BciD Is a Radical S-Adenosyl-l-methionine (SAM) Enzyme That Completes Bacteriochlorophyllide e Biosynthesis by Oxidizing a Methyl Group into a Formyl Group at C-7

Thweatt, Jennifer L.; Ferlez, Bryan H.; Golbeck, John H.; Bryant, Donald A.

doi:10.1074/jbc.M116.767665

Title: BciD Is a Radical S-Adenosyl-l-methionine (SAM) Enzyme That Completes Bacteriochlorophyllide e Biosynthesis by Oxidizing a Methyl Group into a Formyl Group at C-7

Journal Article · Sun Jan 01 00:00:00 EST 2017 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.M116.767665· OSTI ID:1769197

Thweatt, Jennifer L.; Ferlez, Bryan H.; Golbeck, John H.;

Green bacteria are chlorophotorophs that synthesize bacteriochlorophyll (BChl) c, d, or e, which assemble into supramolecular, nanotubular structures in large light-harvesting structures called chlorosomes. The biosynthetic pathways of these chlorophylls are known except for one reaction. Null mutants of bciD, which encodes a putative radical S-adenosyl-L-methionine (SAM) protein, are unable to synthesize BChl e but accumulate BChl c; however, it is unknown whether BciD is sufficient to convert BChl c (or its precursor, bacteriochlorophyllide (BChlide) c) into BChl e (or BChlide e). To determine the function of BciD, we expressed the bciD gene of Chlorobaculum limnaeum strain DSMZ 1677^T in Escherichia coli and purified the enzyme under anoxic conditions. Electron paramagnetic resonance spectroscopy of BciD indicated that it contains a single [4Fe-4S] cluster. In assays containing SAM, BChlide c or d, and sodium dithionite, BciD catalyzed the conversion of SAM into 5'-deoxyadenosine and BChlide c or d into BChlide e or f, respectively. Our analyses also identified intermediates that are proposed to be 7¹-OH-BChlide c and d. Thus, BciD is a radical SAM enzyme that converts the methyl group of BChlide c or d into the formyl group of BChlide e or f. This probably occurs by a mechanism involving consecutive hydroxylation reactions of the C-7 methyl group to form a geminal diol intermediate, which spontaneously dehydrates to produce the final products, BChlide e or BChlide f. The demonstration that BciD is sufficient to catalyze the conversion of BChlide c into BChlide e completes the biosynthetic pathways for all “Chlorobium chlorophylls.”

View Journal Article

Cite

Export

Save

Research Organization:: Pennsylvania State Univ., University Park, PA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG02-94ER20137; FG02-98ER20314

OSTI ID:: 1769197

Alternate ID(s):: OSTI ID: 1535358

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 292 Journal Issue: 4; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 18 works

Citation information provided by
Web of Science

References (57)

Bacteriochlorophyll f: properties of chlorosomes containing the “forbidden chlorophyll” Vogl, Kajetan; Tank, Marcus; Orf, Gregory S. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00298	journal	August 2012
Genetic Analysis of Chlorophyll Biosynthesis Suzuki, Jon Y.; Bollivar, David W.; Bauer, Carl E. Annual Review of Genetics, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.genet.31.1.61	journal	December 1997
Reconstitution of electron transport in photosystem I with PsaC and PsaD proteins expressed in Escherichia coli Zhao, Jindong; Warren, Patrick V.; Li, Ning FEBS Letters, Vol. 276, Issue 1-2 https://doi.org/10.1016/0014-5793(90)80536-R	journal	December 1990
Chlorosome antenna complexes from green photosynthetic bacteria Orf, Gregory S.; Blankenship, Robert E. Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9869-3	journal	June 2013
Bacteriochlorophyllide c C-82 and C-121 Methyltransferases Are Essential for Adaptation to Low Light in Chlorobaculum tepidum Chew, A. G. M.; Frigaard, N. -U.; Bryant, D. A. Journal of Bacteriology, Vol. 189, Issue 17 https://doi.org/10.1128/JB.00519-07	journal	June 2007
The chlorosome: a prototype for efficient light harvesting in photosynthesis Oostergetel, Gert T.; van Amerongen, Herbert; Boekema, Egbert J. Photosynthesis Research, Vol. 104, Issue 2-3 https://doi.org/10.1007/s11120-010-9533-0	journal	February 2010
Chlorobium tepidum Mutant Lacking Bacteriochlorophyll c Made by Inactivation of the bchK Gene, Encoding Bacteriochlorophyll c Synthase Frigaard, N. -U.; Voigt, G. D.; Bryant, D. A. Journal of Bacteriology, Vol. 184, Issue 12 https://doi.org/10.1128/JB.184.12.3368-3376.2002	journal	June 2002
A Broad Host Range Mobilization System for In Vivo Genetic Engineering Transposon Mutagenesis in Gram Negative Bacteria Simon, R.; Priefer, U.; Pühler, A. Bio/Technology, Vol. 1, Issue 9, p. 784-791 https://doi.org/10.1038/nbt1183-784	journal	November 1983
96 Bacteriochlorophyll Biosynthesis and Assembly in Green Chlorophototrophic Bacteria: Theme and Variations Liu, Zhenfeng; Bryant, Donald A. Handbook of Porphyrin Science https://doi.org/10.1142/9789814335508_0023	book	June 2012
The bchU Gene of Chlorobium tepidum Encodes the C-20 Methyltransferase in Bacteriochlorophyll c Biosynthesis Maresca, J. A.; Maqueo Chew, A. G.; Ros Ponsati, M. Journal of Bacteriology, Vol. 186, Issue 9 https://doi.org/10.1128/JB.186.9.2558-2566.2004	journal	April 2004
Chlorophyll Biosynthesis in Bacteria: The Origins of Structural and Functional Diversity Chew, Aline Gomez Maqueo; Bryant, Donald A. Annual Review of Microbiology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093242	journal	October 2007
Aerobic and Anaerobic Mg-Protoporphyrin Monomethyl Ester Cyclases in Purple Bacteria: A STRATEGY ADOPTED TO BYPASS THE REPRESSIVE OXYGEN CONTROL SYSTEM Ouchane, Soufian; Steunou, Anne-Soisig; Picaud, Martine Journal of Biological Chemistry, Vol. 279, Issue 8 https://doi.org/10.1074/jbc.M309851200	journal	November 2003
Selective Protein Extraction from Chlorobium tepidum Chlorosomes Using Detergents. Evidence That CsmA Forms Multimers and Binds Bacteriochlorophyll a ^† Bryant, Donald A.; Vassilieva, Elena V.; Frigaard, Niels-Ulrik Biochemistry, Vol. 41, Issue 48 https://doi.org/10.1021/bi026599s	journal	December 2002
‘Candidatus Thermochlorobacter aerophilum:’ an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics Liu, Zhenfeng; Klatt, Christian G.; Ludwig, Marcus The ISME Journal, Vol. 6, Issue 10 https://doi.org/10.1038/ismej.2012.24	journal	March 2012
Prokaryotic photosynthesis and phototrophy illuminated Bryant, Donald A.; Frigaard, Niels-Ulrik Trends in Microbiology, Vol. 14, Issue 11 https://doi.org/10.1016/j.tim.2006.09.001	journal	November 2006
Candidatus Chloracidobacterium thermophilum: An Aerobic Phototrophic Acidobacterium Bryant, D. A.; Costas, A. M. G.; Maresca, J. A. Science, Vol. 317, Issue 5837 https://doi.org/10.1126/science.1143236	journal	July 2007
Crystal Structures of BchU, a Methyltransferase Involved in Bacteriochlorophyll c Biosynthesis, and its Complex with S-adenosylhomocysteine: Implications for Reaction Mechanism Wada, Kei; Yamaguchi, Hitomi; Harada, Jiro Journal of Molecular Biology, Vol. 360, Issue 4 https://doi.org/10.1016/j.jmb.2006.05.057	journal	July 2006
Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts Tomitani, Akiko; Okada, Kiyotaka; Miyashita, Hideaki Nature, Vol. 400, Issue 6740 https://doi.org/10.1038/22101	journal	July 1999
Large-scale distribution and activity patterns of an extremely low-light-adapted population of green sulfur bacteria in the Black Sea: Green sulfur bacteria in the Black Sea Marschall, Evelyn; Jogler, Mareike; Henßge, Uta Environmental Microbiology, Vol. 12, Issue 5 https://doi.org/10.1111/j.1462-2920.2010.02178.x	journal	March 2010
Identification of a Gene Essential for the First Committed Step in the Biosynthesis of Bacteriochlorophyll c Liu, Zhenfeng; Bryant, Donald A. Journal of Biological Chemistry, Vol. 286, Issue 25 https://doi.org/10.1074/jbc.M111.249433	journal	May 2011
Comparison between chlorosomes containing bacteriochlorophyll-c and chlorosomes containing bacteriochlorophyll-d isolated from two substrains of green sulfur photosynthetic bacterium Chlorobium vibrioforme NCIB 8327 Saga, Yoshitaka; Tamiaki, Hitoshi Journal of Photochemistry and Photobiology B: Biology, Vol. 75, Issue 1-2 https://doi.org/10.1016/j.jphotobiol.2004.05.012	journal	July 2004
Characterization of Chlorophyll a and Bacteriochlorophyll a Synthases by Heterologous Expression in Escherichia coli Oster, Ulrike; Bauer, Carl E.; Rüdiger, Wolfhart Journal of Biological Chemistry, Vol. 272, Issue 15 https://doi.org/10.1074/jbc.272.15.9671	journal	April 1997
Overexpression of biotin synthase and biotin ligase is required for efficient generation of sulfur-35 labeled biotin in E. coli Delli-Bovi, Teegan A.; Spalding, Maroya D.; Prigge, Sean T. BMC Biotechnology, Vol. 10, Issue 1 https://doi.org/10.1186/1472-6750-10-73	journal	January 2010
Purification of ferredoxins and their reaction with purified reaction center complex from the green sulfur bacterium Chlorobium tepidum Seo, Daisuke; Tomioka, Atusi; Kusumoto, Noriaki Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1503, Issue 3 https://doi.org/10.1016/S0005-2728(00)00245-0	journal	January 2001
A seventh bacterial chlorophyll driving a large light-harvesting antenna Harada, Jiro; Mizoguchi, Tadashi; Tsukatani, Yusuke Scientific Reports, Vol. 2, Issue 1 https://doi.org/10.1038/srep00671	journal	September 2012
In Vitro Assays of BciC Showing C13 ² -Demethoxycarbonylase Activity Requisite for Biosynthesis of Chlorosomal Chlorophyll Pigments Teramura, Misato; Harada, Jiro; Mizoguchi, Tadashi Plant and Cell Physiology, Vol. 57, Issue 5 https://doi.org/10.1093/pcp/pcw045	journal	March 2016
Spectroscopic insights into the decreased efficiency of chlorosomes containing bacteriochlorophyll f Orf, Gregory S.; Tank, Marcus; Vogl, Kajetan Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 4 https://doi.org/10.1016/j.bbabio.2013.01.006	journal	April 2013
The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium Eisen, J. A.; Nelson, K. E.; Paulsen, I. T. Proceedings of the National Academy of Sciences, Vol. 99, Issue 14 https://doi.org/10.1073/pnas.132181499	journal	July 2002
In vitro activity of C-20 methyltransferase, BchU, involved in bacteriochlorophyll c biosynthetic pathway in green sulfur bacteria Harada, Jiro; Saga, Yoshitaka; Yaeda, Yuki FEBS Letters, Vol. 579, Issue 9 https://doi.org/10.1016/j.febslet.2005.01.087	journal	March 2005
Signature pigments of green sulfur bacteria in lower Pleistocene deposits from the Banyoles lacustrine area (Spain) Mallorquí, N.; Arellano, J. B.; Borrego, C. M. Journal of Paleolimnology, Vol. 34, Issue 2 https://doi.org/10.1007/s10933-005-3731-3	journal	August 2005
Photophysical Properties of the Excited States of Bacteriochlorophyll f in Solvents and in Chlorosomes Niedzwiedzki, Dariusz M.; Orf, Gregory S.; Tank, Marcus The Journal of Physical Chemistry B, Vol. 118, Issue 9 https://doi.org/10.1021/jp409495m	journal	January 2014
Studies on the Chemical Nature of Clostridial Ferredoxin Lovenberg, Walter; Buchanan, Bob B.; Rabinowitz, Jesse C. Journal of Biological Chemistry, Vol. 238, Issue 12 https://doi.org/10.1016/S0021-9258(18)51805-6	journal	December 1963
Stereochemical conversion of C3-vinyl group to 1-hydroxyethyl group in bacteriochlorophyll c by the hydratases BchF and BchV: adaptation of green sulfur bacteria to limited-light environments : Low-light-intensity adaptation of GSB by hydratases Harada, Jiro; Teramura, Misato; Mizoguchi, Tadashi Molecular Microbiology, Vol. 98, Issue 6 https://doi.org/10.1111/mmi.13208	journal	October 2015
Isolation of a bchl c mutant from Chlorobium with bchl d by cultivation at low light intensity Broch-due, Margrethe; Ormerod, John G. FEMS Microbiology Letters, Vol. 3, Issue 5 https://doi.org/10.1111/j.1574-6968.1978.tb01953.x	journal	May 1978
Characterization of Chlorobium tepidum Chlorosomes: A Calculation of Bacteriochlorophyll c per Chlorosome and Oligomer Modeling Montaño, Gabriel A.; Bowen, Benjamin P.; LaBelle, Jeffrey T. Biophysical Journal, Vol. 85, Issue 4 https://doi.org/10.1016/S0006-3495(03)74678-5	journal	October 2003
Characterization of a Synechococcus sp. strain PCC 7002 mutant lacking Photosystem I. Protein assembly and energy distribution in the absence of the Photosystem I reaction center core complex Shen, Gaozhong; Bryant, Donald A. Photosynthesis Research, Vol. 44, Issue 1-2 https://doi.org/10.1007/BF00018295	journal	May 1995
Quinones in chlorosomes of green sulfur bacteria and their role in the redox-dependent fluorescence studied in chlorosome-like bacteriochlorophyll c aggregates Frigaard, N. -U.; Takaichi, Shinichi; Hirota, Masamitsu Archives of Microbiology, Vol. 167, Issue 6 https://doi.org/10.1007/s002030050453	journal	May 1997
Genetic transfer by conjugation in the thermophilic green sulfur bacterium Chlorobium tepidum. Wahlund, T. M.; Madigan, M. T. Journal of Bacteriology, Vol. 177, Issue 9 https://doi.org/10.1128/JB.177.9.2583-2588.1995	journal	May 1995
Assembly of Iron-Sulfur Clusters: IDENTIFICATION OF AN Zheng, Limin; Cash, Valerie L.; Flint, Dennis H. Journal of Biological Chemistry, Vol. 273, Issue 21 https://doi.org/10.1074/jbc.273.21.13264	journal	May 1998
Red shift of absorption maxima in Chlorobiineae through enzymic methylation of their antenna bacteriocholorphylls Bobe, Frank W.; Pfennig, Norbert; Swanson, Kristin L. Biochemistry, Vol. 29, Issue 18 https://doi.org/10.1021/bi00470a012	journal	May 1990
Comparison of the physical characteristics of chlorosomes from three different phyla of green phototrophic bacteria Adams, Peter G.; Cadby, Ashley J.; Robinson, Benjamin Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 10 https://doi.org/10.1016/j.bbabio.2013.07.004	journal	October 2013
In Vitro Enzymatic Activities of Bacteriochlorophyll a Synthase Derived from the Green Sulfur Photosynthetic Bacterium Chlorobaculum tepidum Saga, Yoshitaka; Hirota, Keiya; Harada, Jiro Biochemistry, Vol. 54, Issue 32 https://doi.org/10.1021/acs.biochem.5b00311	journal	August 2015
The Structure–Function Linkage Database Akiva, Eyal; Brown, Shoshana; Almonacid, Daniel E. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1130	journal	November 2013
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
In vitro stereospecific hydration activities of the 3-vinyl group of chlorophyll derivatives by BchF and BchV enzymes involved in bacteriochlorophyll c biosynthesis of green sulfur bacteria Teramura, Misato; Harada, Jiro; Tamiaki, Hitoshi Photosynthesis Research, Vol. 130, Issue 1-3 https://doi.org/10.1007/s11120-016-0220-7	journal	January 2016
Isorenieratene Biosynthesis in Green Sulfur Bacteria Requires the Cooperative Actions of Two Carotenoid Cyclases Maresca, J. A.; Romberger, S. P.; Bryant, D. A. Journal of Bacteriology, Vol. 190, Issue 19 https://doi.org/10.1128/JB.00758-08	journal	August 2008
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw054	journal	March 2016
Separation of bacteriochlorophyll homologues from green photosynthetic sulfur bacteria by reversed-phase HPLC Borrego, C. M.; Garcia-Gil, L. J. Photosynthesis Research, Vol. 41, Issue 1 https://doi.org/10.1007/BF02184156	journal	July 1994
Physiology and Phylogeny of Green Sulfur Bacteria Forming a Monospecific Phototrophic Assemblage at a Depth of 100 Meters in the Black Sea Manske, A. K.; Glaeser, J.; Kuypers, M. M. M. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8049-8060.2005	journal	December 2005
Mechanism of Isoprenylcysteine Carboxyl Methylation from the Crystal Structure of the Integral Membrane Methyltransferase ICMT Yang, Jing; Kulkarni, Kiran; Manolaridis, Ioannis Molecular Cell, Vol. 44, Issue 6 https://doi.org/10.1016/j.molcel.2011.10.020	journal	December 2011
Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and fmo (Fenna-Matthews-Olson protein) gene sequences Imhoff, J. F. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 4 https://doi.org/10.1099/ijs.0.02403-0	journal	July 2003
Speciation and ecological success in dimly lit waters: horizontal gene transfer in a green sulfur bacteria bloom unveiled by metagenomic assembly Llorens–Marès, Tomàs; Liu, Zhenfeng; Allen, Lisa Zeigler The ISME Journal, Vol. 11, Issue 1 https://doi.org/10.1038/ismej.2016.93	journal	July 2016
Bacteriochlorophyll homolog compositions in the bchU mutants of green sulfur bacteria Tsukatani, Yusuke; Harada, Jiro; Mizoguchi, Tadashi Photochemical & Photobiological Sciences, Vol. 12, Issue 12 https://doi.org/10.1039/c3pp50253h	journal	January 2013
Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a Tanaka, A.; Ito, H.; Tanaka, R. Proceedings of the National Academy of Sciences, Vol. 95, Issue 21 https://doi.org/10.1073/pnas.95.21.12719	journal	October 1998
Recent Advances in Radical SAM Enzymology: New Structures and Mechanisms Wang, Jiarui; Woldring, Rory P.; Román-Meléndez, Gabriel D. ACS Chemical Biology, Vol. 9, Issue 9 https://doi.org/10.1021/cb5004674	journal	July 2014
Absence of the cbb ₃ Terminal Oxidase Reveals an Active Oxygen-Dependent Cyclase Involved in Bacteriochlorophyll Biosynthesis in Rhodobacter sphaeroides Chen, Guangyu E.; Canniffe, Daniel P.; Martin, Elizabeth C. Journal of Bacteriology, Vol. 198, Issue 15 https://doi.org/10.1128/JB.00121-16	journal	May 2016
Specific Gene bciD for C7-Methyl Oxidation in Bacteriochlorophyll e Biosynthesis of Brown-Colored Green Sulfur Bacteria Harada, Jiro; Mizoguchi, Tadashi; Satoh, Souichirou PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0060026	journal	April 2013

Cited By (3)

A paralog of a bacteriochlorophyll biosynthesis enzyme catalyzes the formation of 1,2-dihydrocarotenoids in green sulfur bacteria Canniffe, Daniel P.; Thweatt, Jennifer L.; Gomez Maqueo Chew, Aline Journal of Biological Chemistry, Vol. 293, Issue 39 https://doi.org/10.1074/jbc.ra118.004672	journal	August 2018
A physiological perspective on the origin and evolution of photosynthesis Martin, William F.; Bryant, Donald A.; Beatty, J. Thomas FEMS Microbiology Reviews, Vol. 42, Issue 2 https://doi.org/10.1093/femsre/fux056	journal	November 2017
Advances in the members and biosynthesis of chlorophyll family Qiu, N. W.; Jiang, D. C.; Wang, X. S. Photosynthetica, Vol. 57, Issue 4 https://doi.org/10.32615/ps.2019.116	journal	November 2019

Similar Records

Light Energy Transduction in Green Sulfur Bacteria

Technical Report · Mon Mar 27 00:00:00 EDT 2023 · OSTI ID:1769197

Bryant, Donald A.

Specific inhibition of antenna bacteriochlorophyll synthesis in Chlorobium vibrioforme by anesthetic gases

Journal Article · Thu Mar 01 00:00:00 EST 1990 · Journal of Bacteriology; (USA) · OSTI ID:1769197

Ormerod, J G; Nesbakken, T; Beale, S I

Q{sub y}-excitation resonance Raman spectra of chlorophyll a and bacteriochlorophyll c/d aggregates. Effects of peripheral substituents on the low-frequency vibrational characteristics

Journal Article · Thu May 16 00:00:00 EDT 1996 · Journal of Physical Chemistry · OSTI ID:1769197

Diers, J R; Bocian, D F; Zhu, Y; +1 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Biochemistry & Molecular Biology

Title: BciD Is a Radical S-Adenosyl-l-methionine (SAM) Enzyme That Completes Bacteriochlorophyllide e Biosynthesis by Oxidizing a Methyl Group into a Formyl Group at C-7

Citation Formats

References (57)

Cited By (3)

Similar Records

Related Subjects