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l-Proline catabolism by the high G + C Gram-positive bacterium Paenarthrobacter aurescens strain TC1

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Abstract

Paenarthrobacter aurescens (formerly called Arthrobacter aurescens) strain TC1 is a high G + C Gram-positive aerobic bacterium that can degrade the herbicide atrazine. Analysis of its genome indicated strain TC1 has the potential to form a bifunctional PutA protein containing l-proline dehydrogenase and l-glutamate-γ-semialdehyde dehydrogenase (l-Δ1-pyrroline-5-carboxylate dehydrogenase) activities. P. aurescens strain TC1 grew well in minimal media with l-Proline as a supplemental nutrient, the nitrogen source, or the sole carbon and nitrogen source. Multicellular myceloids induced by NaCl or citrate also grew on l-proline. The specific activity of l-proline dehydrogenase in whole cells was higher whenever l-proline was added to the medium. Both l-proline dehydrogenase and l-glutamate-γ-semialdehyde dehydrogenase (l-Δ1-pyrroline-5-carboxylate dehydrogenase) activities were found primarily in a membrane fraction from exponential-phase cells. The two activities co-eluted from a Bio-Gel P-60 column after precipitation of proteins with ammonium sulfate and solubilization with 0.1% Tween 20. The PutA protein in the active fraction also oxidized 3,4-dehydro-dl-proline, but there was no activity with other l-proline analogues. When P. aurescens strain TC1 was grown in minimal media containing increasing concentrations of NaCl, there was a progressive decrease in the specific activity of l-proline dehydrogenase and a concomitant increase in the intracellular concentration of l-proline. These results indicate that P. aurescens strain TC1 can use l-proline as a nutrient in a regulated fashion. Because this bacterium also showed the ability to degrade most of the other common amino acids, it can serve as a useful model for the control of amino acid catabolism in the high G + C Actinobacteria.

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References

  • Adams E, Frank L (1980) Metabolism of proline and the hydroxyprolines. Ann Rev Biochem 49:1005–1061

    Article  CAS  PubMed  Google Scholar 

  • Anon (2016) American type culture collection. Manassas. https://www.atcc.org/~/media/A4CF742B46514D579AAEB111AA55E7F9.ashx. Accessed 25 August 2016

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Belitsky B (2011) Indirect repression by Bacillus subtilis CodY via displacement of the activator of the proline utilization operon. J Mol Biol 413:321–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berney M, Weimar MR, Heikal Cook GM (2012) Regulation of proline metabolism in mycobacteria and its role in carbon metabolism under hypoxia. Mol Microbiol 84:664–681

    Article  CAS  Google Scholar 

  • Bochner BR, Savageau MA (1977) Generalized indicator plate for genetic, metabolic, and taxonomic studies with microorganisms. J Bacteriol 33:434–444

    CAS  Google Scholar 

  • Bott M, Niebisch A (2003) The respiratory chain of Corynebacterium glutamicum. J Biotechnol 104:129–153

    Article  CAS  PubMed  Google Scholar 

  • Brown ED, Wood JM (1992) Redesigned purification yields a fully functional PutA protein dimer from Escherichia coli. J Biol Chem 267:13086–13092

    CAS  PubMed  Google Scholar 

  • Busse HJ (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., Pseudoglutamibacter gen. nov., Paenarthrobacter gen. nov., and Pseudarthrobacter gen. nov. and emended description of Arthrobacter roseus. Int J Syst Evol Microbiol 66:9–37

    Article  CAS  PubMed  Google Scholar 

  • Chan ECS, Zyk B, Gomersall M (1973) Biotin deficiency in Arthrobacter globiformis: comparative cell ultrastructure and nonreplacement of the compound by structurally unrelated compounds. J Bacteriol 113:394–402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, An L, Fan X, Ju F, Zhang B, S H, Xiao J, Hu W, Qu T, Guan L, Tang S, Chen T, Liu G, Dyson P (2017) A trehalose biosynthetic enzyme doubles as an osmotic sensor to regulate bacterial morphogenesis. PLoS Genet 13:e1007062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho K, Winans SC (1996) The putA gene of Agrobacterium tumefaciens is transcriptionally activated by an Lrp-like protein and is not autoregulated. Mol Microbiol 22:1025–1033

    Article  CAS  PubMed  Google Scholar 

  • Christgen SL, Becker DF (2018) Role of proline in pathogen and host interactions. Antioxid Redox Signal. https://doi.org/10.1089/ars.2017.7335

    Article  PubMed  Google Scholar 

  • Combet C, Blanchet C, Geourjon C, Deléage G (2000) NPS@: network protein sequence analysis. Trends Biochem Sci 25:147–150

    Article  CAS  Google Scholar 

  • Dendinger S, Brill WJ (1970) Regulation of proline degradation in Salmonella typhimurium. J Bacteriol 103:144–152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deutch CE (1992) Oxidation of l-thiazolidine-4-carboxylate by l-proline dehydrogenase in Escherichia coli. J Gen Microbiol 138:1593–1598

    Article  CAS  PubMed  Google Scholar 

  • Deutch CE (2004) Oxidation of 3,4-dehydro-d-proline and other d-amino acid analogues by d-alanine dehydrogenase from Escherichia coli. FEMS Microbiol Lett 238:383–389

    CAS  PubMed  Google Scholar 

  • Deutch CE (2011) l-Proline nutrition and catabolism in Staphylococcus saprophyticus. Antonie van Leeuwenhoek 99:781–793

    Article  CAS  PubMed  Google Scholar 

  • Deutch CE, Perera GS (1992) Myceloid cell formation in Arthrobacter globiformis during osmotic stress. J Appl Bacteriol 72:493–499

    Article  CAS  PubMed  Google Scholar 

  • Deutch CE, Hasler JM, Houston RM, Sharma M, Stone VJ (1989) Nonspecific inhibition of proline dehydrogenase synthesis in Escherichia coli during osmotic stress. Can J Microbiol 35:779–785

    Article  CAS  PubMed  Google Scholar 

  • Deutch CE, Klarstrom JL, Link CL, Ricciardi DL (2001) Oxidation of l-thiazolidie-4-carboxylate by Δ1-pyrroline-5-carboxylate reductase in Escherichia coli. Curr Microbiol 42:442–446

    Article  CAS  PubMed  Google Scholar 

  • Germida JJ, Casida LE Jr (1980) Myceloid growth of Arthrobacter globiformis and other Arthrobacter species. J Bacteriol 144:1152–1158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hodgson DA (2000) Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv Microb Physiol 42:47–238

    Article  CAS  PubMed  Google Scholar 

  • Huang SC, Lin TH, Shaw GC (2011) PrcR, PucR-type transcriptional activator, is essential for proline utilization and mediates proline-responsive expression of the proline utilization operon putBCP in Bacillus subtilis. Microbiology 157:3370–3377

    Article  CAS  PubMed  Google Scholar 

  • Korasick DA, Gamage TT, Christgen S, Stiers KM, Beamer LJ, Henzl MT, Becker DF, Tanner JJ (2017) Structure and characterization of a class 3B proline utilization A: ligand-induced dimerization and importance of the C-terminal domain for catalysis. J Biol Chem 292:9652–9665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang X, Zhang L, Natarajan K, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19:998–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu LK, Becker DF, Tanner JJ (2017) Structure, function, and mechanism of proline utilization A (PutA). Arch Biochem Biophys 632:142–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malwane S, Deutch CE (1999) Adaptive characteristics of salt-induced myceloids of Arthrobacter globiformis. Antonie van Leeuwenhoek 75:335–344

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Stein H, Honig A, Kapulnik Y, Zilberstein A (2005) Responsive modes of Medicago sativa proline dehydrogenase genes during salt stress and recovery dictate free proline accumulation. Planta 225:70–79

    Article  CAS  Google Scholar 

  • Mongodin EF, Shapir N, Daugherty SC, DeBoy RT, Emerson JB, Shvartzbeyn A, Radune D, Vamathevan J, Riggs F, Grinberg V, Khouri H, Wackett LP, Nelson KE, Sadowsky MJ (2006) Secrets of soil survival revealed by the genome sequence of Arthrobacter aurescens TC1. PLoS Genet 2:2094–2105

    Article  CAS  Google Scholar 

  • Monnet C, Loux V, Gibrat JF, Sinnier E, Barbe V, Vacherie B, Gavory F, Gourbeyre E, Siguier P, Chandler M, Elleuch R, Irlinger F, Vallaeysn T (2010) The Arthrobacter arilaitensis Re117 genome sequence reveals its genetic adaptation to the surface of cheese. PLoS ONE 11:e15489

    Article  CAS  Google Scholar 

  • Moses S, Sinner T, Zaprasis A, Stöveken N, Hoffmann T, Belitsky BR, Sonenshein AL, Bremer E (2012) Proline utilization by Bacillus subtilis: uptake and catabolism. J Bacteriol 194:745–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nuxoll AS, Halouska SM, Sadykov MR, Hanke ML, Bayles KW, Kielian T, Powers R, Fey PD (2012) CcpA regulates arginine biosynthesis in Staphylococcus aureus through repression of proline catabolism. PLoS Pathog 8:e1003033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peter H, Bader A, Burkovski A, Lambert C, Krämer R (1997) Isolation of the putP gene of q\Corynebacterium glutamicum and characterization of a low-affinity uptake system for compatible solutes. Arch Microbiol 168:143–151

    Article  CAS  PubMed  Google Scholar 

  • Peter H, Weil B, Burkovski A, Krämer R, Morbach S (1998) Corynebacterium glutamicum is equipped with four secondary carriers for compatible solutes: identification, sequencing, and characterization of the proline/ectoine uptake system, ProP, and the ectoine/proline/glycine betaine carrier, EctP. J Bacteriol 180:6005–6012

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scarpulla RC, Soffer RL (1978) Membrane-bound proline dehydrogenase from Escherichia coli: solubilization, purification, and characterization. J Biol Chem 253:5997–6001

    CAS  PubMed  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Malina AK, Gartner FH, Provensano MD, Fugimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  • Strong LC, Rosendahl C, Johnson G, Sadowsky MJ, Wackett LP (2002) Arthrobacter aurescens TC1 metabolizes diverse s-triazine ring compounds. Appl Environ Microbiol 68:5973–5980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutthiwong N, Dufossé L (2014) Production of carotenoids by Arthrobacter arilaitensis strains isolated from smear-ripened cheeses. FEMS Microbiol Lett 360:174–181

    Article  CAS  PubMed  Google Scholar 

  • Tanner JJ (2008) Structural biology of proline catabolism. Amino Acids 35:719–730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, van Sinderen D (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71:495–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams I, Frank L (1975) Improved chemical synthesis and enzymatic assay of Δ1-pyrroline-5-carboxylic acid. Anal Biochem 64:85–97

    Article  CAS  PubMed  Google Scholar 

  • Williamson NR, Fineran PC, Leeper FJ, Salmond GPC (2006) The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4:887–899

    Article  CAS  PubMed  Google Scholar 

  • Wood JM (1981) Genetics of l-proline utilization in Escherichia coli. J Bacteriol 146:895–901

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wood JM (1988) Proline porters effect the utilization of proline as nutrient or osmoprotectant for bacteria. J Membr Biol 106:183–202

    Article  CAS  PubMed  Google Scholar 

  • Wood JM (2011) Bacterial osmoregulation: a paradigm for the study of cellular homeostasis. Annu Rev Microbiol 65:215–238

    Article  CAS  PubMed  Google Scholar 

  • Wood JM (2015) Bacterial responses to osmotic challenges. J Gen Physiol 145:381–388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, White TA, Schuermann JP, Baban BA, Becker DL, Tanner JJ (2004) Structures of the Escherichia coli PutA proline dehydrogenase domain in complex with competitive inhibitors. Biochemistry 43:12539–12548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Li Y, Chen X, Sheng H, An L (2011) Optimization of electroporation conditions for Arthrobacter with plasmid PART2. J Microbiol Methods 84:114–120

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Larson JD, Bottoms CA, Arturo EC, Henzl MT, Jenkins JL, Nix JC, Becker DF, Tanner JJ (2008) Structural basis of the transcriptional regulation of the proline utilization regulon by multifunctional PutA. J Mol Biol 381:174–188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

I thank Dr. Michael Sadowsky of the University of Minnesota for the culture of P. aurescens strain TC1 used in these studies. Disclaimer: some of these experiments were done off-campus and Arizona State University has no liability for that work.

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  1. All the experiments were designed and performed by Charles E. Deutch. He also created the figures and tables and wrote the manuscript.

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  1. School of Mathematical and Natural Sciences, MC 2352, Arizona State University at the West campus, 4701 W. Thunderbird Road, Glendale, AZ, 85306, USA

    Charles E. Deutch

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Correspondence to Charles E. Deutch.

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Deutch, C.E. l-Proline catabolism by the high G + C Gram-positive bacterium Paenarthrobacter aurescens strain TC1. Antonie van Leeuwenhoek 112, 237–251 (2019). https://doi.org/10.1007/s10482-018-1148-z

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