Carbohydrate Metabolism and Carbon Fixation in Roseobacter denitrificans OCh114

Tang, Kuo-Hsiang; Feng, Xueyang; Tang, Yinjie J.; Blankenship, Robert E.

doi:10.1371/journal.pone.0007233

Title: Carbohydrate Metabolism and Carbon Fixation in Roseobacter denitrificans OCh114

Journal Article · Thu Oct 01 00:00:00 EDT 2009 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0007233· OSTI ID:1904750

Tang, Kuo-Hsiang ^[1]; Feng, Xueyang ^[1]; Tang, Yinjie J. ^[1]; Blankenship, Robert E. ^[1]

Washington Univ., St. Louis, MO (United States)

The Roseobacter clade of aerobic marine proteobacteria, which compose 10–25% of the total marine bacterial community, has been reported to fix CO₂, although it has not been determined what pathway is involved. In this study, we report the first metabolic studies on carbohydrate utilization, CO₂ assimilation, and amino acid biosynthesis in the phototrophic Roseobacter clade bacterium Roseobacter denitrificans OCh114. We develop a new minimal medium containing defined carbon source(s), in which the requirements of yeast extract reported previously for the growth of R. denitrificans can be replaced by vitamin B₁₂ (cyanocobalamin). Tracer experiments were carried out in R. denitrificans grown in a newly developed minimal medium containing isotopically labeled pyruvate, glucose or bicarbonate as a single carbon source or in combination. Through measurements of ¹³C-isotopomer labeling patterns in protein-derived amino acids, gene expression profiles, and enzymatic activity assays, we report that: (1) R. denitrificans uses the anaplerotic pathways mainly via the malic enzyme to fix 10–15% of protein carbon from CO₂; (2) R. denitrificans employs the Entner-Doudoroff (ED) pathway for carbohydrate metabolism and the non-oxidative pentose phosphate pathway for the biosynthesis of histidine, ATP, and coenzymes; (3) the Embden-Meyerhof-Parnas (EMP, glycolysis) pathway is not active and the enzymatic activity of 6-phosphofructokinase (PFK) cannot be detected in R. denitrificans; and (4) isoleucine can be synthesized from both threonine-dependent (20% total flux) and citramalate-dependent (80% total flux) pathways using pyruvate as the sole carbon source.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Washington Univ., St. Louis, MO (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Aeronautics and Space Administration (NASA)

Grant/Contract Number:: FG02-08ER64694

OSTI ID:: 1904750

Journal Information:: PLoS ONE, Vol. 4, Issue 10; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (49)

Effect of Sorghum vulgare phosphoenolpyruvate carboxylase and Lactococcus lactis pyruvate carboxylase coexpression on succinate production in mutant strains of Escherichia coli Lin, Henry; San, Ka-Yiu; Bennett, George N. Applied Microbiology and Biotechnology, Vol. 67, Issue 4 https://doi.org/10.1007/s00253-004-1789-x	journal	November 2004
The Mechanism of 6-Phosphogluconic Dehydrase Meloche, H. P.; Wood, W. A. Journal of Biological Chemistry, Vol. 239, Issue 10 https://doi.org/10.1016/S0021-9258(18)97751-3	journal	October 1964
Resourceful heterotrophs make the most of light in the coastal ocean Moran, Mary Ann; Miller, William L. Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1746	journal	October 2007
Purification, Regulation, and Molecular and Biochemical Characterization of Pyruvate Carboxylase from Methanobacterium thermoautotrophicum Strain ΔH Mukhopadhyay, Biswarup; Stoddard, Steven F.; Wolfe, Ralph S. Journal of Biological Chemistry, Vol. 273, Issue 9 https://doi.org/10.1074/jbc.273.9.5155	journal	February 1998
Analysis of metabolic pathways and fluxes in a newly discovered thermophilic and ethanol-tolerantGeobacillusstrain Tang, Yinjie J.; Sapra, Rajat; Joyner, Dominique Biotechnology and Bioengineering, Vol. 102, Issue 5 https://doi.org/10.1002/bit.22181	journal	April 2009
The Mechanism of 2-Keto-3-deoxy-6-phosphogluconic Aldolase Meloche, H. P.; Wood, W. A. Journal of Biological Chemistry, Vol. 239, Issue 10 https://doi.org/10.1016/S0021-9258(18)97752-5	journal	October 1964
Unsuspected diversity among marine aerobic anoxygenic phototrophs Béjà, Oded; Suzuki, Marcelino T.; Heidelberg, John F. Nature, Vol. 415, Issue 6872 https://doi.org/10.1038/415630a	journal	February 2002
Contribution of Aerobic Photoheterotrophic Bacteria to the Carbon Cycle in the Ocean Kolber, Z. S. Science, Vol. 292, Issue 5526 https://doi.org/10.1126/science.1059707	journal	June 2001
Roseobacter litoralis gen. nov., sp. nov., and Roseobacter denitrificans sp. nov., Aerobic Pink-Pigmented Bacteria which Contain Bacteriochlorophyll a Shiba, Tsuneo Systematic and Applied Microbiology, Vol. 14, Issue 2 https://doi.org/10.1016/S0723-2020(11)80292-4	journal	March 1991
Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment Moran, Mary Ann; Buchan, Alison; González, José M. Nature, Vol. 432, Issue 7019 https://doi.org/10.1038/nature03170	journal	December 2004
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford, Marion M. Analytical Biochemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/0003-2697(76)90527-3	journal	May 1976
Comparison of 16S rRNA, nifD, recA, gyrB, rpoB and fusA genes within the family Geobacteraceae fam. nov. Holmes, D. E. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 5 https://doi.org/10.1099/ijs.0.02958-0	journal	September 2004
Diversity, ecology, and genomics of the Roseobacter clade: a short overview Brinkhoff, Thorsten; Giebel, Helge-Ansgar; Simon, Meinhard Archives of Microbiology, Vol. 189, Issue 6 https://doi.org/10.1007/s00203-008-0353-y	journal	February 2008
Threonine Deaminase from Bacillus subtilis Hatfield, G. Wesley; Umbarger, H. Edwin Journal of Biological Chemistry, Vol. 245, Issue 7 https://doi.org/10.1016/S0021-9258(19)77154-3	journal	April 1970
Analysis of Amino Acid Isotopomers Using FT-ICR MS Pingitore, Francesco; Tang, Yinjie; Kruppa, Gary H. Analytical Chemistry, Vol. 79, Issue 6 https://doi.org/10.1021/ac061906b	journal	February 2007
Structure of the puf operon of the obligately aerobic, bacteriochlorophyll alpha-containing bacterium Roseobacter denitrificans OCh114 and its expression in a Rhodobacter capsulatus puf puc deletion mutant Kortlüke, C.; Breese, K.; Gad'on, N. Journal of Bacteriology, Vol. 179, Issue 17 https://doi.org/10.1128/jb.179.17.5247-5258.1997	journal	September 1997
Dinoroseobacter shibae gen. nov., sp. nov., a new aerobic phototrophic bacterium isolated from dinoflagellates Biebl, Hanno; Allgaier, Martin; Tindall, Brian J. International Journal of Systematic and Evolutionary Microbiology, Vol. 55, Issue 3 https://doi.org/10.1099/ijs.0.63511-0	journal	May 2005
Roseovarius mucosus sp. nov., a member of the Roseobacter clade with trace amounts of bacteriochlorophyll a Biebl, Hanno; Allgaier, Martin; Lünsdorf, Heinrich International Journal of Systematic and Evolutionary Microbiology, Vol. 55, Issue 6 https://doi.org/10.1099/ijs.0.63832-0	journal	November 2005
Covalent intermediate trapped in 2-keto-3-deoxy-6- phosphogluconate (KDPG) aldolase structure at 1.95-Å resolution Allard, Julie; Grochulski, Pawel; Sygusch, Jurgen Proceedings of the National Academy of Sciences, Vol. 98, Issue 7 https://doi.org/10.1073/pnas.071380898	journal	March 2001
Control of liver 6-phosphofructokinase by fructose 2,6-bisphosphate and other effectors. Van Schaftingen, E.; Jett, M. F.; Hue, L. Proceedings of the National Academy of Sciences, Vol. 78, Issue 6 https://doi.org/10.1073/pnas.78.6.3483	journal	June 1981
Optimization of three FISH procedures for in situ detection of anaerobic ammonium oxidizing bacteria in biological wastewater treatment Pavlekovic, Marko; Schmid, Markus C.; Schmider-Poignee, Nadja Journal of Microbiological Methods, Vol. 78, Issue 2 https://doi.org/10.1016/j.mimet.2009.04.003	journal	August 2009
Distribution of bacteriochlorophyll a among aerobic and acidophilic bacteria and light-enhanced CO2-incorporation in Acidiphilium rubrum Kishimoto, Noriaki; Fukaya, Fumihito; Inagaki, Kenji FEMS Microbiology Ecology, Vol. 16, Issue 4 https://doi.org/10.1111/j.1574-6941.1995.tb00293.x	journal	April 1995
Predicting synthetic rescues in metabolic networks Motter, Adilson E.; Gulbahce, Natali; Almaas, Eivind Molecular Systems Biology, Vol. 4, Issue 1 https://doi.org/10.1038/msb.2008.1	journal	January 2008
Environmental Biology of the Marine Roseobacter Lineage Wagner-Döbler, Irene; Biebl, Hanno Annual Review of Microbiology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.micro.60.080805.142115	journal	October 2006
( R )-Citramalate Synthase in Methanogenic Archaea Howell, David M.; Xu, Huimin; White, Robert H. Journal of Bacteriology, Vol. 181, Issue 1 https://doi.org/10.1128/JB.181.1.331-333.1999	journal	January 1999
Characterization of Phosphoenolpyruvate Carboxykinase from Panicum maximum Ray, Thomas B.; Black, Clanton C. Plant Physiology, Vol. 58, Issue 5 https://doi.org/10.1104/pp.58.5.603	journal	November 1976
A Simple and Accurate Spectrophotometric Assay for Phosphoenolpyruvate Carboxylase Activity Meyer, Christopher R.; Rustin, Pierre; Wedding, Randolph T. Plant Physiology, Vol. 86, Issue 2 https://doi.org/10.1104/pp.86.2.325	journal	February 1988
Amino Acid Biosynthesis and its Regulation Umbarger, H. E. Annual Review of Biochemistry, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.bi.47.070178.002533	journal	June 1978
A newly discovered Roseobacter cluster in temperate and polar oceans Selje, Natascha; Simon, Meinhard; Brinkhoff, Thorsten Nature, Vol. 427, Issue 6973 https://doi.org/10.1038/nature02272	journal	January 2004
Influence of Aerobic and Phototrophic Growth Conditions on the Distribution of Glucose and Fructose Carbon into the Entner-Doudoroff and Embden-Meyerhof Pathways in Rhodopseudomonas sphaeroides Conrad, R.; Schlegel, H. G. Journal of General Microbiology, Vol. 101, Issue 2 https://doi.org/10.1099/00221287-101-2-277	journal	August 1977
New tools for mass isotopomer data evaluation in13C flux analysis: Mass isotope correction, data consistency checking, and precursor relationships Wahl, S. Aljoscha; Dauner, Michael; Wiechert, Wolfgang Biotechnology and Bioengineering, Vol. 85, Issue 3 https://doi.org/10.1002/bit.10909	journal	January 2004
Isolation and characterization of Erythrobacter sp. strains from the upper ocean Koblížek, Michal; Béjà, Oded; Bidigare, Robert R. Archives of Microbiology, Vol. 180, Issue 5 https://doi.org/10.1007/s00203-003-0596-6	journal	September 2003
Different degradation pathways for glucose and fructose in Rhodopseudomonas capsulata Conrad, R.; Schlegel, H. G. Archives of Microbiology, Vol. 112, Issue 1 https://doi.org/10.1007/bf00446652	journal	January 1977
Determination of pyruvate in enzyme-catalyzed reactions in the presence of glyoxylate Thompson, J. S.; Richardson, K. E. Analytical Biochemistry, Vol. 24, Issue 2 https://doi.org/10.1016/0003-2697(68)90170-x	journal	August 1968
Glucose and Gluconic acid Oxidation of Pseudomonas Saccharophila Entner, Nathan; Doudoroff, Michael Journal of Biological Chemistry, Vol. 196, Issue 2 https://doi.org/10.1016/s0021-9258(19)52415-2	journal	June 1952
Cloning, isolation and characterization of the Thermotoga maritima KDPG aldolase Griffiths, Jennifer S.; Wymer, Nathan J.; Njolito, Eugenia Bioorganic & Medicinal Chemistry, Vol. 10, Issue 3 https://doi.org/10.1016/s0968-0896(01)00307-8	journal	March 2002
The oxidative pentose phosphate pathway: structure and organisation Kruger, Nicholas J.; von Schaewen, Antje Current Opinion in Plant Biology, Vol. 6, Issue 3 https://doi.org/10.1016/s1369-5266(03)00039-6	journal	June 2003
Use of 16S rRNA and rpoB Genes as Molecular Markers for Microbial Ecology Studies Case, R. J.; Boucher, Y.; Dahllof, I. Applied and Environmental Microbiology, Vol. 73, Issue 1 https://doi.org/10.1128/aem.01177-06	journal	October 2006
Ecological Genomics of Marine Roseobacters Moran, M. A.; Belas, R.; Schell, M. A. Applied and Environmental Microbiology, Vol. 73, Issue 14 https://doi.org/10.1128/aem.02580-06	journal	May 2007
Distribution of Aerobic Bacteria Which Contain Bacteriochlorophyll a Shiba, Tsuneo; Simidu, Usio; Taga, Nobuo Applied and Environmental Microbiology, Vol. 38, Issue 1 https://doi.org/10.1128/aem.38.1.43-45.1979	journal	July 1979
Expression of the Escherichia coli Catabolic Threonine Dehydratase in Corynebacterium glutamicum and Its Effect on Isoleucine Production Guillouet, S.; Rodal, A. A.; An, G. -H. Applied and Environmental Microbiology, Vol. 65, Issue 7 https://doi.org/10.1128/aem.65.7.3100-3107.1999	journal	July 1999
Overview of the Marine Roseobacter Lineage Buchan, A.; Gonzalez, J. M.; Moran, M. A. Applied and Environmental Microbiology, Vol. 71, Issue 10 https://doi.org/10.1128/aem.71.10.5665-5677.2005	journal	October 2005
Role of the AcsF Protein in Chloroflexus aurantiacus Tang, Kuo-Hsiang; Wen, Jianzhong; Li, Xianglu Journal of Bacteriology, Vol. 191, Issue 11 https://doi.org/10.1128/jb.00110-09	journal	June 2009
Pathway Confirmation and Flux Analysis of Central Metabolic Pathways in Desulfovibrio vulgaris Hildenborough using Gas Chromatography-Mass Spectrometry and Fourier Transform-Ion Cyclotron Resonance Mass Spectrometry Tang, Y.; Pingitore, F.; Mukhopadhyay, A. Journal of Bacteriology, Vol. 189, Issue 3 https://doi.org/10.1128/jb.00948-06	journal	November 2006
The Complete Genome Sequence of Roseobacter denitrificans Reveals a Mixotrophic Rather than Photosynthetic Metabolism Swingley, Wesley D.; Sadekar, Sumedha; Mastrian, Stephen D. Journal of Bacteriology, Vol. 189, Issue 3 https://doi.org/10.1128/jb.01390-06	journal	November 2006
Elucidation of an Alternate Isoleucine Biosynthesis Pathway in Geobacter sulfurreducens Risso, C.; Van Dien, S. J.; Orloff, A. Journal of Bacteriology, Vol. 190, Issue 7 https://doi.org/10.1128/jb.01841-07	journal	February 2008
Isoleucine Biosynthesis in Leptospira interrogans Serotype lai Strain 56601 Proceeds via a Threonine-Independent Pathway Xu, H.; Zhang, Y.; Guo, X. Journal of Bacteriology, Vol. 186, Issue 16, p. 5400-5409 https://doi.org/10.1128/jb.186.16.5400-5409.2004	journal	August 2004
Aerobic Anoxygenic Phototrophic Bacteria Yurkov, Vladimir V.; Beatty, J. Thomas Microbiology and Molecular Biology Reviews, Vol. 62, Issue 3 https://doi.org/10.1128/mmbr.62.3.695-724.1998	journal	September 1998
Predicting synthetic rescues in metabolic networks Motter, Adilson E.; Gulbahce, Natali; Almaas, Eivind arXiv https://doi.org/10.48550/arxiv.0803.0962	text	January 2008

Cited By (15)

Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton Garcia, Sarahi L.; McMahon, Katherine D.; Martinez-Garcia, Manuel The ISME Journal, Vol. 7, Issue 1 https://doi.org/10.1038/ismej.2012.86	journal	July 2012
The Entner-Doudoroff and Nonoxidative Pentose Phosphate Pathways Bypass Glycolysis and the Oxidative Pentose Phosphate Pathway in Ralstonia solanacearum Jyoti, Poonam; Shree, Manu; Joshi, Chandrakant mSystems, Vol. 5, Issue 2 https://doi.org/10.1128/msystems.00091-20	journal	April 2020
Metabolic flexibility revealed in the genome of the cyst-forming α-1 proteobacterium Rhodospirillum centenum Lu, Yih-Kuang; Marden, Jeremiah; Han, Mira BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-325	journal	May 2010
Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus Tang, Kuo-Hsiang; Barry, Kerrie; Chertkov, Olga BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-334	journal	June 2011
Compositional and Functional Shifts in the Epibiotic Bacterial Community of Shinkaia crosnieri Baba & Williams (a Squat Lobster from Hydrothermal Vents) during Methane-Fed Rearing Watsuji, Tomo-o; Motoki, Kaori; Hada, Emi Microbes and Environments, Vol. 33, Issue 4 https://doi.org/10.1264/jsme2.me18072	journal	January 2018
Phylogenomic Analysis of Marine Roseobacters Tang, Kai; Huang, Hongzhan; Jiao, Nianzhi PLoS ONE, Vol. 5, Issue 7 https://doi.org/10.1371/journal.pone.0011604	journal	July 2010
Diurnal Rhythms Result in Significant Changes in the Cellular Protein Complement in the Cyanobacterium Cyanothece 51142 Stöckel, Jana; Jacobs, Jon M.; Elvitigala, Thanura R. PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016680	journal	February 2011
Ubiquitous Dissolved Inorganic Carbon Assimilation by Marine Bacteria in the Pacific Northwest Coastal Ocean as Determined by Stable Isotope Probing DeLorenzo, Suzanne; Bräuer, Suzanna L.; Edgmont, Chelsea A. PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0046695	journal	October 2012
Metabolic Evolution of a Deep-Branching Hyperthermophilic Chemoautotrophic Bacterium Braakman, Rogier; Smith, Eric PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0087950	journal	February 2014
Peroxidase Activity and Involvement in the Oxidative Stress Response of Roseobacter denitrificans Truncated Hemoglobin Wang, Yaya; Barbeau, Xavier; Bilimoria, Astha PLOS ONE, Vol. 10, Issue 2 https://doi.org/10.1371/journal.pone.0117768	journal	February 2015
Carbon Metabolic Pathways in Phototrophic Bacteria and Their Broader Evolutionary Implications Tang, Kuo-Hsiang; Tang, Yinjie J.; Blankenship, Robert Eugene Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00165	journal	January 2011
Nutrient requirements and growth physiology of the photoheterotrophic Acidobacterium, Chloracidobacterium thermophilum Tank, Marcus; Bryant, Donald A. Frontiers in Microbiology, Vol. 06 https://doi.org/10.3389/fmicb.2015.00226	journal	March 2015
Metagenomic sequencing of marine periphyton: taxonomic and functional insights into biofilm communities Sanli, Kemal; Bengtsson-Palme, Johan; Nilsson, R. Henrik Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01192	journal	October 2015
Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach Lindemann, Stephen R.; Mobberley, Jennifer M.; Cole, Jessica K. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01020	journal	June 2017
Functional Signatures of the Epiphytic Prokaryotic Microbiome of Agaves and Cacti Flores-Núñez, Víctor M.; Fonseca-García, Citlali; Desgarennes, Damaris Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.03044	journal	January 2020

Similar Records

Energy transfer in an LH4-like light harvesting complex from the aerobic purple photosynthetic bacterium Roseobacter denitrificans

Journal Article · · Biochim. Biophys. Acta · OSTI ID:1904750

Niedzwiedzki, Dariusz; Fuciman, Marcel; Frank, Harry A; +1 more

Environmental proteomics of microbial plankton in a highly productive coastal upwelling system

Journal Article · Sat Jan 01 00:00:00 EST 2011 · The ISME Journal: Multidisciplinary Journal of Microbial Ecology · OSTI ID:1904750

Sowell, Sarah; Abraham, Paul E; Shah, Manesh B; +4 more

Metabolic flux analysis of the halophilic archaeon Haladaptatus paucihalophilus

Journal Article · Fri Nov 27 00:00:00 EST 2015 · Biochemical and Biophysical Research Communications · OSTI ID:1904750

Liu, Guangxiu; Zhang, Manxiao; Mo, Tianlu; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Science & Technology - Other Topics
Pyruvate
Carbon dioxide
Isoleucine
Glucose
Biosynthesis
Cobalamins
Threonine
Yeast

Title: Carbohydrate Metabolism and Carbon Fixation in Roseobacter denitrificans OCh114

Citation Formats

References (49)

Cited By (15)

Similar Records

Related Subjects