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Exploration of Nicotine Metabolism in Paenarthrobacter nicotinovorans pAO1 by Microbial Proteomics

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Advancements of Mass Spectrometry in Biomedical Research

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1140))

Abstract

Proteomics, or the large-scale study of proteins, is a post-genomics field that, together with transcriptomics and metabolomics, has moved the study of bacteria to a new era based on system-wide understanding of bacterial metabolic and regulatory networks. The study of bacterial proteins or microbial proteomics has found a wide array of applications in many fields of microbiology, from food, clinical, and industrial microbiology to microbial ecology and physiology. The current chapter makes a brief technical introduction into the available approaches for the large-scale study of bacterial proteins using mass-spectrometry. Furthermore, the advantages and disadvantages of using bacteria for proteomics studies are indicated as well as several example studies where MS-based bacterial proteomics had a fundamental role in deciphering the scientific question. Finally, the proteomics study of nicotine catabolism in Paenarthrobacter nicotinovorans pAO1 using nanoLC–MS/MS is given as an in-depth example for possible applications of microbial proteomics.

The nicotine degradation pathway functioning in Paenarthrobacter nicotinovorans is encoded by the catabolic megaplasmid pAO1 that contains about 40 nicotine-related genes making out the nic-gens cluster. Despite the promising biotechnological potential for the production of green-chemicals, only half of the nic-genes have been experimentally linked to nicotine. In an attempt to systematically identify all the proteins involved in nicotine degradation, a gel-based proteomics approach was used to identify a total of 801 proteins when Paenarthrobacter nicotinovorans was grown on three carbon sources: citrate, nicotine and nicotine and citrate. The differences in protein abundance showed that the bacterium is able to switch between deamination and demethylation in the lower nicotine pathway based on the available C source. Several pAO1 putative genes including a hypothetical polyketide cyclase have been shown to have a nicotine-dependent expression and we hypothesize that the polyketide cyclase would hydrolyze the N1-C6 bond from the pyridine ring with the formation of alpha-keto-glutaramate. Two chromosomal proteins, a malate dehydrogenase, and a d-3-phosphoglycerate dehydrogenase were shown to be strongly upregulated when nicotine was the sole carbon source and could be related to the production of the alpha-keto-glutaramate by the polyketide cyclase.

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Abbreviations

2D-PAGE:

Two-dimensional polyacrylamide gel electrophoresis

ESI-MS/MS:

Electrospray ionization tandem mass spectrometry

HPLC:

High performance liquid chromatography

IEF:

Isoelectric focusing

LC-MS/MS:

Liquid chromatography tandem mass spectrometry

MALDI-MS/MS:

Matrix-assisted laser desorption/ionization tandem mass spectrometry

MALDI-TOF MS:

Matrix-assisted laser desorption/ionization Time-of-flight mass spectrometry

NDM:

Nicotine-degrading microorganisms

PMF:

Peptide-mass fingerprint

PTMs:

Post-translational modifications

SDS-PAGE:

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

T4SS:

Type IV secretion system

References

  1. Neidhardt, F. C. (2011). How microbial proteomics got started. Proteomics, 11(15), 2943–2946.

    Article  CAS  PubMed  Google Scholar 

  2. Chao, T. C., & Hansmeier, N. (2012). The current state of microbial proteomics: Where we are and where we want to go. Proteomics, 12(4–5), 638–650.

    Article  CAS  PubMed  Google Scholar 

  3. O’Farrell, P. H. (1975). High resolution two-dimensional electrophoresis of proteins. The Journal of Biological Chemistry, 250(10), 4007–4021.

    Google Scholar 

  4. Anderson, N. L., & Anderson, N. G. (1998). Proteome and proteomics: New technologies, new concepts, and new words. Electrophoresis, 19(11), 1853–1861.

    Article  CAS  PubMed  Google Scholar 

  5. Blackstock, W. P., & Weir, M. P. (1999). Proteomics: Quantitative and physical mapping of cellular proteins. Trends in Biotechnology, 17(3), 121–127.

    Article  CAS  PubMed  Google Scholar 

  6. Han, X. M., Aslanian, A., & Yates, J. R. (2008). Mass spectrometry for proteomics. Current Opinion in Chemical Biology, 12(5), 483–490.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Perkins, D. N., Pappin, D. J. C., Creasy, D. M., & Cottrell, J. S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis, 20(18), 3551–3567.

    Article  CAS  PubMed  Google Scholar 

  8. Soufi, Y., & Soufi, B. (2016). Mass spectrometry-based bacterial proteomics: Focus on dermatologic microbial pathogens. Frontiers in Microbiology, 7, 181.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Chenau, J., Michelland, S., Sidibe, J., & Seve, M. (2008). Peptides OFFGEL electrophoresis: A suitable pre-analytical step for complex eukaryotic samples fractionation compatible with quantitative iTRAQ labeling. Proteome Science, 6, 9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Perez-Llarena, F. J., & Bou, G. (2016). Proteomics as a tool for studying bacterial virulence and antimicrobial resistance. Frontiers in Microbiology, 7, 410.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Graham, R. L., Graham, C., & McMullan, G. (2007). Microbial proteomics: A mass spectrometry primer for biologists. Microbial Cell Factories, 6, 26.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Stekhoven, D. J., Omasits, U., Quebatte, M., Dehio, C., & Ahrens, C. H. (2014). Proteome-wide identification of predominant subcellular protein localizations in a bacterial model organism. Journal of Proteomics, 99, 123–137.

    Article  CAS  PubMed  Google Scholar 

  13. Land, M., Hauser, L., Jun, S. R., Nookaew, I., Leuze, M. R., Ahn, T. H., et al. (2015). Insights from 20 years of bacterial genome sequencing. Functional & Integrative Genomics, 15(2), 141–161.

    Article  CAS  Google Scholar 

  14. Bennett, G. M., & Moran, N. A. (2013). Small, smaller, smallest: The origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biology and Evolution, 5(9), 1675–1688.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Han, K., Li, Z. F., Peng, R., Zhu, L. P., Zhou, T., Wang, L. G., et al. (2013). Extraordinary expansion of a Sorangium cellulosum genome from an alkaline milieu. Scientific Reports, 3, 2101.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Metzker, M. L. (2010). Applications of next-generation sequencing sequencing technologies - the next generation. Nature Reviews Genetics, 11(1), 31–46.

    Article  CAS  PubMed  Google Scholar 

  17. Weinstock, G. M. (2000). Genomics and bacterial pathogenesis. Emerging Infectious Diseases, 6(5), 496–504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Woodson, S. A. (1998). Ironing out the kinks: Splicing and translation in bacteria. Genes & Development, 12(9), 1243–1247.

    Article  CAS  Google Scholar 

  19. Hausner, G., Hafez, M., & Edgell, D. R. (2014). Bacterial group I introns: Mobile RNA catalysts. Mobile DNA, 5(1), 8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Potel, C. M., Lin, M. H., Heck, A. J. R., & Lemeer, S. (2018). Widespread bacterial protein histidine phosphorylation revealed by mass spectrometry-based proteomics. Nature Methods, 15(3), 187–190.

    Article  CAS  PubMed  Google Scholar 

  21. Cain, J. A., Solis, N., & Cordwell, S. J. (2014). Beyond gene expression: The impact of protein post-translational modifications in bacteria. Journal of Proteomics, 97, 265–286.

    Article  CAS  PubMed  Google Scholar 

  22. Perler, F. B., Davis, E. O., Dean, G. E., Gimble, F. S., Jack, W. E., Neff, N., et al. (1994). Protein splicing elements - Inteins and Exteins - a definition of terms and recommended nomenclature. Nucleic Acids Research, 22(7), 1125–1127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Shah, N. H., & Muir, T. W. (2014). Inteins: Nature’s gift to protein chemists. Chemical Science, 5(2), 446–461.

    Article  CAS  PubMed  Google Scholar 

  24. Chen, B., Zhang, D., Wang, X., Ma, W., Deng, S., Zhang, P., et al. (2017). Proteomics progresses in microbial physiology and clinical antimicrobial therapy. European Journal of Clinical Microbiology & Infectious Diseases, 36(3), 403–413.

    Article  CAS  Google Scholar 

  25. Otto, A., Bernhardt, J., Hecker, M., & Becher, D. (2012). Global relative and absolute quantitation in microbial proteomics. Current Opinion in Microbiology, 15(3), 364–372.

    Article  CAS  PubMed  Google Scholar 

  26. Chaussee, M. A., McDowell, E. J., Rieck, L. D., Callegari, E. A., & Chaussee, M. S. (2006). Proteomic analysis of a penicillin-tolerant rgg mutant strain of Streptococcus pyogenes. Journal of Antimicrobial Chemotherapy, 58(4), 752–759.

    Article  CAS  Google Scholar 

  27. Tiwari, V., Vashistt, J., Kapil, A., & Moganty, R. R. (2012). Comparative proteomics of inner membrane fraction from carbapenem-resistant Acinetobacter baumannii with a reference strain. PLoS One, 7(6), e39451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chen, H. B., Liu, Y. L., Zhao, C. J., Xiao, D., Zhang, J. Z., Zhang, F. F., et al. (2013). Comparative proteomics-based identification of genes associated with glycopeptide resistance in clinically derived heterogeneous vancomycin-intermediate Staphylococcus aureus strains. PLoS One, 8(6), e66880.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Straus, S. K., & Hancock, R. E. (2006). Mode of action of the new antibiotic for gram-positive pathogens daptomycin: Comparison with cationic antimicrobial peptides and lipopeptides. Biochimica et Biophysica Acta, 1758(9), 1215–1223.

    Article  CAS  PubMed  Google Scholar 

  30. Maria-Neto, S., Candido, E. D., Rodrigues, D. R., de Sousa, D. A., da Silva, E. M., de Moraes, L. M. P., et al. (2012). Deciphering the magainin resistance process of Escherichia coli strains in light of the cytosolic proteome. Antimicrobial Agents and Chemotherapy, 56(4), 1714–1724.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Fernandez-Reyes, M., Rodriguez-Falcon, M., Chiva, C., Pachon, J., Andreu, D., & Rivas, L. (2009). The cost of resistance to colistin in Acinetobacter baumannii: A proteomic perspective. Proteomics, 9(6), 1632–1645.

    Article  CAS  PubMed  Google Scholar 

  32. Vranakis, I., De Bock, P. J., Papadioti, A., Tselentis, Y., Gevaert, K., Tsiotis, G., et al. (2012). Quantitative proteome profiling of C. burnetii under tetracycline stress conditions. PLoS One, 7(3), e33599.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Biot, F. V., Valade, E., Garnotel, E., Chevalier, J., Villard, C., Thibault, F. M., et al. (2011). Involvement of the efflux pumps in chloramphenicol selected strains of Burkholderia thailandensis: Proteomic and mechanistic evidence. PLoS One, 6(2), e16892.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Rao, A. A., Patkari, M., Reddy, P. J., Srivastava, R., Pendharkar, N., Rapole, S., et al. (2014). Proteomic analysis of Streptomyces coelicolor in response to ciprofloxacin challenge. Journal of Proteomics, 97, 222–234.

    Article  CAS  PubMed  Google Scholar 

  35. Beck, M., Malmstrom, J. A., Lange, V., Schmidt, A., Deutsch, E. W., & Aebersold, R. (2009). Visual proteomics of the human pathogen Leptospira interrogans. Nature Methods, 6(11), 817–U55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Ansong, C., Schrimpe-Rutledge, A. C., Mitchell, H. D., Chauhan, S., Jones, M. B., Kim, Y. M., et al. (2013). A multi-omic systems approach to elucidating Yersinia virulence mechanisms. Molecular BioSystems, 9(1), 44–54.

    Article  CAS  PubMed  Google Scholar 

  37. Mirrashidi, K. M., Elwell, C. A., Verschueren, E., Johnson, J. R., Frando, A., Von Dollen, J., et al. (2015). Global mapping of the inc-human interactome reveals that retromer restricts chlamydia infection. Cell Host & Microbe, 18(1), 109–121.

    Article  CAS  Google Scholar 

  38. Boulund, F., Karlsson, R., Gonzales-Siles, L., Johnning, A., Karami, N., Al-Bayati, O., et al. (2017). Typing and characterization of bacteria using bottom-up tandem mass spectrometry proteomics. Molecular & Cellular Proteomics, 16(6), 1052–1063.

    Article  CAS  Google Scholar 

  39. Demirev, P. A., & Fenselau, C. (2008). Mass spectrometry for rapid characterization of microorganisms. Annual Review of Analytical Chemistry, 1, 71–93.

    Article  CAS  PubMed  Google Scholar 

  40. Charretier, Y., Dauwalder, O., Franceschi, C., Degout-Charmette, E., Zambardi, G., Cecchini, T., et al. (2015). Rapid bacterial identification, resistance, virulence and type profiling using selected reaction monitoring mass spectrometry. Scientific Reports, 5, 13944.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Gil, C., & Monteoliva, L. (2014). Trends in microbial proteomics. Journal of Proteomics, 97, 1–2.

    Article  CAS  PubMed  Google Scholar 

  42. Wilmes, P., & Bond, P. L. (2004). The application of two-dimensional polyacrylamide gel electrophoresis and downstream analyses to a mixed community of prokaryotic microorganisms. Environmental Microbiology, 6(9), 911–920.

    Article  CAS  PubMed  Google Scholar 

  43. Herbst, F. A., Lunsmann, V., Kjeldal, H., Jehmlich, N., Tholey, A., von Bergen, M., et al. (2016). Enhancing metaproteomics—the value of models and defined environmental microbial systems. Proteomics, 16(5), 783–798.

    Article  CAS  PubMed  Google Scholar 

  44. Haange, S. B., Oberbach, A., Schlichting, N., Hugenholtz, F., Smidt, H., von Bergen, M., et al. (2012). Metaproteome analysis and molecular genetics of rat intestinal microbiota reveals section and localization resolved species distribution and enzymatic functionalities. Journal of Proteome Research, 11(11), 5406–5417.

    Article  CAS  PubMed  Google Scholar 

  45. Vizcaino, J. A., Cote, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., et al. (2013). The PRoteomics IDEntifications (PRIDE) database and associated tools: Status in 2013. Nucleic Acids Research, 41(Database issue), D1063–D1069.

    CAS  PubMed  Google Scholar 

  46. Broadbent, J. A., Broszczak, D. A., Tennakoon, I. U. K., & Huygens, F. (2016). Pan-proteomics, a concept for unifying quantitative proteome measurements when comparing closely-related bacterial strains. Expert Review of Proteomics, 13(4), 355–365.

    Article  CAS  PubMed  Google Scholar 

  47. Fisunov, G. Y., Alexeev, D. G., Bazaleev, N. A., Ladygina, V. G., Galyamina, M. A., Kondratov, I. G., et al. (2011). Core proteome of the minimal cell: Comparative proteomics of three mollicute species. PLoS One, 6(7), e21964.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Yang, L., Tan, J., O’Brien, E. J., Monk, J. M., Kim, D., Li, H. J., et al. (2015). Systems biology definition of the core proteome of metabolism and expression is consistent with high-throughput data. Proceedings of the National Academy of Sciences of the United States of America, 112(34), 10810–10815.

    Article  CAS  Google Scholar 

  49. Decker, K., Eberwein, H., Gries, F. A., & Bruehmueller, M. (1960). On the degradation of nicotine by bacterial enzymes. Hoppe-Seyler’s Zeitschrift für Physiologische Chemie, 319, 279–282.

    Article  CAS  PubMed  Google Scholar 

  50. Kodama, Y., Yamamoto, H., Amano, N., & Amachi, T. (1992). Reclassification of two strains of Arthrobacter oxydans and proposal of Arthrobacter nicotinovorans sp. nov. International Journal of Systematic Bacteriology, 42(2), 234–239.

    Article  CAS  PubMed  Google Scholar 

  51. Busse, H. J. (2016). Review of the taxonomy of the genus Arthrobacter, emendation of the genus Arthrobacter sensu lato, proposal to reclassify selected species of the genus Arthrobacter in the novel genera Glutamicibacter gen. nov., Paeniglutamicibacter gen. nov., Pseudoglutamicibacter gen. nov., Paenarthrobacter gen. nov and Pseudarthrobacter gen. nov., and emended description of Arthrobacter roseus. International Journal of Systematic and Evolutionary Microbiology, 66, 9–37.

    Article  CAS  PubMed  Google Scholar 

  52. Igloi, G. L., & Brandsch, R. (2003). Sequence of the 165-kilobase catabolic plasmid pAO1 from Arthrobacter nicotinovorans and identification of a pAO1-dependent nicotine uptake system. Journal of Bacteriology, 185(6), 1976–1986.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Liu, J. L., Ma, G. H., Chen, T., Hou, Y., Yang, S. H., Zhang, K. Q., et al. (2015). Nicotine-degrading microorganisms and their potential applications. Applied Microbiology and Biotechnology, 99(9), 3775–3785.

    Article  CAS  PubMed  Google Scholar 

  54. Hritcu, L., & Mihasan, M. (2019). 6-hydroxy-l-nicotine and memory impairment. In V. Preedy (Ed.), The neuroscience of nicotine: Mechanisms and treatment. Academic Press.

    Google Scholar 

  55. Hritcu, L., Ionita, R., Motei, D. E., Babii, C., Stefan, M., & Mihasan, M. (2017). Nicotine versus 6-hydroxy-l-nicotine against chlorisondamine induced memory impairment and oxidative stress in the rat hippocampus. Biomedicine & Pharmacotherapy, 86, 102–108.

    Article  CAS  Google Scholar 

  56. Wang, S. N., Xu, P., Tang, H. Z., Meng, J., Liu, X. L., & Ma, C. Q. (2005). “Green” route to 6-hydroxy-3-succinoyl-pyridine from (S)-nicotine of tobacco waste by whole cells of a Pseudomonas sp. Environmental Science & Technology, 39(17), 6877–6880.

    Article  CAS  Google Scholar 

  57. Wang, W. W., Xu, P., & Tang, H. Z. (2015). Sustainable production of valuable compound 3-succinoyl-pyridine by genetically engineering Pseudomonas putida using the tobacco waste. Scientific Reports, 5, 16411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Yu, W. J., Wang, R. S., Li, H. L., Liang, J. Y., Wang, Y. Y., Huang, H. Y., et al. (2017). Green route to synthesis of valuable chemical 6-hydroxynicotine from nicotine in tobacco wastes using genetically engineered agrobacterium tumefaciens S33. Biotechnology for Biofuels, 10, 288.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Brandsch, R. (2006). Microbiology and biochemistry of nicotine degradation. Applied Microbiology and Biotechnology, 69(5), 493–498.

    Article  CAS  PubMed  Google Scholar 

  60. Chiribau, C. B., Mihasan, M., Ganas, P., Igloi, G. L., Artenie, V., & Brandsch, R. (2006). Final steps in the catabolism of nicotine. The FEBS Journal, 273(7), 1528–1536.

    Article  CAS  PubMed  Google Scholar 

  61. Ganas, P., Igloi, G. L., & Brandsch, R. (2009). The megaplasmid pAO1 of Arthrobacter nicotinovorans and nicotine catabolism. In E. Schwartz (Ed.), Microbial megaplasmids (pp. 271–282).

    Chapter  Google Scholar 

  62. Vandera, E., Samiotaki, M., Parapouli, M., Panayotou, G., & Koukkou, A. I. (2015). Comparative proteomic analysis of Arthrobacter phenanthrenivorans Sphe3 on phenanthrene, phthalate and glucose. Journal of Proteomics, 113, 73–89.

    Article  CAS  PubMed  Google Scholar 

  63. Wetie, A. G. N., Wormwood, K. L., Charette, L., Ryan, J. P., Woods, A. G., & Darie, C. C. (2015). Comparative two-dimensional polyacrylamide gel electrophoresis of the salivary proteome of children with autism spectrum disorder. Journal of Cellular and Molecular Medicine, 19(11), 2664–2678.

    Article  CAS  Google Scholar 

  64. Channaveerappa, D., Lux, J. C., Wormwood, K. L., Heintz, T. A., McLerie, M., Treat, J. A., et al. (2017). Atrial electrophysiological and molecular remodelling induced by obstructive sleep apnoea. Journal of Cellular and Molecular Medicine, 21(9), 2223–2235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Maor, R., Jones, A., Nuhse, T. S., Studholme, D. J., Peck, S. C., & Shirasu, K. (2007). Multidimensional protein identification technology (MudPIT) analysis of ubiquitinated proteins in plants. Molecular & Cellular Proteomics, 6(4), 601–610.

    Article  CAS  Google Scholar 

  66. Delahunty, C. M., & Yates, J. R. (2007). MudPIT: Multidimensional protein identification technology. BioTechniques, 43(5), 563–56+.

    CAS  PubMed  Google Scholar 

  67. Mongodin, E. F., Shapir, N., Daugherty, S. C., Deboy, R. T., Emerson, J. B., Shvartzbeyn, A., et al. (2006). Secrets of soil survival revealed by the genome sequence of Arthrobacter aurescens TC1. PLoS Genetics, 2(12), 2094–2106.

    Article  CAS  Google Scholar 

  68. Meng, J., Sun, X., Li, S., & Liang, H. (2017). Draft genome sequence of Paenarthrobacter nicotinovorans Hce-1. Genome Announcements, 5(30), e00727–e00717.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Oren, A., & Garrity, G. M. (2016). Notification that new names of prokaryotes, new combinations, and new taxonomic opinions have appeared in volume 66, part 2, of the IJSEM (vol 66, pg 1916, 2016). International Journal of Systematic and Evolutionary Microbiology, 66, 2455–2455.

    Article  PubMed  Google Scholar 

  70. Unell, M., Abraham, P. E., Shah, M., Zhang, B., Ruckert, C., VerBerkmoes, N. C., et al. (2009). Impact of phenolic substrate and growth temperature on the Arthrobacter chlorophenolicus proteome. Journal of Proteome Research, 8(4), 1953–1964.

    Article  CAS  PubMed  Google Scholar 

  71. Burnett, B. J., Altman, R. B., Ferguson, A., Wasserman, M. R., Zhou, Z., & Blanchard, S. C. (2014). Direct evidence of an elongation factor-Tu/Ts.GTP.Aminoacyl-tRNA quaternary complex. Journal of Biological Chemistry, 289(34), 23917–23927.

    Article  CAS  Google Scholar 

  72. Zeilstraryalls, J., Fayet, O., & Georgopoulos, C. (1991). The universally conserved Groe (Hsp60) chaperonins. Annual Review of Microbiology, 45, 301–325.

    Article  CAS  Google Scholar 

  73. Ganas, P., Mihasan, M., Igloi, G. L., & Brandsch, R. (2007). A two-component small multidrug resistance pump functions as a metabolic valve during nicotine catabolism by Arthrobacter nicotinovorans. Microbiology, 153, 1546–1555.

    Article  CAS  PubMed  Google Scholar 

  74. Chiribau, C. B., Sandu, C., Fraaije, M., Schiltz, E., & Brandsch, R. (2004). A novel gamma-N-methylaminobutyrate demethylating oxidase involved in catabolism of the tobacco alkaloid nicotine by Arthrobacter nicotinovorans pAO1. European Journal of Biochemistry, 271(23–24), 4677–4684.

    Article  CAS  PubMed  Google Scholar 

  75. Caspi, R., Billington, R., Ferrer, L., Foerster, H., Fulcher, C. A., Keseler, I. M., et al. (2016). The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Research, 44(D1), D471–D480.

    Article  CAS  PubMed  Google Scholar 

  76. Kurnasov, O., Jablonski, L., Polanuyer, B., Dorrestein, P., Begley, T., & Osterman, A. (2003). Aerobic tryptophan degradation pathway in bacteria: Novel kynurenine formamidase. FEMS Microbiology Letters, 227(2), 219–227.

    Article  CAS  PubMed  Google Scholar 

  77. Cobzaru, C., Ganas, P., Mihasan, M., Schleberger, P., & Brandsch, R. (2011). Homologous gene clusters of nicotine catabolism, including a new omega-amidase for alpha-ketoglutaramate, in species of three genera of gram-positive bacteria. Research in Microbiology, 162(3), 285–291.

    Article  CAS  PubMed  Google Scholar 

  78. Vaitekunas, J., Gasparaviciute, R., Rutkiene, R., Tauraite, D., & Meskys, R. (2016). A 2-hydroxypyridine catabolism pathway in Rhodococcus rhodochrous strain PY11. Applied and Environmental Microbiology, 82(4), 1264–1273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Fan, J., Teng, X., Liu, L., Mattaini, K. R., Looper, R. E., Vander Heiden, M. G., et al. (2015). Human phosphoglycerate dehydrogenase produces the oncometabolite D-2-hydroxyglutarate. ACS Chemical Biology, 10(2), 510–516.

    Article  CAS  PubMed  Google Scholar 

  80. Mihasan, M., Chiribau, C. B., Friedrich, T., Artenie, V., & Brandsch, R. (2007). An NAD(P)H-nicotine blue oxidoreductase is part of the nicotine regulon and may protect Arthrobacter nicotinovorans from oxidative stress during nicotine catabolism. Applied and Environmental Microbiology, 73(8), 2479–2485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Kallimanis, A., Kavakiotis, K., Perisynakis, A., Sproer, C., Pukall, R., Drainas, C., et al. (2009). Arthrobacter phenanthrenivorans sp nov., to accommodate the phenanthrene-degrading bacterium Arthrobacter sp strain Sphe3. International Journal of Systematic and Evolutionary Microbiology, 59, 275–279.

    Article  CAS  PubMed  Google Scholar 

  82. Sahoo, N. K., Pakshirajan, K., & Ghosh, P. K. (2010). Enhancing the biodegradation of 4-chlorophenol by Arthrobacter chlorophenolicus A6 via medium development. International Biodeterioration & Biodegradation, 64(6), 474–480.

    Article  CAS  Google Scholar 

  83. Borodina, E., Kelly, D. P., Schumann, P., Rainey, F. A., Ward-Rainey, N. L., & Wood, A. P. (2002). Enzymes of dimethylsulfone metabolism and the phylogenetic characterization of the facultative methylotrophs Arthrobacter sulfonivorans sp nov., Arthrobacter methylotrophus sp nov., and Hyphomicrobium sulfonivorans sp. Archives of Microbiology, 177(2), 173–183.

    Article  CAS  PubMed  Google Scholar 

  84. Sagarkar, S., Bhardwaj, P., Storck, V., Devers-Lamrani, M., Martin-Laurent, F., & Kapley, A. (2016). s-triazine degrading bacterial isolate Arthrobacter sp AK-YN10, a candidate for bioaugmentation of atrazine contaminated soil. Applied Microbiology and Biotechnology, 100(2), 903–913.

    Article  CAS  PubMed  Google Scholar 

  85. Mihasan, M. (2015). Bioinformatics-based molecular classification of Arthrobacter plasmids. Cellular & Molecular Biology Letters, 20(4), 612–625.

    Article  CAS  Google Scholar 

  86. Mihasan, M., & Brandsch, R. (2013). pAO1 of Arthrobacter nicotinovorans and the spread of catabolic traits by horizontal gene transfer in gram-positive soil Bacteria. Journal of Molecular Evolution, 77(1–2), 22–30.

    Article  CAS  PubMed  Google Scholar 

  87. Mihasan, M., & Brandsch, R. (2016). A predicted T4 secretion system and conserved DNA-repeats identified in a subset of related Arthrobacter plasmids. Microbiological Research, 191, 32–37.

    Article  CAS  PubMed  Google Scholar 

  88. Meyer, R. R., & Laine, P. S. (1990). The single-stranded DNA-binding protein of Escherichia-Coli. Microbiological Reviews, 54(4), 342–380.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank the past and present members of BioActive Group and the Biochemistry & Proteomics Group for the pleasant environment and fruitful discussions. MM was supported by the Fulbright Senior Postdoctoral Fellowship awarded by the Romania-USA Fulbright Commission to MM (guest) and CCD (host).

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Authors and Affiliations

  1. BioActive Group, Department of Biology, Alexandru Ioan Cuza University of Iaşi, Iasi, Romania

    Marius Mihăşan & Cornelia Babii

  2. Biochemistry & Proteomics Group, Department of Chemistry & Biomolecular Science, Clarkson University, Potsdam, NY, USA

    Marius Mihăşan, Roshanak Aslebagh, Devika Channaveerappa, Emmalyn J. Dupree & Costel C. Darie

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  1. Marius Mihăşan
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  2. Cornelia Babii
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  3. Roshanak Aslebagh
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  5. Emmalyn J. Dupree
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  6. Costel C. Darie
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Correspondence to Marius Mihăşan .

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  1. Biochemistry and Proteomics Group, Department of Chemistry and Biomolecular Science, Clarkson University, Potsdam, NY, USA

    Alisa G. Woods

  2. Biochemistry and Proteomics Group, Department of Chemistry and Biomolecular Science, Clarkson University, Potsdam, NY, USA

    Costel C. Darie

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Mihăşan, M., Babii, C., Aslebagh, R., Channaveerappa, D., Dupree, E.J., Darie, C.C. (2019). Exploration of Nicotine Metabolism in Paenarthrobacter nicotinovorans pAO1 by Microbial Proteomics. In: Woods, A., Darie, C. (eds) Advancements of Mass Spectrometry in Biomedical Research. Advances in Experimental Medicine and Biology, vol 1140. Springer, Cham. https://doi.org/10.1007/978-3-030-15950-4_30

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