate Reduction by Selenate Postgate, John Nature, Vol. 164, Issue 4172 https://doi.org/10.1038/164670b0	journal	October 1949
Mechanisms of direct inhibition of the respiratory sulfate-reduction pathway by (per)chlorate and nitrate Carlson, Hans K.; Kuehl, Jennifer V.; Hazra, Amrita B. The ISME Journal, Vol. 9, Issue 6 https://doi.org/10.1038/ismej.2014.216	journal	November 2014
Mechanistic study of microbial control of hydrogen sulfide production in oil reservoirs Nemati, M.; Jenneman, G. E.; Voordouw, G. Biotechnology and Bioengineering, Vol. 74, Issue 5 https://doi.org/10.1002/bit.1133	journal	January 2001
Spectrophotometric Determination Of Hydrogen Sulfide In Natural Waters Cline, Joel D. Limnology and Oceanography, Vol. 14, Issue 3, p. 454-458 https://doi.org/10.4319/lo.1969.14.3.0454	journal	May 1969
Dethiosulfovibrio russensis sp. nov., Dethosulfovibrio marinus sp. nov. and Dethosulfovibrio acidaminovorans sp. nov., novel anaerobic, thiosulfate- and sulfur-reducing bacteria isolated from 'Thiodendron' sulfur mats in different saline environments. Surkov, A. V.; Dubinina, G. A.; Lysenko, A. M. International Journal of Systematic and Evolutionary Microbiology, Vol. 51, Issue 2 https://doi.org/10.1099/00207713-51-2-327	journal	March 2001
Non-parametric multivariate analyses of changes in community structure Clarke, K. R. Austral Ecology, Vol. 18, Issue 1 https://doi.org/10.1111/j.1442-9993.1993.tb00438.x	journal	March 1993
Reactive Transport Model of Sulfur Cycling as Impacted by Perchlorate and Nitrate Treatments Cheng, Yiwei; Hubbard, Christopher G.; Li, Li Environmental Science & Technology, Vol. 50, Issue 13 https://doi.org/10.1021/acs.est.6b00081	journal	June 2016
Mechanism of H ₂ S Oxidation by the Dissimilatory Perchlorate-Reducing Microorganism Azospira suillum PS Mehta-Kolte, Misha G.; Loutey, Dana; Wang, Ouwei mBio, Vol. 8, Issue 1 https://doi.org/10.1128/mbio.02023-16	journal	February 2017
Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies Klindworth, Anna; Pruesse, Elmar; Schweer, Timmy Nucleic Acids Research, Vol. 41, Issue 1 https://doi.org/10.1093/nar/gks808	journal	August 2012
Dethiosulfovibrio peptidovorans gen. nov., sp. nov., a New Anaerobic, Slightly Halophilic, Thiosulfate-Reducing Bacterium from Corroding Offshore Oil Wells Magot, M.; Ravot, G.; Campaignolle, X. International Journal of Systematic Bacteriology, Vol. 47, Issue 3 https://doi.org/10.1099/00207713-47-3-818	journal	July 1997
Changes in sulfate-reducing bacterial populations during the onset of black band disease Bourne, David G.; Muirhead, Andrew; Sato, Yui The ISME Journal, Vol. 5, Issue 3 https://doi.org/10.1038/ismej.2010.143	journal	September 2010
Petrimonas sulfuriphila gen. nov., sp. nov., a mesophilic fermentative bacterium isolated from a biodegraded oil reservoir Grabowski, A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 3 https://doi.org/10.1099/ijs.0.63426-0	journal	May 2005
Independence of Nitrate and Nitrite Inhibition of Desulfovibrio vulgaris Hildenborough and Use of Nitrite as a Substrate for Growth Korte, Hannah L.; Saini, Avneesh; Trotter, Valentine V. Environmental Science & Technology, Vol. 49, Issue 2 https://doi.org/10.1021/es504484m	journal	January 2015
Independence of Nitrate and Nitrite Inhibition of Desulfovibrio vulgaris Hildenborough and Use of Nitrite as a Substrate for Growth Korte, Hannah L.; Saini, Avneesh; Trotter, Valentine V. Environmental Science & Technology, Vol. 49, Issue 2 https://doi.org/10.1021/es504484m	journal	January 2015
Physiological and Genetic Description of Dissimilatory Perchlorate Reduction by the Novel Marine Bacterium Arcobacter sp. Strain CAB Carlström, Charlotte I.; Wang, Ouwei; Melnyk, Ryan A. mBio, Vol. 4, Issue 3 https://doi.org/10.1128/mBio.00217-13	journal	May 2013
Microbial perchlorate reduction: rocket-fuelled metabolism Coates, John D.; Achenbach, Laurie A. Nature Reviews Microbiology, Vol. 2, Issue 7 https://doi.org/10.1038/nrmicro926	journal	July 2004
Reactive Transport Model of Sulfur Cycling as Impacted by Perchlorate and Nitrate Treatments Cheng, Yiwei; Hubbard, Christopher G.; Li, Li Environmental Science & Technology, Vol. 50, Issue 13 https://doi.org/10.1021/acs.est.6b00081	journal	June 2016
Development and comparison of SYBR Green quantitative real-time PCR assays for detection and enumeration of sulfate-reducing bacteria in stored swine manure Spence, C.; Whitehead, T. R.; Cotta, M. A. Journal of Applied Microbiology, Vol. 105, Issue 6 https://doi.org/10.1111/j.1365-2672.2008.03900.x	journal	December 2008
Mechanistic study of microbial control of hydrogen sulfide production in oil reservoirs Nemati, M.; Jenneman, G. E.; Voordouw, G. Biotechnology and Bioengineering, Vol. 74, Issue 5 https://doi.org/10.1002/bit.1133	journal	January 2001
Biological souring and mitigation in oil reservoirs Gieg, Lisa M.; Jack, Tom R.; Foght, Julia M. Applied Microbiology and Biotechnology, Vol. 92, Issue 2 https://doi.org/10.1007/s00253-011-3542-6	journal	August 2011
Changes in sulfate-reducing bacterial populations during the onset of black band disease Bourne, David G.; Muirhead, Andrew; Sato, Yui The ISME Journal, Vol. 5, Issue 3 https://doi.org/10.1038/ismej.2010.143	journal	September 2010
Petrimonas sulfuriphila gen. nov., sp. nov., a mesophilic fermentative bacterium isolated from a biodegraded oil reservoir Grabowski, A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 3 https://doi.org/10.1099/ijs.0.63426-0	journal	May 2005
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities Schloss, P. D.; Westcott, S. L.; Ryabin, T. Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541 https://doi.org/10.1128/AEM.01541-09	journal	October 2009
Characterization of an anaerobic marine microbial community exposed to combined fluxes of perchlorate and salinity Carlström, Charlotte I.; Lucas, Lauren N.; Rohde, Robert A. Applied Microbiology and Biotechnology, Vol. 100, Issue 22 https://doi.org/10.1007/s00253-016-7780-5	journal	September 2016
Genetics and Molecular Biology of the Electron Flow for Sulfate Respiration in Desulfovibrio Keller, Kimberly L.; Wall, Judy D. Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00135	journal	January 2011
Monofluorophosphate Is a Selective Inhibitor of Respiratory Sulfate-Reducing Microorganisms Carlson, Hans K.; Stoeva, Magdalena K.; Justice, Nicholas B. Environmental Science & Technology, Vol. 49, Issue 6 https://doi.org/10.1021/es505843z	journal	February 2015
Isolation and characterization of Desulfocurvus thunnarius sp. nov., a sulfate-reducing bacterium isolated from an anaerobic sequencing batch reactor treating cooking wastewater Hamdi, O.; Ben Hania, W.; Postec, A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 11 https://doi.org/10.1099/ijs.0.051664-0	journal	June 2013
Competitive and Non-competitive Inhibitors of Bacterial Sulphate Reduction Postgate, J. R. Journal of General Microbiology, Vol. 6, Issue 1-2 https://doi.org/10.1099/00221287-6-1-2-128	journal	February 1952
Dethiosulfatibacter aminovorans gen. nov., sp. nov., a novel thiosulfate-reducing bacterium isolated from coastal marine sediment via sulfate-reducing enrichment with Casamino acids Takii, S.; Hanada, S.; Tamaki, H. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 10 https://doi.org/10.1099/ijs.0.64882-0	journal	October 2007
Variation among Desulfovibrio Species in Electron Transfer Systems Used for Syntrophic Growth Meyer, B.; Kuehl, J.; Deutschbauer, A. M. Journal of Bacteriology, Vol. 195, Issue 5 https://doi.org/10.1128/JB.01959-12	journal	December 2012
Competitive Inhibition of Sulphate Reduction by Selenate Postgate, John Nature, Vol. 164, Issue 4172 https://doi.org/10.1038/164670b0	journal	October 1949
Control of sulfidogenesis through bio-oxidation of H ₂ S coupled to (per)chlorate reduction : (Per)chlorate-mediated sulfide bio-oxidation Gregoire, Patrick; Engelbrektson, Anna; Hubbard, Christopher G. Environmental Microbiology Reports, Vol. 6, Issue 6 https://doi.org/10.1111/1758-2229.12156	journal	April 2014
Stratified Microbial Structure and Activity in Sulfide- and Methane-Producing Anaerobic Sewer Biofilms Sun, Jing; Hu, Shihu; Sharma, Keshab Raj Applied and Environmental Microbiology, Vol. 80, Issue 22 https://doi.org/10.1128/aem.02146-14	journal	September 2014
Mechanisms of direct inhibition of the respiratory sulfate-reduction pathway by (per)chlorate and nitrate Carlson, Hans K.; Kuehl, Jennifer V.; Hazra, Amrita B. The ISME Journal, Vol. 9, Issue 6 https://doi.org/10.1038/ismej.2014.216	journal	November 2014
Rex (Encoded by DVU_0916) in Desulfovibrio vulgaris Hildenborough Is a Repressor of Sulfate Adenylyl Transferase and Is Regulated by NADH Christensen, G. A.; Zane, G. M.; Kazakov, A. E. Journal of Bacteriology, Vol. 197, Issue 1 https://doi.org/10.1128/JB.02083-14	journal	October 2014
Biological souring and mitigation in oil reservoirs Gieg, Lisa M.; Jack, Tom R.; Foght, Julia M. Applied Microbiology and Biotechnology, Vol. 92, Issue 2 https://doi.org/10.1007/s00253-011-3542-6	journal	August 2011
Genetic basis for nitrate resistance in Desulfovibrio strains Korte, Hannah L.; Fels, Samuel R.; Christensen, Geoff A. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00153	journal	April 2014
Phenotypic and Genotypic Description of Sedimenticola selenatireducens Strain CUZ, a Marine (Per)Chlorate-Respiring Gammaproteobacterium, and Its Close Relative the Chlorate-Respiring Sedimenticola Strain NSS Carlström, Charlotte I.; Loutey, Dana E.; Wang, Ouwei Applied and Environmental Microbiology, Vol. 81, Issue 8 https://doi.org/10.1128/AEM.03606-14	journal	February 2015
Nitrite reductase activity of sulphate-reducing bacteria prevents their inhibition by nitrate-reducing, sulphide-oxidizing bacteria Greene, E. A.; Hubert, C.; Nemati, M. Environmental Microbiology, Vol. 5, Issue 7 https://doi.org/10.1046/j.1462-2920.2003.00446.x	journal	July 2003
Microbial community succession in a bioreactor modeling a souring low-temperature oil reservoir subjected to nitrate injection Callbeck, Cameron M.; Dong, Xiaoli; Chatterjee, Indranil Applied Microbiology and Biotechnology, Vol. 91, Issue 3 https://doi.org/10.1007/s00253-011-3287-2	journal	May 2011
Corrosion of Iron by Sulfate-Reducing Bacteria: New Views of an Old Problem Enning, Dennis; Garrelfs, Julia Applied and Environmental Microbiology, Vol. 80, Issue 4 https://doi.org/10.1128/AEM.02848-13	journal	December 2013
Reductive precipitation of sulfate and soluble Fe(III) by Desulfovibrio vulgaris: Electron donor regulates intracellular electron flow and nano-FeS crystallization Zhou, Chen; Zhou, Yun; Rittmann, Bruce E. Water Research, Vol. 119 https://doi.org/10.1016/j.watres.2017.04.044	journal	August 2017
Isolation and characterization of Desulfocurvus thunnarius sp. nov., a sulfate-reducing bacterium isolated from an anaerobic sequencing batch reactor treating cooking wastewater Hamdi, O.; Ben Hania, W.; Postec, A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 11 https://doi.org/10.1099/ijs.0.051664-0	journal	June 2013
Spirochaeta perfilievii sp. nov., an oxygen-tolerant, sulfide-oxidizing, sulfur- and thiosulfate-reducing spirochaete isolated from a saline spring Dubinina, G.; Grabovich, M.; Leshcheva, N. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 1 https://doi.org/10.1099/ijs.0.018333-0	journal	February 2010
Global Transcriptional, Physiological, and Metabolite Analyses of the Responses of Desulfovibrio vulgaris Hildenborough to Salt Adaptation He, Z.; Zhou, A.; Baidoo, E. Applied and Environmental Microbiology, Vol. 76, Issue 5 https://doi.org/10.1128/AEM.02141-09	journal	December 2009
Desulfocurvus vexinensis gen. nov., sp. nov., a sulfate-reducing bacterium isolated from a deep subsurface aquifer Klouche, N.; Basso, O.; Lascourreges, J. -F. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 12 https://doi.org/10.1099/ijs.0.010363-0	journal	July 2009
Detection and Enumeration of Sulphate-Reducing Bacteria in Estuarine Sediments by Competitive PCR Kondo, Ryuji; Nedwell, David B.; Purdy, Kevin J. Geomicrobiology Journal, Vol. 21, Issue 3 https://doi.org/10.1080/01490450490275307	journal	April 2004
Sulfide Remediation by Pulsed Injection of Nitrate into a Low Temperature Canadian Heavy Oil Reservoir Voordouw, Gerrit; Grigoryan, Aleksandr A.; Lambo, Adewale Environmental Science & Technology, Vol. 43, Issue 24 https://doi.org/10.1021/es902211j	journal	December 2009
Growth Kinetics of Suspended Microbial Cells: From Single-Substrate-Controlled Growth to Mixed-Substrate Kinetics Kovárová-Kovar, Karin; Egli, Thomas Microbiology and Molecular Biology Reviews, Vol. 62, Issue 3 https://doi.org/10.1128/MMBR.62.3.646-666.1998	journal	September 1998