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Title: Metabolic regulation as a consequence of anaerobic 5-methylthioadenosine recycling in Rhodospirillum rubrum

Journal Article · · mBio (Online)
 [1];  [1];  [2];  [1];  [3];  [1];  [2];  [1]
  1. The Ohio State Univ., Columbus, OH (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Univ. of Tennessee, Knoxville, TN (United States). ORNL Graduate School of Genome Science and Tech.
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Rhodospirillum rubrum possesses a novel oxygen-independent, aerobic methionine salvage pathway (MSP) for recycling methionine from 5-methylthioadenosine (MTA), the MTA-isoprenoid shunt. This organism can also metabolize MTA as a sulfur source under anaerobic conditions, suggesting that the MTA-isoprenoid shunt may also function anaerobically as well. In this study, deep proteomics profiling, directed metabolite analysis, and reverse transcriptase quantitative PCR (RT-qPCR) revealed metabolic changes in response to anaerobic growth on MTA versus sulfate as sole sulfur source. The abundance of protein levels associated with methionine transport, cell motility, and chemotaxis increased in the presence of MTA over that in the presence of sulfate. Purine salvage from MTA resulted primarily in hypoxanthine accumulation and a decrease in protein levels involved in GMP-to-AMP conversion to balance purine pools. Acyl coenzyme A (acyl-CoA) metabolic protein levels for lipid metabolism were lower in abundance, whereas poly-β-hydroxybutyrate synthesis and storage were increased nearly 10-fold. The known R. rubrum aerobic MSP was also shown to be upregulated, to function anaerobically, and to recycle MTA. This suggested that other organisms with gene homologues for the MTA-isoprenoid shunt may also possess a functioning anaerobic MSP. In support of our previous findings that ribulose-1,5-carboxylase/oxygenase (RubisCO) is required for an apparently purely anaerobic MSP, RubisCO transcript and protein levels both increased in abundance by over 10-fold in cells grown anaerobically on MTA over those in cells grown on sulfate, resulting in increased intracellular RubisCO activity. Lastly, these results reveal for the first time global metabolic responses as a consequence of anaerobic MTA metabolism compared to using sulfate as the sulfur source.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1326542
Journal Information:
mBio (Online), Vol. 7, Issue 4; ISSN 2150-7511
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 11 works
Citation information provided by
Web of Science

References (53)

Mechanism of action of 5'-methylthioadenosine in S49 cells journal November 1984
Function, Structure, and Evolution of the RubisCO-Like Proteins and Their RubisCO Homologs journal December 2007
STRING v10: protein–protein interaction networks, integrated over the tree of life journal October 2014
Metabolic characteristics and importance of the universal methionine salvage pathway recycling methionine from 5′-methylthioadenosine journal December 2009
Precision and Kinetics of Adaptation in Bacterial Chemotaxis journal November 2010
A Rubisco Mutant That Confers Growth under a Normally “Inhibitory” Oxygen Concentration journal September 2009
Assay of Poly-β-Hydroxybutyric acid journal January 1961
Accumulation of the PhaP Phasin of Ralstonia eutropha Is Dependent on Production of Polyhydroxybutyrate in Cells journal July 2001
Structural Analysis of Bacterial Chemotaxis Proteins: Components of a Dynamic Signaling System journal December 1998
A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress journal April 2001
Analyzing real-time PCR data by the comparative CT method journal June 2008
The metNPQ operon of Bacillus subtilis encodes an ABC permease transporting methionine sulfoxide, d- and l-methionine journal March 2004
Regulating the production of (R)-3-hydroxybutyrate in Escherichia coli by N or P limitation journal August 2015
Integration of untargeted metabolomics with transcriptomics reveals active metabolic pathways journal August 2014
CheB is required for behavioural responses to negative stimuli during chemotaxis in Bacillus subtilis journal January 2000
RuBisCO-like proteins as the enolase enzyme in the methionine salvage pathway: functional and evolutionary relationships between RuBisCO-like proteins and photosynthetic RuBisCO journal June 2007
Complementation analysis and regulation of CO2 fixation gene expression in a ribulose 1,5-bisphosphate carboxylase-oxygenase deletion strain of Rhodospirillum rubrum. journal August 1993
Coupling a Detergent Lysis/Cleanup Methodology with Intact Protein Fractionation for Enhanced Proteome Characterization journal October 2012
Direct Cellular Lysis/Protein Extraction Protocol for Soil Metaproteomics journal December 2010
Mechanistic Diversity in the RuBisCO Superfamily: A Novel Isomerization Reaction Catalyzed by the RuBisCO-like Protein from Rhodospirillum rubrum † journal October 2008
A Functional Link Between RuBisCO-like Protein of Bacillus and Photosynthetic RuBisCO journal October 2003
Observations on the metabolism of 5′-methylthioadenosine journal January 1964
Unraveling the Function of the Rhodospirillum rubrum Activator of Polyhydroxybutyrate (PHB) Degradation: the Activator Is a PHB-Granule-Bound Protein (Phasin) journal April 2004
The methionine salvage pathway in Bacillus subtilis journal January 2002
Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria journal September 2002
Inward facing conformations of the MetNI methionine ABC transporter: Implications for the mechanism of transinhibition: Inward Facing Conformations of the MetNI ABC Transporter journal December 2011
1-Methylthio- d -xylulose 5-Phosphate Methylsulfurylase: A Novel Route to 1-Deoxy- d -xylulose 5-Phosphate in Rhodospirillum rubrum journal October 2012
A method of preparing agarose journal April 1964
Structural and Functional Similarities between a Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (RuBisCO)-like Protein from Bacillus subtilis and Photosynthetic RuBisCO journal March 2009
MtnBD Is a Multifunctional Fusion Enzyme in the Methionine Salvage Pathway of Tetrahymena thermophila journal July 2013
A Common Transport System for Methionine, l-methionine-dl-Sulfoximine (MSX), and Phosphinothricin (PPT) in the Diazotrophic Cyanobacterium Nostoc muscorum journal February 2008
DTASelect and Contrast:  Tools for Assembling and Comparing Protein Identifications from Shotgun Proteomics journal February 2002
Identification of yrrU as the Methylthioadenosine Nucleosidase Gene in Bacillus subtilis journal January 1999
Structure and Function of the Bi-Directional Bacterial Flagellar Motor journal February 2014
Methylthioadenosine toxicity and metabolism to methionine in mammalian cells journal October 1988
Chemotaxis signaling protein CheY binds to the rotor protein FliN to control the direction of flagellar rotation in Escherichia coli journal May 2010
Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms journal May 2008
A RubisCO-like protein links SAM metabolism with isoprenoid biosynthesis journal October 2012
Insights into the stress response and sulfur metabolism revealed by proteome analysis of a Chlorobium tepidum mutant lacking the Rubisco-like protein journal January 2003
Poly(3-hydroxybutyrate) Granule-Associated Proteins:  Impacts on Poly(3-hydroxybutyrate) Synthesis and Degradation † journal March 2005
Targeting tumors that lack methylthioadenosine phosphorylase (MTAP) activity: Current strategies journal April 2011
Inhibition of cytokine production and endothelial expression of adhesion antigens by 5′-methylthioadenosine journal March 1993
Mechanistic Diversity in the RuBisCO Superfamily:  The “Enolase” in the Methionine Salvage Pathway in Geobacillus kaustophilus † , ‡ journal April 2007
Methylthioadenosine phosphorylase gene expression is impaired in human liver cirrhosis and hepatocarcinoma journal November 2004
In Vivo Studies in Rhodospirillum rubrum Indicate That Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (Rubisco) Catalyzes Two Obligatorily Required and Physiologically Significant Reactions for Distinct Carbon and Sulfur Metabolic Pathways journal October 2015
PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes journal May 2010
A Phasin with Many Faces: Structural Insights on PhaP from Azotobacter sp. FA8 journal July 2014
PhaP phasins play a principal role in poly-β-hydroxybutyrate accumulation in free-living Bradyrhizobium japonicum journal January 2013
The Poor Growth of Rhodospirillum rubrum Mutants Lacking RubisCO Is Due to the Accumulation of Ribulose-1,5-Bisphosphate journal April 2011
Roles of RubisCO and the RubisCO-Like Protein in 5-Methylthioadenosine Metabolism in the Nonsulfur Purple Bacterium Rhodospirillum rubrum journal December 2009
Complete genome sequence of Rhodospirillum rubrum type strain (S1T) journal June 2011
Methylthioadenosine/S-adenosylhomocysteine nucleosidase, a critical enzyme for bacterial metabolism: Involvement of MTA/SAH nucleosidase in bacterial metabolism journal November 2010
Dynamic motors for bacterial flagella journal June 2010

Cited By (3)

Revisiting the methionine salvage pathway and its paralogues journal October 2018
Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea journal August 2017
Comparative genomic inference suggests mixotrophic lifestyle for Thorarchaeota journal February 2018

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