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Title: A genome-scale metabolic model for the denitrifying bacterium Thauera sp. MZ1T accurately predicts degradation of pollutants and production of polymers

Journal Article · · PLoS Computational Biology (Online)

The denitrifying bacterium Thauera sp . MZ1T, a common member of microbial communities in wastewater treatment facilities, can produce different compounds from a range of carbon (C) and nitrogen (N) sources under aerobic and anaerobic conditions. In these different conditions, Thauera modifies its metabolism to produce different compounds that influence the microbial community. In particular, Thauera sp . MZ1T produces different exopolysaccharides with floc-forming properties, impacting the physical disposition of wastewater consortia and the efficiency of nutrient assimilation by the microbial community. Under N-limiting conditions, Thauera sp . MZ1T decreases its growth rate and accelerates the accumulation of polyhydroxyalkanoate-related (PHA) compounds including polyhydroxybutyrate (PHB), which plays a fundamental role as C and energy storage in this β-proteobacterium. However, the metabolic mechanisms employed by Thauera sp . MZ1T to assimilate and catabolize many of the different C and N sources under aerobic and anaerobic conditions remain unknown. Systems biology approaches such as genome-scale metabolic modeling have been successfully used to unveil complex metabolic mechanisms for various microorganisms. Here, we developed a comprehensive metabolic model (M-model) for Thauera sp . MZ1T ( i Thauera861), consisting of 1,744 metabolites, 2,384 reactions, and 861 genes. We validated the model experimentally using over 70 different C and N sources under both aerobic and anaerobic conditions. i Thauera861 achieved a prediction accuracy of 95% for growth on various C and N sources and close to 85% for assimilation of aromatic compounds under denitrifying conditions. The M-model was subsequently deployed to determine the effects of substrates, oxygen presence, and the C:N ratio on the production of PHB and exopolysaccharides (EPS), showing the highest polymer yields are achieved with nucleotides and amino acids under aerobic conditions. This comprehensive M-model will help reveal the metabolic processes by which this ubiquitous species influences communities in wastewater treatment systems and natural environments.

Sponsoring Organization:
USDOE
Grant/Contract Number:
AC36-08GO28308; SC0021234
OSTI ID:
2503550
Journal Information:
PLoS Computational Biology (Online), Journal Name: PLoS Computational Biology (Online) Journal Issue: 1 Vol. 21; ISSN 1553-7358
Publisher:
Public Library of Science (PLoS)Copyright Statement
Country of Publication:
United States
Language:
English

References (69)

Inhibition and gene expression of Nitrosomonas europaea biofilms exposed to phenol and toluene journal November 2010
Structure of Catechol 2,3-Dioxygenase Gene Encoded in Chromosomal DNA ofPseudomonas putidaKF715 journal July 1996
Structure of Catechol 2,3-Dioxygenase Gene fromAlcaligenes eutrophus335 journal April 1998
The Family Rhodocyclaceae book January 2014
Phylogenetic and metabolic diversity of bacteria degrading aromatic compounds under denitrifying conditions, and description of Thauera phenylacetica sp. nov., Thauera aminoaromatica sp. nov., and Azoarcus buckelii sp. nov. journal July 2002
Two distinct pathways for anaerobic degradation of aromatic compounds in the denitrifying bacterium Thauera aromatica strain AR-1 journal December 1999
Reconstructing a Thauera genome from a hydrogenotrophic-denitrifying consortium using metagenomic sequence data journal April 2014
Versatile aromatic compound-degrading capacity and microdiversity of Thauera strains isolated from a coking wastewater treatment bioreactor journal May 2010
Production of poly-β-hydroxybutyrate by activated sludge in sequencing batch reactor under aerobic conditions journal June 2017
Effect of Cycle Time on Polyhydroxybutyrate (PHB) Production in Aerobic Mixed Cultures journal January 2014
Creating a synthetic lichen: Mutualistic co-culture of fungi and extracellular polysaccharide-secreting cyanobacterium Nostoc PCC 7413 journal January 2020
Formation of aerobic granules and their PHB production at various substrate and ammonium concentrations journal January 2009
Rhodopseudomonas palustris CGA009 polyhydroxybutyrate production from a lignin aromatic and quantification via flow cytometry journal September 2020
Complete nitrogen removal and electricity production in Thauera-dominated air-cathode single chambered microbial fuel cell journal January 2019
Tracking multiple aromatic compounds in a full-scale coking wastewater reclamation plant: Interaction with biological and advanced treatments journal May 2019
Molecular mechanisms through which different carbon sources affect denitrification by Thauera linaloolentis: Electron generation, transfer, and competition journal December 2022
Dissimilatory nitrate/nitrite reduction to ammonium (DNRA) pathway dominates nitrate reduction processes in rhizosphere and non-rhizosphere of four fertilized farmland soil journal July 2020
Exopolysaccharide production by the marine bacterium Alteromonas macleodii Mo169 using fruit pulp waste as the sole carbon source journal May 2023
Optimization of polyhydroxybutyrate (PHB) production by excess activated sludge and microbial community analysis journal January 2011
Production of poly-β-hydroxybutyrate (PHB) by Methylobacterium organophilum isolated from a methanotrophic consortium in a two-phase partition bioreactor journal June 2011
Effect of C/N ratio on the PHA accumulation capability of microbial mixed culture fed with leachates from the organic fraction of municipal solid waste (OFMSW) journal April 2021
Modeling of nitrogen fixation and polymer production in the heterotrophic diazotroph Azotobacter vinelandii DJ journal December 2020
Thauera sp. Sel9, a new bacterial strain for polyhydroxyalkanoates production from volatile fatty acids journal December 2022
The impact of carbon to nitrogen ratios and pH on the microbial prevalence and polyhydroxybutyrate production levels using a mixed microbial starter culture journal March 2022
Influence of the C/N ratio on the performance of polyhydroxybutyrate (PHB) producing sequencing batch reactors at short SRTs journal April 2010
Aromatic compounds lead to increased abundance of antibiotic resistance genes in wastewater treatment bioreactors journal December 2019
Genetic potential for exopolysaccharide synthesis in activated sludge bacteria uncovered by genome-resolved metagenomics journal February 2023
Global Patterns and Drivers of Soil Dissimilatory Nitrate Reduction to Ammonium journal February 2022
Physiological and Transcriptional Responses of Nitrosomonas europaea to Toluene and Benzene Inhibition journal June 2008
What is flux balance analysis? journal March 2010
iML1515, a knowledgebase that computes Escherichia coli traits journal October 2017
KBase: The United States Department of Energy Systems Biology Knowledgebase journal July 2018
Linking metabolic phenotypes to pathogenic traits among “Candidatus Liberibacter asiaticus” and its hosts journal August 2020
Creation and analysis of biochemical constraint-based models using the COBRA Toolbox v.3.0 journal February 2019
Biomineralization of selenium by the selenate-respiring bacterium Thauera selenatis journal November 2012
The BioCyc collection of microbial genomes and metabolic pathways journal August 2017
KEGG: Kyoto Encyclopedia of Genes and Genomes journal January 2000
BRENDA, the ELIXIR core data resource in 2021: new developments and updates journal November 2020
UniProt: the universal protein knowledgebase in 2021 journal November 2020
The ModelSEED Biochemistry Database for the integration of metabolic annotations and the reconstruction, comparison and analysis of metabolic models for plants, fungi and microbes journal September 2020
MetaNetX/MNXref: unified namespace for metabolites and biochemical reactions in the context of metabolic models journal November 2020
PubChem 2023 update journal October 2022
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases journal November 2013
BiGG Models: A platform for integrating, standardizing and sharing genome-scale models journal October 2015
Improvements to PATRIC, the all-bacterial Bioinformatics Database and Analysis Resource Center journal November 2016
TransportDB 2.0: a database for exploring membrane transporters in sequenced genomes from all domains of life journal November 2016
Genome-Scale Metabolic Model for the Green Alga Chlorella vulgaris UTEX 395 Accurately Predicts Phenotypes under Autotrophic, Heterotrophic, and Mixotrophic Growth Conditions journal July 2016
Strains in the genus Thauera exhibit remarkably different denitrification regulatory phenotypes journal May 2013
Food waste conversion to microbial polyhydroxyalkanoates journal July 2017
Analysis and glycosyl composition of the exopolysaccharide isolated from the floc-forming wastewater bacterium Thauera sp. MZ1T journal August 2004
Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway journal December 1998
Flocculation-Related Gene Identification by Whole-Genome Sequencing of Thauera aminoaromatica MZ1T Floc-Defective Mutants journal December 2015
The Role of Benzoate in Anaerobic Degradation of Terephthalate journal March 1999
An Experimentally Validated Genome-Scale Metabolic Reconstruction of Klebsiella pneumoniae MGH 78578, iYL1228 journal February 2011
Physically associated enzymes produce and metabolize 2-hydroxy-2,4-dienoate, a chemically unstable intermediate formed in catechol metabolism via meta cleavage in Pseudomonas putida. journal November 1989
Anaerobic degradation of 2-aminobenzoic acid (anthranilic acid) via benzoyl-coenzyme A (CoA) and cyclohex-1-enecarboxyl-CoA in a denitrifying bacterium journal June 1992
BLAST+: architecture and applications journal January 2009
A genome-scale metabolic reconstruction of Pseudomonas putida KT2440: iJN746 as a cell factory journal January 2008
Constraint-Based Modeling of Carbon Fixation and the Energetics of Electron Transfer in Geobacter metallireducens journal April 2014
RAVEN 2.0: A versatile toolbox for metabolic network reconstruction and a case study on Streptomyces coelicolor journal October 2018
Flux balance analysis of the ammonia-oxidizing bacterium Nitrosomonas europaea ATCC19718 unravels specific metabolic activities while degrading toxic compounds journal February 2022
The genome-scale metabolic model for the purple non-sulfur bacterium Rhodopseudomonas palustris Bis A53 accurately predicts phenotypes under chemoheterotrophic, chemoautotrophic, photoheterotrophic, and photoautotrophic growth conditions journal August 2023
Optimization of exopolysaccharide production by response surface methodology from Enterococcus faecium isolated from the fermented foods of Western Himalaya journal August 2019
Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies journal May 2015
Thauera aminoaromatica MZ1T Identified as a Polyhydroxyalkanoate-Producing Bacterium within a Mixed Microbial Consortium journal February 2020
Genome-Scale Metabolic Modeling Enables In-Depth Understanding of Big Data journal December 2021
Role of Exopolysaccharides of Pseudomonas in Heavy Metal Removal and Other Remediation Strategies journal October 2022
Recent Advances in the Production of Exopolysaccharide (EPS) from Lactobacillus spp. and Its Application in the Food Industry: A Review journal November 2021
Complete genome sequence of Thauera aminoaromatica strain MZ1T journal July 2012