LurR is a regulator of the central lactate oxidation pathway in sulfate-reducing Desulfovibrio species
Abstract
The central carbon/lactate utilization pathway in the model sulfate-reducing bacterium, Desulfovibrio vulgaris Hildenborough, is encoded by the highly conserved operon DVU3025-3033. Our earlier in vitro genome-wide study had suggested a network of four two-component system regulators that target this large operon; however, how these four regulators control this operon was not known. Here, we probe the regulation of the lactate utilization operon with mutant strains and DNA-protein binding assays. We show that the LurR response regulator is required for optimal growth and complete lactate utilization, and that it activates the DVU3025-3033 lactate oxidation operon as well as DVU2451, a lactate permease gene, in the presence of lactate. We show by electrophoretic mobility shift assays that LurR binds to three sites in the upstream region of DVU3025, the first gene of the operon. NrfR, a response regulator that is activated under nitrite stress, and LurR share similar binding site motifs and bind the same sites upstream of DVU3025. The DVU3025 promoter also has a binding site motif (Pho box) that is bound by PhoB, a two-component response regulator activated under phosphate limitation. The lactate utilization operon, the regulator LurR, and LurR binding sites are conserved across the order Desulfovibrionales whereas possiblemore »
- Authors:
-
[1];
[1];
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Univ. of Missouri, Columbia, MO (United States)
- LSU Health Sciences Center School of Dentistry, New Orleans, LA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1545315
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 14; Journal Issue: 4; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Rajeev, Lara, Luning, Eric G., Zane, Grant M., Juba, Thomas R., Kazakov, Alexey E., Novichkov, Pavel S., Wall, Judy D., Mukhopadhyay, Aindrila, and Wen, Z. Tom. LurR is a regulator of the central lactate oxidation pathway in sulfate-reducing Desulfovibrio species. United States: N. p., 2019.
Web. doi:10.1371/journal.pone.0214960.
Rajeev, Lara, Luning, Eric G., Zane, Grant M., Juba, Thomas R., Kazakov, Alexey E., Novichkov, Pavel S., Wall, Judy D., Mukhopadhyay, Aindrila, & Wen, Z. Tom. LurR is a regulator of the central lactate oxidation pathway in sulfate-reducing Desulfovibrio species. United States. https://doi.org/10.1371/journal.pone.0214960
Rajeev, Lara, Luning, Eric G., Zane, Grant M., Juba, Thomas R., Kazakov, Alexey E., Novichkov, Pavel S., Wall, Judy D., Mukhopadhyay, Aindrila, and Wen, Z. Tom. Tue .
"LurR is a regulator of the central lactate oxidation pathway in sulfate-reducing Desulfovibrio species". United States. https://doi.org/10.1371/journal.pone.0214960. https://www.osti.gov/servlets/purl/1545315.
@article{osti_1545315,
title = {LurR is a regulator of the central lactate oxidation pathway in sulfate-reducing Desulfovibrio species},
author = {Rajeev, Lara and Luning, Eric G. and Zane, Grant M. and Juba, Thomas R. and Kazakov, Alexey E. and Novichkov, Pavel S. and Wall, Judy D. and Mukhopadhyay, Aindrila and Wen, Z. Tom},
abstractNote = {The central carbon/lactate utilization pathway in the model sulfate-reducing bacterium, Desulfovibrio vulgaris Hildenborough, is encoded by the highly conserved operon DVU3025-3033. Our earlier in vitro genome-wide study had suggested a network of four two-component system regulators that target this large operon; however, how these four regulators control this operon was not known. Here, we probe the regulation of the lactate utilization operon with mutant strains and DNA-protein binding assays. We show that the LurR response regulator is required for optimal growth and complete lactate utilization, and that it activates the DVU3025-3033 lactate oxidation operon as well as DVU2451, a lactate permease gene, in the presence of lactate. We show by electrophoretic mobility shift assays that LurR binds to three sites in the upstream region of DVU3025, the first gene of the operon. NrfR, a response regulator that is activated under nitrite stress, and LurR share similar binding site motifs and bind the same sites upstream of DVU3025. The DVU3025 promoter also has a binding site motif (Pho box) that is bound by PhoB, a two-component response regulator activated under phosphate limitation. The lactate utilization operon, the regulator LurR, and LurR binding sites are conserved across the order Desulfovibrionales whereas possible modulation of the lactate utilization genes by additional regulators such as NrfR and PhoB appears to be limited to D. vulgaris.},
doi = {10.1371/journal.pone.0214960},
journal = {PLoS ONE},
number = 4,
volume = 14,
place = {United States},
year = {Tue Apr 09 00:00:00 EDT 2019},
month = {Tue Apr 09 00:00:00 EDT 2019}
}
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Figures / Tables:
Fig 1: Lactate utilization operon in Desulfovibrio. A. Lactate is transported inside the cell by a lactate permease (DVU3026, llp). D- (DVU3027-3028, dld-II) and L-lactate dehydrogenases (DVU3032-3033, lldGH) oxidize lactate to pyruvate [6]. Pyruvate is then oxidatively decarboxylated to acetyl-CoA via a pyruvate ferredoxin oxidoreductase (DVU3025, por) [7,8]. Acetyl-CoA ismore »
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Works referenced in this record:
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape
journal, May 2016
- O’Malley, Ronan C.; Huang, Shao-shan Carol; Song, Liang
- Cell, Vol. 165, Issue 5
Response of Desulfovibrio vulgaris to Alkaline Stress
journal, October 2007
- Stolyar, S.; He, Q.; Joachimiak, M. P.
- Journal of Bacteriology, Vol. 189, Issue 24
Regulation of L-Lactate Utilization by the FadR-Type Regulator LldR of Corynebacterium glutamicum
journal, November 2007
- Georgi, T.; Engels, V.; Wendisch, V. F.
- Journal of Bacteriology, Vol. 190, Issue 3
Mutant phenotypes for thousands of bacterial genes of unknown function
journal, May 2018
- Price, Morgan N.; Wetmore, Kelly M.; Waters, R. Jordan
- Nature, Vol. 557, Issue 7706
Multiple signaling systems target a core set of transition metal homeostasis genes using similar binding motifs: Multiple signaling systems
journal, January 2018
- Garber, Megan E.; Rajeev, Lara; Kazakov, Alexey E.
- Molecular Microbiology, Vol. 107, Issue 6
How sulphate-reducing microorganisms cope with stress: lessons from systems biology
journal, May 2011
- Zhou, Jizhong; He, Qiang; Hemme, Christopher L.
- Nature Reviews Microbiology, Vol. 9, Issue 6
Transcription Factor Family-Based Reconstruction of Singleton Regulons and Study of the Crp/Fnr, ArsR, and GntR Families in Desulfovibrionales Genomes
journal, October 2012
- Kazakov, A. E.; Rodionov, D. A.; Price, M. N.
- Journal of Bacteriology, Vol. 195, Issue 1
Strong cross-system interactions drive the activation of the QseB response regulator in the absence of its cognate sensor
journal, September 2013
- Guckes, K. R.; Kostakioti, M.; Breland, E. J.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 41
Deletion of the Desulfovibrio vulgaris Carbon Monoxide Sensor Invokes Global Changes in Transcription
journal, August 2012
- Rajeev, L.; Hillesland, K. L.; Zane, G. M.
- Journal of Bacteriology, Vol. 194, Issue 21
Regulation of Nitrite Stress Response in Desulfovibrio vulgaris Hildenborough, a Model Sulfate-Reducing Bacterium
journal, August 2015
- Rajeev, Lara; Chen, Amy; Kazakov, Alexey E.
- Journal of Bacteriology, Vol. 197, Issue 21
The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris
journal, July 2009
- Walker, C. B.; He, Z.; Yang, Z. K.
- Journal of Bacteriology, Vol. 191, Issue 18
Octomeric pyruvate-ferredoxin oxidoreductase from Desulfovibrio vulgaris
journal, July 2007
- Garczarek, F.; Dong, M.; Typke, D.
- Journal of Structural Biology, Vol. 159, Issue 1
Salt Stress in Desulfovibrio vulgaris Hildenborough: an Integrated Genomics Approach
journal, May 2006
- Mukhopadhyay, A.; He, Z.; Alm, E. J.
- Journal of Bacteriology, Vol. 188, Issue 11
Energetic Consequences of Nitrite Stress in Desulfovibrio vulgaris Hildenborough, Inferred from Global Transcriptional Analysis
journal, June 2006
- He, Q.; Huang, K. H.; He, Z.
- Applied and Environmental Microbiology, Vol. 72, Issue 6
Temporal Transcriptomic Analysis as Desulfovibrio vulgaris Hildenborough Transitions into Stationary Phase during Electron Donor Depletion
journal, August 2006
- Clark, M. E.; He, Q.; He, Z.
- Applied and Environmental Microbiology, Vol. 72, Issue 8
The primary pathway for lactate oxidation in Desulfovibrio vulgaris
journal, June 2015
- Vita, Nicolas; Valette, Odile; Brasseur, Gaël
- Frontiers in Microbiology, Vol. 6
A Widely Conserved Gene Cluster Required for Lactate Utilization in Bacillus subtilis and Its Involvement in Biofilm Formation
journal, February 2009
- Chai, Y.; Kolter, R.; Losick, R.
- Journal of Bacteriology, Vol. 191, Issue 8
Genomic reconstruction of Shewanella oneidensis MR-1 metabolism reveals a previously uncharacterized machinery for lactate utilization
journal, February 2009
- Pinchuk, Grigory E.; Rodionov, Dmitry A.; Yang, Chen
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 8
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
Cell-Wide Responses to Low-Oxygen Exposure in Desulfovibrio vulgaris Hildenborough
journal, June 2007
- Mukhopadhyay, A.; Redding, A. M.; Joachimiak, M. P.
- Journal of Bacteriology, Vol. 189, Issue 16
Genetics and Molecular Biology of the Electron Flow for Sulfate Respiration in Desulfovibrio
journal, January 2011
- Keller, Kimberly L.; Wall, Judy D.
- Frontiers in Microbiology, Vol. 2
Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC
journal, February 2007
- Li, Mamie Z.; Elledge, Stephen J.
- Nature Methods, Vol. 4, Issue 3
MtrA, an essential response regulator of the MtrAB two-component system, regulates the transcription of resuscitation-promoting factor B of Mycobacterium tuberculosis
journal, June 2015
- Basu, Joyoti; Kundu, Manikuntala; Mandal, Sukhendu
- Microbiology, Vol. 161, Issue 6
Pyruvate Dehydrogenase and the Path of Lactate Degradation in Desulfovibrio vulgaris Miyazaki F1
journal, January 1986
- Ogata, Mari; Yagi, Tatsuhiko
- The Journal of Biochemistry, Vol. 100, Issue 2
Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks
journal, September 2010
- Ishihama, Akira
- FEMS Microbiology Reviews, Vol. 34, Issue 5
Dual Role of LldR in Regulation of the lldPRD Operon, Involved in L-Lactate Metabolism in Escherichia coli
journal, February 2008
- Aguilera, L.; Campos, E.; Gimenez, R.
- Journal of Bacteriology, Vol. 190, Issue 8
Lactate Utilization Is Regulated by the FadR-Type Regulator LldR in Pseudomonas aeruginosa
journal, March 2012
- Gao, C.; Hu, C.; Zheng, Z.
- Journal of Bacteriology, Vol. 194, Issue 10
Global Analysis of Heat Shock Response in Desulfovibrio vulgaris Hildenborough
journal, February 2006
- Chhabra, S. R.; He, Q.; Huang, K. H.
- Journal of Bacteriology, Vol. 188, Issue 5
The ecology and biotechnology of sulphate-reducing bacteria
journal, May 2008
- Muyzer, Gerard; Stams, Alfons J. M.
- Nature Reviews Microbiology, Vol. 6, Issue 6
Erosion of functional independence early in the evolution of a microbial mutualism
journal, September 2014
- Hillesland, K. L.; Lim, S.; Flowers, J. J.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 41
Systematic mapping of two component response regulators to gene targets in a model sulfate reducing bacterium
journal, January 2011
- Rajeev, Lara; Luning, Eric G.; Dehal, Paramvir S.
- Genome Biology, Vol. 12, Issue 10
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape
journal, September 2016
- O’Malley, Ronan C.; Huang, Shao-shan Carol; Song, Liang
- Cell, Vol. 166, Issue 6
Preferential Utilization of d-Lactate by Shewanella oneidensis
journal, September 2012
- Brutinel, Evan D.; Gralnick, Jeffrey A.
- Applied and Environmental Microbiology, Vol. 78, Issue 23
Effect of the Deletion of qmoABC and the Promoter-Distal Gene Encoding a Hypothetical Protein on Sulfate Reduction in Desulfovibrio vulgaris Hildenborough
journal, June 2010
- Zane, G. M.; Yen, H. -c. B.; Wall, J. D.
- Applied and Environmental Microbiology, Vol. 76, Issue 16
System-Wide Adaptations of Desulfovibrio alaskensis G20 to Phosphate-Limited Conditions
journal, December 2016
- Bosak, Tanja; Schubotz, Florence; de Santiago-Torio, Ana
- PLOS ONE, Vol. 11, Issue 12
IMG/M: integrated genome and metagenome comparative data analysis system
journal, October 2016
- Chen, I-Min A.; Markowitz, Victor M.; Chu, Ken
- Nucleic Acids Research, Vol. 45, Issue D1
Evidence-Based Annotation of Transcripts and Proteins in the Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough
journal, August 2011
- Price, M. N.; Deutschbauer, A. M.; Kuehl, J. V.
- Journal of Bacteriology, Vol. 193, Issue 20
WebLogo: A Sequence Logo Generator
journal, May 2004
- Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc
- Genome Research, Vol. 14, Issue 6, p. 1188-1190
Functional Genomics with a Comprehensive Library of Transposon Mutants for the Sulfate-Reducing Bacterium Desulfovibrio alaskensis G20
journal, May 2014
- Kuehl, Jennifer V.; Price, Morgan N.; Ray, Jayashree
- mBio, Vol. 5, Issue 3
Global Transcriptional, Physiological, and Metabolite Analyses of the Responses of Desulfovibrio vulgaris Hildenborough to Salt Adaptation
journal, December 2009
- He, Z.; Zhou, A.; Baidoo, E.
- Applied and Environmental Microbiology, Vol. 76, Issue 5
Microbial community response to addition of polylactate compounds to stimulate hexavalent chromium reduction in groundwater
journal, October 2011
- Brodie, Eoin L.; Joyner, Dominique C.; Faybishenko, Boris
- Chemosphere, Vol. 85, Issue 4
Regulation of Oxidative Stress Response by CosR, an Essential Response Regulator in Campylobacter jejuni
journal, July 2011
- Hwang, Sunyoung; Kim, Minkyeong; Ryu, Sangryeol
- PLoS ONE, Vol. 6, Issue 7
Recent advances in the study of the sulfate-reducing bacteria
journal, December 1965
- Postgate, J. R.
- Bacteriological Reviews, Vol. 29, Issue 4
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