Nitrite Control over Dissimilatory Nitrate/Nitrite Reduction Pathways in Shewanella loihica Strain PV-4
Abstract
ABSTRACT Shewanella loihicastrain PV-4 harbors both a functional denitrification (NO3-→N2) and a respiratory ammonification (NO3-→NH4+) pathway. Batch and chemostat experiments revealed that NO2-affects pathway selection and the formation of reduced products. Strain PV-4 cells grown with NO2-as the sole electron acceptor produced exclusively NH4+. With NO3-as the electron acceptor, denitrification predominated and N2O accounted for ~90% of reduced products in the presence of acetylene. Additionally, chemostat experiments demonstrated that the NO2-:NO3-ratio affected the distribution of reduced products, and respiratory ammonification dominated at high NO2-:NO3-ratios, whereas low NO2-:NO3-ratios favored denitrification. The NO2-:NO3-ratios affectednirKtranscript abundance, a measure of denitrification activity, in the chemostat experiments, and cells grown at a NO2-:NO3-ratio of 3 had ~37-fold fewernirKtranscripts per cell than cells grown with NO3-as the sole electron acceptor. In contrast, the transcription ofnrfA, implicated in NO2--to-NH4+reduction, remained statistically unchanged under continuous cultivation conditions at NO2-:NO3-ratios below 3. At NO2-:NO3-ratios above 3, bothnirKandnrfAtranscript numbers decreased and the chemostat culture washed out, presumably due to NO2-toxicity. Finally, these findings implicate NO2-as a relevant modulator of NO3-fate inS. loihicastrain PV-4, and, by extension, suggest that NO2-is a relevant determinant for N retention (i.e., ammonification) versus N loss and greenhouse gas emission (i.e., denitrification).
- Authors:
-
- Univ. of Tennessee, Knoxville, TN (United States). Center for Environmental Biotechnology and Department of Microbiology; Korea Advanced Institute of Science and Technology, Daejeon (South Korea). Department of Civil and Environmental Engineering
- Univ. of Illinois, Urbana, IL (United States). Department of Geology
- Univ. of Tennessee, Knoxville, TN (United States). Center for Environmental Biotechnology, Department of Microbiology and Department of Civil and Environmental Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). University of Tennessee and Oak Ridge National Laboratory (UT-ORNL) Joint Institute for Biological Sciences (JIBS) and Biosciences Division
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1470901
- Grant/Contract Number:
- AC05-00OR22725; SC0006662
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Applied and Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 81; Journal Issue: 10; Journal ID: ISSN 0099-2240
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES
Citation Formats
Yoon, Sukhwan, Sanford, Robert A., and Löffler, Frank E. Nitrite Control over Dissimilatory Nitrate/Nitrite Reduction Pathways in Shewanella loihica Strain PV-4. United States: N. p., 2015.
Web. doi:10.1128/AEM.00688-15.
Yoon, Sukhwan, Sanford, Robert A., & Löffler, Frank E. Nitrite Control over Dissimilatory Nitrate/Nitrite Reduction Pathways in Shewanella loihica Strain PV-4. United States. https://doi.org/10.1128/AEM.00688-15
Yoon, Sukhwan, Sanford, Robert A., and Löffler, Frank E. Fri .
"Nitrite Control over Dissimilatory Nitrate/Nitrite Reduction Pathways in Shewanella loihica Strain PV-4". United States. https://doi.org/10.1128/AEM.00688-15. https://www.osti.gov/servlets/purl/1470901.
@article{osti_1470901,
title = {Nitrite Control over Dissimilatory Nitrate/Nitrite Reduction Pathways in Shewanella loihica Strain PV-4},
author = {Yoon, Sukhwan and Sanford, Robert A. and Löffler, Frank E.},
abstractNote = {ABSTRACT Shewanella loihicastrain PV-4 harbors both a functional denitrification (NO3-→N2) and a respiratory ammonification (NO3-→NH4+) pathway. Batch and chemostat experiments revealed that NO2-affects pathway selection and the formation of reduced products. Strain PV-4 cells grown with NO2-as the sole electron acceptor produced exclusively NH4+. With NO3-as the electron acceptor, denitrification predominated and N2O accounted for ~90% of reduced products in the presence of acetylene. Additionally, chemostat experiments demonstrated that the NO2-:NO3-ratio affected the distribution of reduced products, and respiratory ammonification dominated at high NO2-:NO3-ratios, whereas low NO2-:NO3-ratios favored denitrification. The NO2-:NO3-ratios affectednirKtranscript abundance, a measure of denitrification activity, in the chemostat experiments, and cells grown at a NO2-:NO3-ratio of 3 had ~37-fold fewernirKtranscripts per cell than cells grown with NO3-as the sole electron acceptor. In contrast, the transcription ofnrfA, implicated in NO2--to-NH4+reduction, remained statistically unchanged under continuous cultivation conditions at NO2-:NO3-ratios below 3. At NO2-:NO3-ratios above 3, bothnirKandnrfAtranscript numbers decreased and the chemostat culture washed out, presumably due to NO2-toxicity. Finally, these findings implicate NO2-as a relevant modulator of NO3-fate inS. loihicastrain PV-4, and, by extension, suggest that NO2-is a relevant determinant for N retention (i.e., ammonification) versus N loss and greenhouse gas emission (i.e., denitrification).},
doi = {10.1128/AEM.00688-15},
journal = {Applied and Environmental Microbiology},
number = 10,
volume = 81,
place = {United States},
year = {Fri Mar 13 00:00:00 EDT 2015},
month = {Fri Mar 13 00:00:00 EDT 2015}
}
Web of Science
Works referenced in this record:
Viologen dye Inhibition of Methane Formation by Methanobacillus Omelianskii
journal, January 1964
- Wolin, E. A.; Wolfe, R. S.; Wolin, M. J.
- Journal of Bacteriology, Vol. 87, Issue 5
Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils
journal, November 2012
- Sanford, R. A.; Wagner, D. D.; Wu, Q.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 48
Shewanella loihica sp. nov., isolated from iron-rich microbial mats in the Pacific Ocean
journal, August 2006
- Gao, H.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 8
Denitrification and its control
journal, January 1994
- Ferguson, Stuart J.
- Antonie van Leeuwenhoek, Vol. 66, Issue 1-3
Nitrite in soils: accumulation and role in the formation of gaseous N compounds
journal, January 1995
- Cleemput, Oswald; Samater, Abdullahi H.
- Fertilizer Research, Vol. 45, Issue 1
Denitrification versus respiratory ammonification: environmental controls of two competing dissimilatory NO3−/NO2− reduction pathways in Shewanella loihica strain PV-4
journal, October 2014
- Yoon, Sukhwan; Cruz-García, Claribel; Sanford, Robert
- The ISME Journal, Vol. 9, Issue 5
Nitrous Oxide (N2O): The Dominant Ozone-Depleting Substance Emitted in the 21st Century
journal, August 2009
- Ravishankara, A. R.; Daniel, J. S.; Portmann, R. W.
- Science, Vol. 326, Issue 5949
Shewanella spp. Use Acetate as an Electron Donor for Denitrification but Not Ferric Iron or Fumarate Reduction
journal, February 2013
- Yoon, Sukhwan; Sanford, Robert A.; Löffler, Frank E.
- Applied and Environmental Microbiology, Vol. 79, Issue 8
Growth Yields in Bacterial Denitrification and Nitrate Ammonification
journal, January 2007
- Strohm, T. O.; Griffin, B.; Zumft, W. G.
- Applied and Environmental Microbiology, Vol. 73, Issue 5
In silico analysis of complete bacterial genomes: PCR, AFLP-PCR and endonuclease restriction
journal, January 2004
- Bikandi, J.; Millan, R. S.; Rementeria, A.
- Bioinformatics, Vol. 20, Issue 5
The environmental controls that govern the end product of bacterial nitrate respiration
journal, August 2014
- Kraft, B.; Tegetmeyer, H. E.; Sharma, R.
- Science, Vol. 345, Issue 6197
Co-Occurring Anammox, Denitrification, and Codenitrification in Agricultural Soils
journal, October 2012
- Long, Andrew; Heitman, Joshua; Tobias, Craig
- Applied and Environmental Microbiology, Vol. 79, Issue 1
Soil pH affects the processes reducing nitrate to nitrous oxide and di-nitrogen
journal, August 1998
- Stevens, R. J.; Laughlin, R. J.; Malone, J. P.
- Soil Biology and Biochemistry, Vol. 30, Issue 8-9
Nitrite concentration influences the population structure of Nitrospira-like bacteria
journal, August 2006
- Maixner, Frank; Noguera, Daniel R.; Anneser, Bettina
- Environmental Microbiology, Vol. 8, Issue 8
Dissimilatory nitrate reduction in anaerobic sediments leading to river nitrite accumulation.
journal, January 1997
- Kelso, B.; Smith, R. V.; Laughlin, R. J.
- Applied and environmental microbiology, Vol. 63, Issue 12
Respiratory Nitrate Ammonification by Shewanella oneidensis MR-1
journal, November 2006
- Cruz-Garcia, C.; Murray, A. E.; Klappenbach, J. A.
- Journal of Bacteriology, Vol. 189, Issue 2
Oxygen Effect on Dehalococcoides Viability and Biomarker Quantification
journal, August 2008
- Amos, Benjamin K.; Ritalahti, Kirsti M.; Cruz-Garcia, Claribel
- Environmental Science & Technology, Vol. 42, Issue 15
Transcription and activities of NO x reductases in Agrobacterium tumefaciens : the influence of nitrate, nitrite and oxygen availability
journal, November 2008
- Bergaust, Linda; Shapleigh, James; Frostegård, Åsa
- Environmental Microbiology, Vol. 10, Issue 11
Influence of nitrite accumulation in association with seasonal patterns and mineralization of soil nitrogen in a semi-arid pine forest
journal, February 2008
- Gelfand, Ilya; Yakir, Dan
- Soil Biology and Biochemistry, Vol. 40, Issue 2
Kinetic Explanation for Accumulation of Nitrite, Nitric Oxide, and Nitrous Oxide During Bacterial Denitrification †
journal, January 1981
- Betlach, Michael R.; Tiedje, James M.
- Applied and Environmental Microbiology, Vol. 42, Issue 6
Denitrification kinetics of high nitrate concentration water: pH effect on inhibition and nitrite accumulation
journal, March 1998
- Glass, Charles; Silverstein, JoAnn
- Water Research, Vol. 32, Issue 3
Acetylene inhibition of nitrous oxide reduction and measurement of denitrification and nitrogen fixation in soil
journal, January 1977
- Yoshinari, T.; Hynes, R.; Knowles, R.
- Soil Biology and Biochemistry, Vol. 9, Issue 3, p. 177-183
New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation
journal, May 2007
- Francis, Christopher A.; Beman, J. Michael; Kuypers, Marcel M. M.
- The ISME Journal, Vol. 1, Issue 1
Distribution of adsorbed ammonium pools in two intertidal sedimentary structures, Marennes-Oléron Bay, France
journal, January 1999
- Laima, Mjc; Girard, Mf; Vouvé, F.
- Marine Ecology Progress Series, Vol. 182
Microarray analysis of gene regulation by oxygen, nitrate, nitrite, FNR, NarL and NarP during anaerobic growth of Escherichia coli: new insights into microbial physiology
journal, January 2006
- Overton, T. W.; Griffiths, L.; Patel, M. D.
- Biochemical Society Transactions, Vol. 34, Issue 1
The estimation of gas solubilities in salt solutions
journal, January 1993
- Schumpe, Adrian
- Chemical Engineering Science, Vol. 48, Issue 1
Biotic and abiotic immobilization of ammonium, nitrite, and nitrate in soils developed under different tree species in the Catskill Mountains, New York, USA
journal, November 2003
- Fitzhugh, Ross D.; Lovett, Gary M.; Venterea, Rodney T.
- Global Change Biology, Vol. 9, Issue 11
Free Ammonia Inhibition of Nitrification in River Sediments Leading to Nitrite Accumulation
journal, January 1997
- Smith, R. V.; Burns, L. C.; Doyle, R. M.
- Journal of Environment Quality, Vol. 26, Issue 4
Competition in denitrification systems affecting reduction rate and accumulation of nitrite
journal, February 1987
- Wilderer, Peter A.; Jones, Warren L.; Dau, Ursula
- Water Research, Vol. 21, Issue 2
Origin, causes and effects of increased nitrite concentrations in aquatic environments
journal, June 2002
- Philips, Sarah; Laanbroek, Hendrikus J.; Verstraete, Willy
- Reviews in Environmental Science and Bio/Technology, Vol. 1, Issue 2
Mechanisms of nitrite accumulation occurring in soil nitrification
journal, February 2003
- Shen, Q. R.; Ran, W.; Cao, Z. H.
- Chemosphere, Vol. 50, Issue 6
Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways
journal, March 2007
- Burgin, Amy J.; Hamilton, Stephen K.
- Frontiers in Ecology and the Environment, Vol. 5, Issue 2
An Internal Reference Technique for Accurately Quantifying Specific mRNAs by Real-Time PCR with Application to the tceA Reductive Dehalogenase Gene
journal, July 2005
- Johnson, D. R.; Lee, P. K. H.; Holmes, V. F.
- Applied and Environmental Microbiology, Vol. 71, Issue 7
The nrfA and nirB Nitrite Reductase Operons in Escherichia coli Are Expressed Differently in Response to Nitrate than to Nitrite
journal, October 2000
- Wang, H.; Gunsalus, R. P.
- Journal of Bacteriology, Vol. 182, Issue 20
Inhibitory effects of nitrate, nitrite, NO and N2O on methanogenesis by Methanosarcina barkeri and Methanobacterium bryantii
journal, April 1998
- Klüber, H. Detlef; Conrad, Ralf
- FEMS Microbiology Ecology, Vol. 25, Issue 4
Relative contributions of greenhouse gas emissions to global warming
journal, April 1990
- Lashof, Daniel A.; Ahuja, Dilip R.
- Nature, Vol. 344, Issue 6266
Effect of nitrite on anoxic phosphate uptake in biological phosphorus removal activated sludge
journal, June 1999
- Meinhold, Jens; Arnold, Eva; Isaacs, Steven
- Water Research, Vol. 33, Issue 8
Denitrification: ecological niches, competition and survival
journal, January 1983
- Tiedje, James M.; Sexstone, Alan J.; Myrold, David D.
- Antonie van Leeuwenhoek, Vol. 48, Issue 6
Inhibitory effects of nitrate, nitrite, NO and N2O on methanogenesis by Methanosarcina barkeri and Methanobacterium bryantii
journal, April 1998
- Klüber, H.
- FEMS Microbiology Ecology, Vol. 25, Issue 4
Works referencing / citing this record:
Role of nitrite in the competition between denitrification and DNRA in a chemostat enrichment culture
journal, May 2017
- van den Berg, Eveline M.; Rombouts, Julius L.; Kuenen, J. Gijs
- AMB Express, Vol. 7, Issue 1
Ecological and physiological implications of nitrogen oxide reduction pathways on greenhouse gas emissions in agroecosystems
journal, May 2019
- Yoon, Sukhwan; Song, Bongkeun; Phillips, Rebecca L.
- FEMS Microbiology Ecology, Vol. 95, Issue 6
Influence of nitrate and nitrite concentration on N 2 O production via dissimilatory nitrate/nitrite reduction to ammonium in Bacillus paralicheniformis LMG 6934
journal, March 2018
- Sun, Yihua; De Vos, Paul; Willems, Anne
- MicrobiologyOpen, Vol. 7, Issue 4
Nitrogen assimilation in denitrifier Bacillus azotoformans LMG 9581T
journal, July 2017
- Sun, Yihua; De Vos, Paul; Willems, Anne
- Antonie van Leeuwenhoek, Vol. 110, Issue 12
Resource Concentration Modulates the Fate of Dissimilated Nitrogen in a Dual-Pathway Actinobacterium
journal, January 2019
- Vuono, David C.; Read, Robert W.; Hemp, James
- Frontiers in Microbiology, Vol. 10
Highly diverse nirK genes comprise two major clades that harbour ammonium-producing denitrifiers
journal, February 2016
- Helen, Decleyre; Kim, Heylen; Tytgat, Bjorn
- BMC Genomics, Vol. 17, Issue 1
Elucidating the Competition between Heterotrophic Denitrification and DNRA Using the Resource-Ratio Theory
journal, October 2020
- Jia, Mingsheng; Winkler, Mari K. H.; Volcke, Eveline I. P.
- Environmental Science & Technology, Vol. 54, Issue 21