A Cobalamin Activity-Based Probe Enables Microbial Cell Growth and Finds New Cobalamin-Protein Interactions across Domains

Rosnow, Joshua J.; Hwang, Sungmin; Killinger, Bryan J.; Kim, Young-Mo; Moore, Ronald J.; Lindemann, Stephen R.; Maupin-Furlow, Julie A.; Wright, Aaron T.

doi:10.1128/aem.00955-18

Title: A Cobalamin Activity-Based Probe Enables Microbial Cell Growth and Finds New Cobalamin-Protein Interactions across Domains

Journal Article · Fri Aug 31 00:00:00 EDT 2018 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/aem.00955-18· OSTI ID:1688417

^[1]; Hwang, Sungmin ^[2]; Killinger, Bryan J. ^[3];

^[1]; Moore, Ronald J. ^[1]; Lindemann, Stephen R. ^[4]; Maupin-Furlow, Julie A. ^[5];

^[3]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
Univ. of Florida, Gainesville, FL (United States). Dept. of Microbiology and Cell Science
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division; Washington State Univ., Pullman, WA (United States). School of Chemical Engineering and Bioengineering
Purdue Univ., West Lafayette, IN (United States). Dept. of Food Science
Univ. of Florida, Gainesville, FL (United States). Dept. of Microbiology and Cell Science and Genetics Inst.

Understanding the factors that regulate microbe function and microbial community assembly, function, and fitness is a grand challenge. A critical factor and an important enzyme cofactor and regulator of gene expression is cobalamin (vitamin B₁₂). Our knowledge of the roles of vitamin B₁₂ is limited, because technologies that enable in situ characterization of microbial metabolism and gene regulation with minimal impact on cell physiology are needed. To meet this need, here we show that a synthetic probe mimic of B₁₂ supports the growth of B₁₂-auxotrophic bacteria and archaea. We demonstrate that a B₁₂ activity-based probe (B₁₂-ABP) is actively transported into Escherichia coli cells and converted to adenosyl-B₁₂-ABP akin to native B₁₂. Identification of the proteins that bind the B₁₂-ABP in vivo in E. coli, a Rhodobacteraceae sp. and Haloferax volcanii, demonstrate the specificity for known and novel B₁₂ protein targets. The B₁₂-ABP also regulates the B₁₂ dependent RNA riboswitch btuB and the transcription factor EutR. Our results demonstrate a new approach to gain knowledge about the role of B₁₂ in microbe functions. Our approach provides a powerful nondisruptive tool to analyze B₁₂ interactions in living cells and can be used to discover the role of B₁₂ in diverse microbial systems.

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Research Organization:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Laboratory Directed Research and Development (LDRD) Program; National Institutes of Health (NIH)

Grant/Contract Number:: AC05-76RL01830; FG02-05ER15650; R01-GM57498

OSTI ID:: 1688417

Report Number(s):: PNNL-SA-127734

Journal Information:: Applied and Environmental Microbiology, Vol. 84, Issue 18; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

Biocatalytic Production of Coenzyme A Analogues Strauss, Erick; de Villiers, Marianne; Rootman, Ilse ChemCatChem, Vol. 2, Issue 8 https://doi.org/10.1002/cctc.201000139	journal	July 2010
Microbial production of vitamin B 12 Martens, H. Barg, M. Warren, D. Jah, J. -H. Applied Microbiology and Biotechnology, Vol. 58, Issue 3 https://doi.org/10.1007/s00253-001-0902-7	journal	March 2002
Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection Baba, Tomoya; Ara, Takeshi; Hasegawa, Miki Molecular Systems Biology, Vol. 2, Article No. 2006.0008 https://doi.org/10.1038/msb4100050	journal	February 2006
Activity-based protein profiling of microbes Sadler, Natalie C.; Wright, Aaron T. Current Opinion in Chemical Biology, Vol. 24 https://doi.org/10.1016/j.cbpa.2014.10.022	journal	February 2015
Activity-Based Protein Profiling: From Enzyme Chemistry to Proteomic Chemistry Cravatt, Benjamin F.; Wright, Aaron T.; Kozarich, John W. Annual Review of Biochemistry, Vol. 77, Issue 1 https://doi.org/10.1146/annurev.biochem.75.101304.124125	journal	June 2008
Vitamin B ₁₂ -Mediated Restoration of Defective Anaerobic Growth Leads to Reduced Biofilm Formation in Pseudomonas aeruginosa Lee, Kang-Mu; Go, Junhyeok; Yoon, Mi Young Infection and Immunity, Vol. 80, Issue 5 https://doi.org/10.1128/IAI.06161-11	journal	February 2012
Photo-leucine and photo-methionine allow identification of protein-protein interactions in living cells Suchanek, Monika; Radzikowska, Anna; Thiele, Christoph Nature Methods, Vol. 2, Issue 4 https://doi.org/10.1038/nmeth752	journal	March 2005
Multiple B-vitamin depletion in large areas of the coastal ocean Sanudo-Wilhelmy, S. A.; Cutter, L. S.; Durazo, R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 35 https://doi.org/10.1073/pnas.1208755109	journal	July 2012
Vitamin B12 Uptake by the Gut Commensal Bacteria Bacteroides thetaiotaomicron Limits the Production of Shiga Toxin by Enterohemorrhagic Escherichia coli Cordonnier, Charlotte; Le Bihan, Guillaume; Emond-Rheault, Jean-Guillaume Toxins, Vol. 8, Issue 1 https://doi.org/10.3390/toxins8010014	journal	January 2016
Outer Membrane Active Transport: Structure of the BtuB:TonB Complex Shultis, D. D.; Purdy, M. D.; Banchs, C. N. Science, Vol. 312, Issue 5778 https://doi.org/10.1126/science.1127694	journal	June 2006
Cobalamin's (Vitamin B 12 ) Surprising Function as a Photoreceptor Cheng, Zhuo; Yamamoto, Haruki; Bauer, Carl E. Trends in Biochemical Sciences, Vol. 41, Issue 8 https://doi.org/10.1016/j.tibs.2016.05.002	journal	August 2016
Underlying mechanisms for syntrophic metabolism of essential enzyme cofactors in microbial communities Romine, Margaret F.; Rodionov, Dmitry A.; Maezato, Yukari The ISME Journal, Vol. 11, Issue 6 https://doi.org/10.1038/ismej.2017.2	journal	February 2017
Live Cell Discovery of Microbial Vitamin Transport and Enzyme-Cofactor Interactions Anderson, Lindsey N.; Koech, Phillip K.; Plymale, Andrew E. ACS Chemical Biology, Vol. 11, Issue 2 https://doi.org/10.1021/acschembio.5b00918	journal	December 2015
Beyond catalysis: vitamin B ₁₂ as a cofactor in gene regulation : B12 in gene regulation Klug, Gabriele Molecular Microbiology, Vol. 91, Issue 4 https://doi.org/10.1111/mmi.12490	journal	January 2014
Decoupling of microbial carbon, nitrogen, and phosphorus cycling in response to extreme temperature events Mooshammer, Maria; Hofhansl, Florian; Frank, Alexander H. Science Advances, Vol. 3, Issue 5 https://doi.org/10.1126/sciadv.1602781	journal	May 2017
Genetic analysis of homologous recombination in Archaea: Haloferax volcanii as a model organism Allers, T.; Ngo, H. -P. Biochemical Society Transactions, Vol. 31, Issue 3 https://doi.org/10.1042/bst0310706	journal	June 2003
Activity-Based Protein Profiling in Vivo Using a Copper(I)-Catalyzed Azide-Alkyne [3 + 2] Cycloaddition Speers, Anna E.; Adam, Gregory C.; Cravatt, Benjamin F. Journal of the American Chemical Society, Vol. 125, Issue 16, p. 4686-4687 https://doi.org/10.1021/ja034490h	journal	April 2003
Metabolic cross-talk allows labeling of O-linked -N-acetylglucosamine-modified proteins via the N-acetylgalactosamine salvage pathway Boyce, M.; Carrico, I. S.; Ganguli, A. S. Proceedings of the National Academy of Sciences, Vol. 108, Issue 8 https://doi.org/10.1073/pnas.1010045108	journal	February 2011
Development of a Gene Knockout System for the Halophilic Archaeon Haloferax volcanii by Use of the pyrE Gene Bitan-Banin, G.; Ortenberg, R.; Mevarech, M. Journal of Bacteriology, Vol. 185, Issue 3 https://doi.org/10.1128/JB.185.3.772-778.2003	journal	February 2003
Phototrophic biofilm assembly in microbial-mat-derived unicyanobacterial consortia: model systems for the study of autotroph-heterotroph interactions Cole, Jessica K.; Hutchison, Janine R.; Renslow, Ryan S. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00109	journal	April 2014
Ethanolamine utilization in Salmonella typhimurium. Roof, D. M.; Roth, J. R. Journal of Bacteriology, Vol. 170, Issue 9 https://doi.org/10.1128/jb.170.9.3855-3863.1988	journal	September 1988
Two distinct pools of B ₁₂ analogs reveal community interdependencies in the ocean Heal, Katherine R.; Qin, Wei; Ribalet, Francois Proceedings of the National Academy of Sciences, Vol. 114, Issue 2 https://doi.org/10.1073/pnas.1608462114	journal	December 2016
Profiling Genome-Wide Chromatin Methylation with Engineered Posttranslation Apparatus within Living Cells Wang, Rui; Islam, Kabirul; Liu, Ying Journal of the American Chemical Society, Vol. 135, Issue 3 https://doi.org/10.1021/ja309412s	journal	January 2013
B12 cofactors directly stabilize an mRNA regulatory switch Johnson Jr, James E.; Reyes, Francis E.; Polaski, Jacob T. Nature, Vol. 492, Issue 7427 https://doi.org/10.1038/nature11607	journal	October 2012
Photo-lysine captures proteins that bind lysine post-translational modifications Yang, Tangpo; Li, Xiao-Meng; Bao, Xiucong Nature Chemical Biology, Vol. 12, Issue 2 https://doi.org/10.1038/nchembio.1990	journal	December 2015
In Vitro Functional Characterization of BtuCD-F, the Escherichia coli ABC Transporter for Vitamin B ₁₂ Uptake ^† Borths, Elizabeth L.; Poolman, Bert; Hvorup, Rikki N. Biochemistry, Vol. 44, Issue 49 https://doi.org/10.1021/bi0513103	journal	December 2005
The Many Faces of Vitamin B₁₂: Catalysis by Cobalamin-Dependent Enzymes Banerjee, Ruma; Ragsdale, Stephen W. Annual Review of Biochemistry, Vol. 72, Issue 1, p. 209-247 https://doi.org/10.1146/annurev.biochem.72.121801.161828	journal	June 2003
Chemical Proteomic Profiling of Human Methyltransferases Horning, Benjamin D.; Suciu, Radu M.; Ghadiri, Darian A. Journal of the American Chemical Society, Vol. 138, Issue 40 https://doi.org/10.1021/jacs.6b07830	journal	September 2016
Ethanolamine utilization in bacterial pathogens: roles and regulation Garsin, Danielle A. Nature Reviews Microbiology, Vol. 8, Issue 4 https://doi.org/10.1038/nrmicro2334	journal	April 2010
Glycerol-Mediated Repression of Glucose Metabolism and Glycerol Kinase as the Sole Route of Glycerol Catabolism in the Haloarchaeon Haloferax volcanii Sherwood, K. E.; Cano, D. J.; Maupin-Furlow, J. A. Journal of Bacteriology, Vol. 191, Issue 13 https://doi.org/10.1128/JB.00131-09	journal	May 2009
Marine Microbes See a Sea of Gradients Stocker, R. Science, Vol. 338, Issue 6107 https://doi.org/10.1126/science.1208929	journal	November 2012
Comparative Genomics of the Vitamin B ₁₂ Metabolism and Regulation in Prokaryotes Rodionov, Dmitry A.; Vitreschak, Alexey G.; Mironov, Andrey A. Journal of Biological Chemistry, Vol. 278, Issue 42 https://doi.org/10.1074/jbc.M305837200	journal	July 2003
A new metabolic cell-wall labelling method reveals peptidoglycan in Chlamydia trachomatis Liechti, G. W.; Kuru, E.; Hall, E. Nature, Vol. 506, Issue 7489 https://doi.org/10.1038/nature12892	journal	December 2013
Development of Additional Selectable Markers for the Halophilic Archaeon Haloferax volcanii Based on the leuB and trpA Genes Allers, T.; Ngo, H. -P.; Mevarech, M. Applied and Environmental Microbiology, Vol. 70, Issue 2 https://doi.org/10.1128/AEM.70.2.943-953.2004	journal	February 2004
Current Developments in Activity-Based Protein Profiling Willems, Lianne I.; Overkleeft, Herman S.; van Kasteren, Sander I. Bioconjugate Chemistry, Vol. 25, Issue 7 https://doi.org/10.1021/bc500208y	journal	June 2014
Radical Carbon Skeleton Rearrangements: Catalysis by Coenzyme B ₁₂ -Dependent Mutases Banerjee, Ruma Chemical Reviews, Vol. 103, Issue 6 https://doi.org/10.1021/cr0204395	journal	June 2003
2016 update of the PRIDE database and its related tools Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1145	journal	November 2015
An accurate mass tag strategy for quantitative and high-throughput proteome measurements Smith, Richard D.; Anderson, Gordon A.; Lipton, Mary S. PROTEOMICS, Vol. 2, Issue 5 https://doi.org/10.1002/1615-9861(200205)2:5<513::AID-PROT513>3.0.CO;2-W	journal	May 2002
A new simvastatin (mevinolin)-resistance marker from Haloarcula hispanica and a new Haloferax volcanii strain cured of plasmid pHV2 Dyall-Smith, M. L.; Wendoloski, D.; Ferrer, C. Microbiology, Vol. 147, Issue 4 https://doi.org/10.1099/00221287-147-4-959	journal	April 2001
Discovery of a SAR11 growth requirement for thiamin’s pyrimidine precursor and its distribution in the Sargasso Sea Carini, Paul; Campbell, Emily O.; Morré, Jeff The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.61	journal	April 2014
The Human Microbiome: From Symbiosis to Pathogenesis Eloe-Fadrosh, Emiley A.; Rasko, David A. Annual Review of Medicine, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-med-010312-133513	journal	January 2013
Using a Riboswitch Sensor to Examine Coenzyme B12 Metabolism and Transport in E. coli Fowler, Casey C.; Brown, Eric D.; Li, Yingfu Chemistry & Biology, Vol. 17, Issue 7 https://doi.org/10.1016/j.chembiol.2010.05.025	journal	July 2010
In Vivo Imaging of Membrane-Associated Glycans in Developing Zebrafish Laughlin, S. T.; Baskin, J. M.; Amacher, S. L. Science, Vol. 320, Issue 5876 https://doi.org/10.1126/science.1155106	journal	May 2008
Manipulating the soil microbiome to increase soil health and plant fertility Chaparro, Jacqueline M.; Sheflin, Amy M.; Manter, Daniel K. Biology and Fertility of Soils, Vol. 48, Issue 5 https://doi.org/10.1007/s00374-012-0691-4	journal	May 2012
Human Gut Microbes Use Multiple Transporters to Distinguish Vitamin B12 Analogs and Compete in the Gut Degnan, Patrick H.; Barry, Natasha A.; Mok, Kenny C. Cell Host & Microbe, Vol. 15, Issue 1 https://doi.org/10.1016/j.chom.2013.12.007	journal	January 2014
Dynamics in microbial communities: unraveling mechanisms to identify principles Konopka, Allan; Lindemann, Stephen; Fredrickson, Jim The ISME Journal, Vol. 9, Issue 7 https://doi.org/10.1038/ismej.2014.251	journal	December 2014
Geomicrobiology of High-Level Nuclear Waste-Contaminated Vadose Sediments at the Hanford Site, Washington State Fredrickson, J. K.; Zachara, J. M.; Balkwill, D. L. Applied and Environmental Microbiology, Vol. 70, Issue 7 https://doi.org/10.1128/AEM.70.7.4230-4241.2004	journal	July 2004
EutR Is a Direct Regulator of Genes That Contribute to Metabolism and Virulence in Enterohemorrhagic Escherichia coli O157:H7 Luzader, D. H.; Clark, D. E.; Gonyar, L. A. Journal of Bacteriology, Vol. 195, Issue 21 https://doi.org/10.1128/JB.00937-13	journal	August 2013
A Decade of Riboswitches Serganov, Alexander; Nudler, Evgeny Cell, Vol. 152, Issue 1-2 https://doi.org/10.1016/j.cell.2012.12.024	journal	January 2013
Members of the PpaA/AerR Antirepressor Family Bind Cobalamin Vermeulen, Arjan J.; Bauer, Carl E. Journal of Bacteriology, Vol. 197, Issue 16 https://doi.org/10.1128/JB.00374-15	journal	June 2015
Cobalamin-Dependent Methyltransferases Matthews, Rowena G. Accounts of Chemical Research, Vol. 34, Issue 8 https://doi.org/10.1021/ar0000051	journal	August 2001
Elucidation of roles for vitamin B ₁₂ in regulation of folate, ubiquinone, and methionine metabolism Romine, Margaret F.; Rodionov, Dmitry A.; Maezato, Yukari Proceedings of the National Academy of Sciences, Vol. 114, Issue 7 https://doi.org/10.1073/pnas.1612360114	journal	January 2017
COBALAMIN (COENZYME B ₁₂ ): Synthesis and Biological Significance Roth, Jr; Lawrence, Jg; Bobik, Ta Annual Review of Microbiology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.micro.50.1.137	journal	October 1996
Illumination of growth, division and secretion by metabolic labeling of the bacterial cell surface Siegrist, M. Sloan; Swarts, Benjamin M.; Fox, Douglas M. FEMS Microbiology Reviews, Vol. 39, Issue 2 https://doi.org/10.1093/femsre/fuu012	journal	February 2015
Microbial metabolism of amino alcohols. Purification and properties of coenzyme B12-dependent ethanolamine ammonia-lysae of Escherichia coli Blackwell, Carol M.; Turner, John M. Biochemical Journal, Vol. 175, Issue 2 https://doi.org/10.1042/bj1750555	journal	November 1978
Crystal Structures of Ethanolamine Ammonia-lyase Complexed with Coenzyme B ₁₂ Analogs and Substrates Shibata, Naoki; Tamagaki, Hiroko; Hieda, Naoki Journal of Biological Chemistry, Vol. 285, Issue 34 https://doi.org/10.1074/jbc.M110.125112	journal	June 2010
The 17-Gene Ethanolamine (eut) Operon ofSalmonella typhimurium Encodes Five Homologues of Carboxysome Shell Proteins Kofoid, Eric; Rappleye, Chad; Stojiljkovic, Igor Journal of Bacteriology, Vol. 181, Issue 17 https://doi.org/10.1128/JB.181.17.5317-5329.1999	journal	September 1999
2016 update of the PRIDE database and its related tools Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi Nucleic Acids Research, Vol. 44, Issue 22 https://doi.org/10.1093/nar/gkw880	journal	September 2016
Identification and Characterization of a Novel FosA7 Member from Fosfomycin-Resistant Escherichia coli Clinical Isolates from Canadian Hospitals Milner, Kieran A.; Bay, Denice C.; Alexander, David Antimicrobial Agents and Chemotherapy, Vol. 65, Issue 1 https://doi.org/10.1128/aac.00865-20	journal	December 2020
Radical Carbon Skeleton Rearrangements: Catalysis by Coenzyme B12-Dependent Mutases Banerjee, Ruma ChemInform, Vol. 34, Issue 32 https://doi.org/10.1002/chin.200332271	journal	August 2003

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vitamin B12
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Title: A Cobalamin Activity-Based Probe Enables Microbial Cell Growth and Finds New Cobalamin-Protein Interactions across Domains

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