Genome-Scale, Constraint-Based Modeling of Nitrogen Oxide Fluxes during Coculture of Nitrosomonas europaea and Nitrobacter winogradskyi

Mellbye, Brett L.; Giguere, Andrew T.; Murthy, Ganti S.; Bottomley, Peter J.; Sayavedra-Soto, Luis A.; Chaplen, Frank W.  R.

doi:10.1128/msystems.00170-17

Title: Genome-Scale, Constraint-Based Modeling of Nitrogen Oxide Fluxes during Coculture of Nitrosomonas europaea and Nitrobacter winogradskyi

Journal Article · Tue Mar 13 00:00:00 EDT 2018 · mSystems

DOI:https://doi.org/10.1128/msystems.00170-17· OSTI ID:1626174

^[1]; Giguere, Andrew T. ^[2]; Murthy, Ganti S. ^[3]; Bottomley, Peter J. ^[4]; Sayavedra-Soto, Luis A. ^[1]; Chaplen, Frank W. R. ^[3]

Oregon State Univ., Corvallis, OR (United States). Dept. of Botany and Plant Pathology
Oregon State Univ., Corvallis, OR (United States). Dept. of Crop and Soil Science
Oregon State Univ., Corvallis, OR (United States). Biological and Ecological Engineering
Oregon State Univ., Corvallis, OR (United States). Dept. of Crop and Soil Science; Oregon State Univ., Corvallis, OR (United States). Dept. of Microbiology

Nitrification, the aerobic oxidation of ammonia to nitrate via nitrite, emits nitrogen (N) oxide gases (NO, NO₂, and N₂O), which are potentially hazardous compounds that contribute to global warming. To better understand the dynamics of nitrification-derived N oxide production, we conducted culturing experiments and used an integrative genome-scale, constraint-based approach to model N oxide gas sources and sinks during complete nitrification in an aerobic coculture of two model nitrifying bacteria, the ammonia-oxidizing bacterium Nitrosomonas europaea and the nitrite-oxidizing bacterium Nitrobacter winogradskyi. The model includes biotic genome-scale metabolic models (iFC578 and iFC579) for each nitrifier and abiotic N oxide reactions. Modeling suggested both biotic and abiotic reactions are important sources and sinks of N oxides, particularly under microaerobic conditions predicted to occur in coculture. In particular, integrative modeling suggested that previous models might have underestimated gross NO production during nitrification due to not taking into account its rapid oxidation in both aqueous and gas phases. The integrative model may be found at https://github.com/chaplenf/microBiome-v2.1.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oregon State Univ., Corvallis, OR (United States)

Sponsoring Organization:: USDOE Office of Science (SC); USDA; National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231; ER65192; 2012-67019-3028; 2016-67012-24691; 1239870; IIS-1320943

OSTI ID:: 1626174

Journal Information:: mSystems, Vol. 3, Issue 3; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

Energy model and metabolic flux analysis for autotrophic nitrifiers Poughon, Laurent; Dussap, Claude-Gilles; Gros, Jean-Bernard Biotechnology and Bioengineering, Vol. 72, Issue 4 https://doi.org/10.1002/1097-0290(20000220)72:4<416::AID-BIT1004>3.0.CO;2-D	journal	January 2001
Nitrite Reductase of Nitrosomonas europaea Is Not Essential for Production of Gaseous Nitrogen Oxides and Confers Tolerance to Nitrite Beaumont, H. J. E.; Hommes, N. G.; Sayavedra-Soto, L. A. Journal of Bacteriology, Vol. 184, Issue 9 https://doi.org/10.1128/JB.184.9.2557-2560.2002	journal	May 2002
Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase Caranto, Jonathan D.; Lancaster, Kyle M. Proceedings of the National Academy of Sciences, Vol. 114, Issue 31 https://doi.org/10.1073/pnas.1704504114	journal	July 2017
Quorum Quenching of Nitrobacter winogradskyi Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification Mellbye, Brett L.; Giguere, Andrew T.; Bottomley, Peter J. mBio, Vol. 7, Issue 5 https://doi.org/10.1128/mBio.01753-16	journal	October 2016
Complete genome of Nitrosospira briensis C-128, an ammonia-oxidizing bacterium from agricultural soil Rice, Marlen C.; Norton, Jeanette M.; Valois, Frederica Standards in Genomic Sciences, Vol. 11, Issue 1 https://doi.org/10.1186/s40793-016-0168-4	journal	July 2016
Influence of physicochemical and operational parameters on Nitrobacter and Nitrospira communities in an aerobic activated sludge bioreactor Huang, Zhonghua; Gedalanga, Phillip B.; Asvapathanagul, Pitiporn Water Research, Vol. 44, Issue 15 https://doi.org/10.1016/j.watres.2010.05.037	journal	August 2010
Interactions of Nitrosomonas europaea and Nitrobacter winogradskyi grown in co-culture Pérez, José; Buchanan, Alex; Mellbye, Brett Archives of Microbiology, Vol. 197, Issue 1 https://doi.org/10.1007/s00203-014-1056-1	journal	November 2014
Nitrous oxide production by lithotrophic ammonia-oxidizing bacteria and implications for engineered nitrogen-removal systems Chandran, Kartik; Stein, Lisa Y.; Klotz, Martin G. Biochemical Society Transactions, Vol. 39, Issue 6 https://doi.org/10.1042/BST20110717	journal	November 2011
Dynamic flux balance analysis for synthetic microbial communities Henson, Michael A.; Hanly, Timothy J. IET Systems Biology, Vol. 8, Issue 5 https://doi.org/10.1049/iet-syb.2013.0021	journal	October 2014
Complete Genome Sequence of the Ammonia-Oxidizing Bacterium and Obligate Chemolithoautotroph Nitrosomonas europaea Chain, Patrick; Lamerdin, Jane; Larimer, Frank Journal of Bacteriology, Vol. 185, Issue 21 https://doi.org/10.1128/JB.185.21.6496.2003	journal	November 2003
Genome Sequence of the Chemolithoautotrophic Nitrite-Oxidizing Bacterium Nitrobacter winogradskyi Nb-255 Starkenburg, S. R.; Chain, P. S. G.; Sayavedra-Soto, L. A. Applied and Environmental Microbiology, Vol. 72, Issue 3 https://doi.org/10.1128/AEM.72.3.2050-2063.2006	journal	March 2006
Data, information, knowledge and principle: back to metabolism in KEGG Kanehisa, Minoru; Goto, Susumu; Sato, Yoko Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1076	journal	November 2013
Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Butterbach-Bahl, Klaus; Baggs, Elizabeth M.; Dannenmann, Michael Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1621 https://doi.org/10.1098/rstb.2013.0122	journal	July 2013
Assessment of nitric oxide (NO) redox reactions contribution to nitrous oxide (N ₂ O) formation during nitrification using a multispecies metabolic network model: Multispecies Metabolic Network Modeling of N ₂ O Production in Nitrifying Mixed Cultures Perez-Garcia, Octavio; Chandran, Kartik; Villas-Boas, Silas G. Biotechnology and Bioengineering, Vol. 113, Issue 5 https://doi.org/10.1002/bit.25880	journal	November 2015
Advances in flux balance analysis Kauffman, Kenneth J.; Prakash, Purusharth; Edwards, Jeremy S. Current Opinion in Biotechnology, Vol. 14, Issue 5 https://doi.org/10.1016/j.copbio.2003.08.001	journal	October 2003
Nitrous Oxide: No Laughing Matter Wuebbles, D. J. Science, Vol. 326, Issue 5949 https://doi.org/10.1126/science.1179571	journal	October 2009
Mechanisms and Specific Directionality of Autotrophic Nitrous Oxide and Nitric Oxide Generation during Transient Anoxia Yu, Ran; Kampschreur, Marlies J.; Loosdrecht, Mark C. M. van Environmental Science & Technology, Vol. 44, Issue 4 https://doi.org/10.1021/es902794a	journal	February 2010
Clarifying the regulation of NO/N2O production in Nitrosomonas europaea during anoxic–oxic transition via flux balance analysis of a metabolic network model Perez-Garcia, Octavio; Villas-Boas, Silas G.; Swift, Simon Water Research, Vol. 60 https://doi.org/10.1016/j.watres.2014.04.049	journal	September 2014
Strategies of aerobic ammonia-oxidizing bacteria for coping with nutrient and oxygen fluctuations: Strategies of AOB for coping with nutrient and oxygen fluctuations Geets, Joke; Boon, Nico; Verstraete, Willy FEMS Microbiology Ecology, Vol. 58, Issue 1 https://doi.org/10.1111/j.1574-6941.2006.00170.x	journal	October 2006
Energy conservation in Nitrobacter Freitag, A.; Bock, E. FEMS Microbiology Letters, Vol. 66, Issue 1-3 https://doi.org/10.1111/j.1574-6968.1990.tb03989.x	journal	January 1990
N2O production rate of an enriched ammonia-oxidising bacteria culture exponentially correlates to its ammonia oxidation rate Law, Yingyu; Ni, Bing-Jie; Lant, Paul Water Research, Vol. 46, Issue 10 https://doi.org/10.1016/j.watres.2012.03.043	journal	June 2012
A consilience model to describe N ₂ O production during biological N removal Domingo-Félez, C.; Smets, B. F. Environmental Science: Water Research & Technology, Vol. 2, Issue 6 https://doi.org/10.1039/C6EW00179C	journal	January 2016
Regulation of Gene Expression in Flux Balance Models of Metabolism Covert, Markus W.; Schilling, Christophe H.; Palsson, Bernhard Journal of Theoretical Biology, Vol. 213, Issue 1 https://doi.org/10.1006/jtbi.2001.2405	journal	November 2001
Complete Genome Sequence of Nitrosospira multiformis, an Ammonia-Oxidizing Bacterium from the Soil Environment Norton, J. M.; Klotz, M. G.; Stein, L. Y. Applied and Environmental Microbiology, Vol. 74, Issue 11 https://doi.org/10.1128/AEM.02722-07	journal	April 2008
Alternative Methods for Measuring Inorganic, Organic, and Total Dissolved Nitrogen in Soil Hood-Nowotny, Rebecca; Umana, Nina Hinko-Najera; Inselbacher, Erich Soil Science Society of America Journal, Vol. 74, Issue 3 https://doi.org/10.2136/sssaj2009.0389	journal	January 2010
Genome-scale modeling for metabolic engineering Simeonidis, Evangelos; Price, Nathan D. Journal of Industrial Microbiology & Biotechnology, Vol. 42, Issue 3 https://doi.org/10.1007/s10295-014-1576-3	journal	January 2015
Challenges in microbial ecology: Building predictive understanding of community function and dynamics Unknown, (:Unkn) My University https://doi.org/10.34944/dspace/5051	text	January 2016
Reconstruction and analysis of a genome-scale metabolic model for Scheffersomyces stipitis Balagurunathan, Balaji; Jonnalagadda, Sudhakar; Tan, Lily Microbial Cell Factories, Vol. 11, Issue 1 https://doi.org/10.1186/1475-2859-11-27	journal	January 2012
Revision of N ₂ O-Producing Pathways in the Ammonia-Oxidizing Bacterium Nitrosomonas europaea ATCC 19718 Kozlowski, Jessica A.; Price, Jennifer; Stein, Lisa Y. Applied and Environmental Microbiology, Vol. 80, Issue 16 https://doi.org/10.1128/AEM.01061-14	journal	June 2014
Nitric oxide and nitrous oxide turnover in natural and engineered microbial communities: biological pathways, chemical reactions, and novel technologies Schreiber, Frank; Wunderlin, Pascal; Udert, Kai M. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00372	journal	January 2012
N2O emission hotspots at different spatial scales and governing factors for small scale hotspots van den Heuvel, R. N.; Hefting, M. M.; Tan, N. C. G. Science of The Total Environment, Vol. 407, Issue 7 https://doi.org/10.1016/j.scitotenv.2008.11.010	journal	March 2009
Challenges in microbial ecology: building predictive understanding of community function and dynamics. Widder, Stefanie; Allen, Rosalind J.; Allen, Rosalind J. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.10735	text	January 2016
Effects of temperature on nitrous oxide (N2O) emission from intensive aquaculture system Paudel, Shukra Raj; Choi, Ohkyung; Khanal, Samir Kumar Science of The Total Environment, Vol. 518-519 https://doi.org/10.1016/j.scitotenv.2015.02.076	journal	June 2015
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
A protocol for generating a high-quality genome-scale metabolic reconstruction Thiele, Ines; Palsson, Bernhard Ø Nature Protocols, Vol. 5, Issue 1 https://doi.org/10.1038/nprot.2009.203	journal	January 2010
Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions Galloway, J. N.; Townsend, A. R.; Erisman, J. W. Science, Vol. 320, Issue 5878 https://doi.org/10.1126/science.1136674	journal	May 2008
Nitrosomonas europaea adaptation to anoxic-oxic cycling: Insights from transcription analysis, proteomics and metabolic network modeling Yu, Ran; Perez-Garcia, Octavio; Lu, Huijie Science of The Total Environment, Vol. 615 https://doi.org/10.1016/j.scitotenv.2017.09.142	journal	February 2018
The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes Overbeek, R. Nucleic Acids Research, Vol. 33, Issue 17 https://doi.org/10.1093/nar/gki866	journal	September 2005
Expression of nitrite reductase in Nitrosomonas europaea involves NsrR, a novel nitrite-sensitive transcription repressor: NsrR regulation of NirK expression in N. europaea Beaumont, Hubertus J. E.; Lens, Sylvia I.; Reijnders, Willem N. M. Molecular Microbiology, Vol. 54, Issue 1 https://doi.org/10.1111/j.1365-2958.2004.04248.x	journal	July 2004
Complete nitrification by Nitrospira bacteria Daims, Holger; Lebedeva, Elena V.; Pjevac, Petra Nature, Vol. 528, Issue 7583 https://doi.org/10.1038/nature16461	journal	November 2015
Nitric oxide and nitrous oxide turnover in natural and engineered microbial communities: biological pathways, chemical reactions, and novel technologies Schreiber, Frank; Wunderlin, Pascal; Udert, Kai M. ETH Zurich https://doi.org/10.3929/ethz-b-000059567	text	January 2012
Modelling nitrous and nitric oxide emissions by autotrophic ammonia-oxidizing bacteria Mampaey, K. E.; Beuckels, B.; Kampschreur, M. J. Taylor & Francis https://doi.org/10.6084/m9.figshare.825416.v1	text	January 2013
Bidirectional Catalysis by Copper-Containing Nitrite Reductase ^† Wijma, Hein J.; Canters, Gerard W.; de Vries, Simon Biochemistry, Vol. 43, Issue 32 https://doi.org/10.1021/bi0496687	journal	August 2004
Growth of Nitrobacter by dissimilatoric nitrate reduction Freitag, Annette; Rudert, Michael; Bock, Eberhard FEMS Microbiology Letters, Vol. 48, Issue 1-2 https://doi.org/10.1111/j.1574-6968.1987.tb02524.x	journal	December 1987
Nitrosomonas europaea cytochrome P460 is a direct link between nitrification and nitrous oxide emission Caranto, Jonathan D.; Vilbert, Avery C.; Lancaster, Kyle M. Proceedings of the National Academy of Sciences, Vol. 113, Issue 51 https://doi.org/10.1073/pnas.1611051113	journal	November 2016
Complete nitrification by a single microorganism van Kessel, Maartje A. H. J.; Speth, Daan R.; Albertsen, Mads Nature, Vol. 528, Issue 7583 https://doi.org/10.1038/nature16459	journal	November 2015
A genome‐scale metabolic reconstruction for Escherichia coli K‐12 MG1655 that accounts for 1260 ORFs and thermodynamic information Feist, Adam M.; Henry, Christopher S.; Reed, Jennifer L. Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100155	journal	January 2007
Fixation of N ₂ ¹⁵ by Excised Nodules. Magee, Wayne E.; Burris, R. H. Plant Physiology, Vol. 29, Issue 2 https://doi.org/10.1104/pp.29.2.199	journal	March 1954
Challenges in microbial ecology: building predictive understanding of community function and dynamics Widder, Stefanie; Allen, Rosalind J.; Pfeiffer, Thomas The ISME Journal, Vol. 10, Issue 11 https://doi.org/10.1038/ismej.2016.45	journal	March 2016
Acidity and organic matter promote abiotic nitric oxide production in drying soils Homyak, Peter M.; Kamiyama, Matthew; Sickman, James O. Global Change Biology, Vol. 23, Issue 4 https://doi.org/10.1111/gcb.13507	journal	September 2016
Molecular and Kinetic Characterization of Planktonic Nitrospira spp. Selectively Enriched from Activated Sludge Park, Mee-Rye; Park, Hongkeun; Chandran, Kartik Environmental Science & Technology, Vol. 51, Issue 5 https://doi.org/10.1021/acs.est.6b05184	journal	February 2017
Steady-State Growth under Inorganic Carbon Limitation Conditions Increases Energy Consumption for Maintenance and Enhances Nitrous Oxide Production in Nitrosomonas europaea Mellbye, Brett L.; Giguere, Andrew; Chaplen, Frank Applied and Environmental Microbiology, Vol. 82, Issue 11 https://doi.org/10.1128/AEM.00294-16	journal	March 2016
Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments Zhuang, Kai; Izallalen, Mounir; Mouser, Paula The ISME Journal, Vol. 5, Issue 2 https://doi.org/10.1038/ismej.2010.117	journal	July 2010
Applications of genome‐scale metabolic reconstructions Oberhardt, Matthew A.; Palsson, Bernhard Ø; Papin, Jason A. Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2009.77	journal	January 2009
Expression of a putative nitrite reductase and the reversible inhibition of nitrite-dependent respiration by nitric oxide in Nitrobacter winogradskyi Nb-255 Starkenburg, Shawn R.; Arp, Daniel J.; Bottomley, Peter J. Environmental Microbiology, Vol. 10, Issue 11 https://doi.org/10.1111/j.1462-2920.2008.01763.x	journal	November 2008
Modelling nitrous and nitric oxide emissions by autotrophic ammonia-oxidizing bacteria Mampaey, K. E.; Beuckels, B.; Kampschreur, M. J. Environmental Technology, Vol. 34, Issue 12 https://doi.org/10.1080/09593330.2012.758666	journal	June 2013
Distinctive NO and N 2 O emission patterns in ammonia oxidizing bacteria: Effect of ammonia oxidation rate, DO and pH Ribera-Guardia, Anna; Pijuan, Maite Chemical Engineering Journal, Vol. 321 https://doi.org/10.1016/j.cej.2017.03.122	journal	August 2017
Heterotrophic nitrification in samples from natural environments Verstraete, W.; Alexander, M. Die Naturwissenschaften, Vol. 59, Issue 2 https://doi.org/10.1007/BF00593473	journal	February 1972
SBMLToolbox: an SBML toolbox for MATLAB users Keating, S. M.; Bornstein, B. J.; Finney, A. Bioinformatics, Vol. 22, Issue 10 https://doi.org/10.1093/bioinformatics/btl111	journal	March 2006
Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota Kozlowski, Jessica A.; Stieglmeier, Michaela; Schleper, Christa The ISME Journal, Vol. 10, Issue 8 https://doi.org/10.1038/ismej.2016.2	journal	February 2016
Characterizing the Metabolic Trade-Off in Nitrosomonas europaea in Response to Changes in Inorganic Carbon Supply Jiang, D.; Khunjar, W. O.; Wett, B. Environmental Science & Technology, Vol. 49, Issue 4 https://doi.org/10.1021/es5043222	journal	January 2015
Growth at Low Ammonium Concentrations and Starvation Response as Potential Factors Involved in Niche Differentiation among Ammonia-Oxidizing Bacteria Bollmann, Annette; Bär-Gilissen, Marie-José; Laanbroek, Hendrikus J. Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/AEM.68.10.4751-4757.2002	journal	October 2002
Production of NO and N(inf2)O by Pure Cultures of Nitrifying and Denitrifying Bacteria during Changes in Aeration. Kester, R. A.; De Boer, W.; Laanbroek, H. J. Applied and environmental microbiology, Vol. 63, Issue 10 https://doi.org/10.1128/AEM.63.10.3872-3877.1997	journal	January 1997
LibSBML: an API Library for SBML Bornstein, B. J.; Keating, S. M.; Jouraku, A. Bioinformatics, Vol. 24, Issue 6 https://doi.org/10.1093/bioinformatics/btn051	journal	February 2008
Complete Genome Sequence of the Ammonia-Oxidizing Bacterium and Obligate Chemolithoautotroph Nitrosomonas europaea Chain, P.; Lamerdin, J.; Larimer, F. Journal of Bacteriology, Vol. 185, Issue 9 https://doi.org/10.1128/JB.185.9.2759-2773.2003	journal	May 2003
Nitrous Oxide - No Laughing Matter? Brandt, L. The Thoracic and Cardiovascular Surgeon, Vol. 38, Issue 02 https://doi.org/10.1055/s-2007-1013998	journal	April 1990
Modelling nitrous and nitric oxide emissions by autotrophic ammonia-oxidizing bacteria Mampaey, K. E.; Beuckels, B.; Kampschreur, M. J. Taylor & Francis https://doi.org/10.6084/m9.figshare.825416	text	January 2013

Cited By (1)

Transcriptomic Response of Nitrosomonas europaea Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth Sedlacek, Christopher J.; Giguere, Andrew T.; Dobie, Michael D. mSystems, Vol. 5, Issue 1 https://doi.org/10.1128/msystems.00562-19	journal	January 2020

Similar Records

Quorum Quenching of Nitrobacter winogradskyi Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification

Journal Article · Wed Nov 02 00:00:00 EDT 2016 · mBio · OSTI ID:1626174

Mellbye, Brett L.; Giguere, Andrew T.; Bottomley, Peter J.; +2 more

Transcriptomic Response of Nitrosomonas europaea Transitioned from Ammonia- to Oxygen-Limited Steady-State Growth

Journal Article · Tue Jan 14 00:00:00 EST 2020 · mSystems · OSTI ID:1626174

Sedlacek, Christopher J.; Giguere, Andrew T.; Dobie, Michael D.; +8 more

Activity-Based Protein Profiling of Ammonia Monooxygenase in Nitrosomonas europaea

Journal Article · Fri Jan 29 00:00:00 EST 2016 · Applied and Environmental Microbiology · OSTI ID:1626174

Bennett, Kristen; Sadler, Natalie C.; Wright, Aaron T.; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
microbiology
Nitrobacter winogradskyi
Nitrosomonas europaea
genome-scale
hydroxylamine
metabolic modeling
nitric oxide
nitrification
nitrous oxide

Title: Genome-Scale, Constraint-Based Modeling of Nitrogen Oxide Fluxes during Coculture of Nitrosomonas europaea and Nitrobacter winogradskyi

Citation Formats

References (67)

Cited By (1)

Similar Records

Related Subjects