1887

Microbiology Society logo

Volume 170, Issue 3

Gene expression reprogramming of in response to arginine through the transcriptional regulator ArgR Open Access

Abstract

Different bacteria change their life styles in response to specific amino acids. In (now ) KT2440, arginine acts both as an environmental and a metabolic indicator that modulates the turnover of the intracellular second messenger c-di-GMP, and expression of biofilm-related genes. The transcriptional regulator ArgR, belonging to the AraC/XylS family, is key for the physiological reprogramming in response to arginine, as it controls transport and metabolism of the amino acid. To further expand our knowledge on the roles of ArgR, a global transcriptomic analysis of KT2440 and a null mutant growing in the presence of arginine was carried out. Results indicate that this transcriptional regulator influences a variety of cellular functions beyond arginine metabolism and transport, thus widening its regulatory role. ArgR acts as positive or negative modulator of the expression of several metabolic routes and transport systems, respiratory chain and stress response elements, as well as biofilm-related functions. The partial overlap between the ArgR regulon and those corresponding to the global regulators RoxR and ANR is also discussed.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): arginine , gene expression , metabolism , redox and regulation
Funding
This study was supported by the:
  • MCIN/AEI/10.13039/501100011033 (Award PID2019-109372GB-I00)
    • Principle Award Recipient: MaríaAntonia Molina-Henares
  • MCIN/AEI/10.13039/501100011033 (Award PID2019-109372GB-I00)
    • Principle Award Recipient: MaríaIsabel Ramos-González
  • MCIN/AEI/10.13039/501100011033 (Award PID2019-109372GB-I00)
    • Principle Award Recipient: ManuelEspinosa-Urgel
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001449
2024-03-21
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/170/3/mic001449.html?itemId=/content/journal/micro/10.1099/mic.0.001449&mimeType=html&fmt=ahah

References

  1. Nadell CD, Xavier JB, Foster KR. The sociobiology of biofilms. FEMS Microbiol Rev 2009; 33:206–224 [View Article] [PubMed]
     [Google Scholar]
  2. Tolker-Nielsen T. Biofilm development. Microbiol Spectr 2015; 3:MB–0001 [View Article] [PubMed]
     [Google Scholar]
  3. Sauer K, Stoodley P, Goeres DM, Hall-Stoodley L, Burmølle M et al. The biofilm life cycle: expanding the conceptual model of biofilm formation. Nat Rev Microbiol 2022; 20:608–620 [View Article] [PubMed]
     [Google Scholar]
  4. Valentini M, Filloux A. Biofilms and cyclic di-GMP (c-di-GMP) signaling: lessons from Pseudomonas aeruginosa and other bacteria. J Biol Chem 2016; 291:12547–12555 [View Article] [PubMed]
     [Google Scholar]
  5. Park S, Sauer K. Controlling biofilm development through cyclic di-GMP signaling. Adv Exp Med Biol 2022; 1386:69–94 [View Article] [PubMed]
     [Google Scholar]
  6. Hengge R, Pruteanu M, Stülke J, Tschowri N, Turgay K. Recent advances and perspectives in nucleotide second messenger signaling in bacteria. Microlife 2023; 4:uqad015 [View Article] [PubMed]
     [Google Scholar]
  7. Römling U. Cyclic di-GMP signaling-Where did you come from and where will you go?. Mol Microbiol 2023; 120:564–574 [View Article] [PubMed]
     [Google Scholar]
  8. Yu Z, Zhang W, Yang H, Chou SH, Galperin MY et al. Gas and light: triggers of c-di-GMP-mediated regulation. FEMS Microbiol Rev 2023; 47:fuad034 [View Article] [PubMed]
     [Google Scholar]
  9. Bernier SP, Ha DG, Khan W, Merritt JH, O’Toole GA. Modulation of Pseudomonas aeruginosa surface-associated group behaviors by individual amino acids through c-di-GMP signaling. Res Microbiol 2011; 162:680–688 [View Article] [PubMed]
     [Google Scholar]
  10. Paiardini A, Mantoni F, Giardina G, Paone A, Janson G et al. A novel bacterial L-arginine sensor controlling c-di-GMP levels in Pseudomonas aeruginosa. Proteins 2018; 86:1088–1096 [View Article] [PubMed]
     [Google Scholar]
  11. Kumar B, Sorensen JL, Cardona ST. A c-di-GMP-modulating protein regulates swimming motility of Burkholderia cenocepacia in response to arginine and glutamate. Front Cell Infect Microbiol 2018; 8:56 [View Article] [PubMed]
     [Google Scholar]
  12. Mills E, Petersen E, Kulasekara BR, Miller SI. A direct screen for c-di-GMP modulators reveals a Salmonella Typhimurium periplasmic ʟ-arginine-sensing pathway. Sci Signal 2015; 8:ra57 [View Article] [PubMed]
     [Google Scholar]
  13. Keshavarz-Tohid V, Vacheron J, Dubost A, Prigent-Combaret C, Taheri P et al. Genomic, phylogenetic and catabolic re-assessment of the Pseudomonas putida clade supports the delineation of Pseudomonas alloputida sp. nov., Pseudomonas inefficax sp. nov., Pseudomonas persica sp. nov., and Pseudomonas shirazica sp. nov. Syst Appl Microbiol 2019; 42:468–480 [View Article] [PubMed]
     [Google Scholar]
  14. Morimoto Y, Tohya M, Aibibula Z, Baba T, Daida H et al. Re-identification of strains deposited as Pseudomonas aeruginosa, Pseudomonas fluorescens and Pseudomonas putida in GenBank based on whole genome sequences. Int J Syst Evol Microbiol 2020; 70:5958–5963 [View Article]
     [Google Scholar]
  15. Espinosa-Urgel M, Ramos-González MI. Becoming settlers: elements and mechanisms for surface colonization by Pseudomonas putida. Environ Microbiol 2023; 25:1575–1593 [View Article] [PubMed]
     [Google Scholar]
  16. Costa-Gutierrez SB, Adler C, Espinosa-Urgel M, de Cristóbal RE. Pseudomonas putida and its close relatives: mixing and mastering the perfect tune for plants. Appl Microbiol Biotechnol 2022; 106:3351–3367 [View Article] [PubMed]
     [Google Scholar]
  17. Nikel PI, de Lorenzo V. Pseudomonas putida as a functional chassis for industrial biocatalysis: From native biochemistry to trans-metabolism. Metab Eng 2018; 50:142–155 [View Article] [PubMed]
     [Google Scholar]
  18. Ramos-González MI, Travieso ML, Soriano MI, Matilla MA, Huertas-Rosales Ó et al. Genetic dissection of the regulatory network associated with high c-di-GMP levels in Pseudomonas putida KT2440. Front Microbiol 2016; 7:1093 [View Article] [PubMed]
     [Google Scholar]
  19. Barrientos-Moreno L, Molina-Henares MA, Ramos-González MI, Espinosa-Urgel M. Arginine as an environmental and metabolic cue for cyclic diguanylate signalling and biofilm formation in Pseudomonas putida. Sci Rep 2020; 10:13623 [View Article] [PubMed]
     [Google Scholar]
  20. Barrientos-Moreno L, Molina-Henares MA, Ramos-González MI, Espinosa-Urgel M. Role of the transcriptional regulator ArgR in the connection between arginine metabolism and c-di-GMP signaling in Pseudomonas putida. Appl Environ Microbiol 2022; 88:e0006422 [View Article] [PubMed]
     [Google Scholar]
  21. Park SM, Lu CD, Abdelal AT. Purification and characterization of an arginine regulatory protein, ArgR, from Pseudomonas aeruginosa and its interactions with the control regions for the car, argF, and aru operons. J Bacteriol 1997; 179:5309–5317 [View Article]
     [Google Scholar]
  22. Caldara M, Charlier D, Cunin R. The arginine regulon of Escherichia coli: whole-system transcriptome analysis discovers new genes and provides an integrated view of arginine regulation. Microbiology 2006; 152:3343–3354 [View Article] [PubMed]
     [Google Scholar]
  23. Barrientos-Moreno L, Molina-Henares MA, Pastor-García M, Ramos-González MI, Espinosa-Urgel M. Arginine biosynthesis modulates pyoverdine production and release in Pseudomonas putida as part of the mechanism of adaptation to oxidative stress. J Bacteriol 2019; 201:e00454-19 [View Article] [PubMed]
     [Google Scholar]
  24. Scribani-Rossi C, Molina-Henares MA, Espinosa-Urgel M, Rinaldo S. Exploring the metabolic response of Pseudomonas putida to L-arginine. In Donelli G. eds Advances in Microbiology, Infectious Diseases and Public Health. Advances in Experimental Medicine and Biology Cham: Springer;
     [Google Scholar]
  25. Scribani Rossi C, Barrientos-Moreno L, Paone A, Cutruzzolà F, Paiardini A et al. Nutrient sensing and biofilm modulation: the example of L-arginine in Pseudomonas. Int J Mol Sci 2022; 23:4386 [View Article] [PubMed]
     [Google Scholar]
  26. Scribani-Rossi C, Molina-Henares MA, Angeli S, Cutruzzolà F, Paiardini A et al. The phosphodiesterase RmcA contributes to the adaptation of Pseudomonas putida to L-arginine. FEMS Microbiol Lett 2023; 370:fnad077 [View Article] [PubMed]
     [Google Scholar]
  27. Regenhardt D, Heuer H, Heim S, Fernandez DU, Strömpl C et al. Pedigree and taxonomic credentials of Pseudomonas putida strain KT2440. Environ Microbiol 2002; 4:912–915 [View Article] [PubMed]
     [Google Scholar]
  28. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual, 3rd ed Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2001
     [Google Scholar]
  29. Afgan E, Baker D, Batut B, van den Beek M, Bouvier D et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 2018; 46:W537–W544 [View Article] [PubMed]
     [Google Scholar]
  30. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013; 29:15–21 [View Article] [PubMed]
     [Google Scholar]
  31. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014; 30:923–930 [View Article] [PubMed]
     [Google Scholar]
  32. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139–140 [View Article] [PubMed]
     [Google Scholar]
  33. Liu R, Holik AZ, Su S, Jansz N, Chen K et al. Why weight? Modelling sample and observational level variability improves power in RNA-seq analyses. Nucleic Acids Res 2015; 43:e97 [View Article] [PubMed]
     [Google Scholar]
  34. Winsor GL, Griffiths EJ, Lo R, Dhillon BK, Shay JA et al. Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database. Nucleic Acids Res 2016; 44:D646–53 [View Article] [PubMed]
     [Google Scholar]
  35. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402–408 [View Article] [PubMed]
     [Google Scholar]
  36. Dudek CA, Jahn D. PRODORIC: state-of-the-art database of prokaryotic gene regulation. Nucleic Acids Res 2022; 50:D295–D302 [View Article] [PubMed]
     [Google Scholar]
  37. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14:1188–1190 [View Article] [PubMed]
     [Google Scholar]
  38. D’Arrigo I, Bojanovič K, Yang X, Holm Rau M, Long KS. Genome-wide mapping of transcription start sites yields novel insights into the primary transcriptome of Pseudomonas putida. Environ Microbiol 2016; 18:3466–3481 [View Article] [PubMed]
     [Google Scholar]
  39. Lu CD, Yang Z, Li W. Transcriptome analysis of the ArgR regulon in Pseudomonas aeruginosa. J Bacteriol 2004; 186:3855–3861 [View Article] [PubMed]
     [Google Scholar]
  40. Botas A, Pérez-Redondo R, Rodríguez-García A, Álvarez-Álvarez R, Yagüe P et al. ArgR of Streptomyces coelicolor is a pleiotropic transcriptional regulator: effect on the transcriptome, antibiotic production, and differentiation in liquid cultures. Front Microbiol 2018; 9:361 [View Article] [PubMed]
     [Google Scholar]
  41. Jo J, Cortez KL, Cornell WC, Price-Whelan A, Dietrich LEP. An orphan Cbb3-type cytochrome oxidase subunit supports Pseudomonas aeruginosa biofilm growth and virulence. eLife 2017 [View Article]
     [Google Scholar]
  42. Schmidt M, Pearson AN, Incha MR, Thompson MG, Baidoo EEK et al. Nitrogen metabolism in Pseudomonas putida: functional analysis using random barcode transposon sequencing. Appl Environ Microbiol 2022; 88:e0243021 [View Article] [PubMed]
     [Google Scholar]
  43. Daddaoua A, Krell T, Alfonso C, Morel B, Ramos JL. Compartmentalized glucose metabolism in Pseudomonas putida is controlled by the PtxS repressor. J Bacteriol 2010; 192:4357–4366 [View Article] [PubMed]
     [Google Scholar]
  44. Udaondo Z, Ramos JL, Segura A, Krell T, Daddaoua A. Regulation of carbohydrate degradation pathways in Pseudomonas involves a versatile set of transcriptional regulators. Microb Biotechnol 2018; 11:442–454 [View Article] [PubMed]
     [Google Scholar]
  45. Li SS, Hu X, Zhao H, Li YX, Zhang L et al. Quantitative analysis of cellular proteome alterations of Pseudomonas putida to naphthalene-induced stress. Biotechnol Lett 2015; 37:1645–1654 [View Article] [PubMed]
     [Google Scholar]
  46. Boes N, Schreiber K, Härtig E, Jaensch L, Schobert M. The Pseudomonas aeruginosa universal stress protein PA4352 is essential for surviving anaerobic energy stress. J Bacteriol 2006; 188:6529–6538 [View Article] [PubMed]
     [Google Scholar]
  47. Martínez-Gil M, Yousef-Coronado F, Espinosa-Urgel M. LapF, the second largest Pseudomonas putida protein, contributes to plant root colonization and determines biofilm architecture. Mol Microbiol 2010; 77:549–561 [View Article] [PubMed]
     [Google Scholar]
  48. Elsen S, Swem LR, Swem DL, Bauer CE. RegB/RegA, a highly conserved redox-responding global two-component regulatory system. Microbiol Mol Biol Rev 2004; 68:263–279 [View Article] [PubMed]
     [Google Scholar]
  49. Fernández-Piñar R, Ramos JL, Rodríguez-Herva JJ, Espinosa-Urgel M. A two-component regulatory system integrates redox state and population density sensing in Pseudomonas putida. J Bacteriol 2008; 190:7666–7674 [View Article] [PubMed]
     [Google Scholar]
  50. Fernández-Piñar R, Espinosa-Urgel M, Dubern JF, Heeb S, Ramos JL et al. Fatty acid-mediated signalling between two Pseudomonas species. Environ Microbiol Rep 2012; 4:417–423 [View Article] [PubMed]
     [Google Scholar]
  51. Scribani Rossi C, Eckartt K, Scarchilli E, Angeli S, Price-Whelan A et al. Molecular insights into RmcA-mediated c-di-GMP consumption: linking redox potential to biofilm morphogenesis in Pseudomonas aeruginosa. Microbiol Res 2023; 277:127498 [View Article] [PubMed]
     [Google Scholar]
  52. Zúñiga M, Pérez G, González-Candelas F. Evolution of arginine deiminase (ADI) pathway genes. Mol Phylogenet Evol 2002; 25:429–444 [View Article] [PubMed]
     [Google Scholar]
  53. Ugidos A, Morales G, Rial E, Williams HD, Rojo F. The coordinate regulation of multiple terminal oxidases by the Pseudomonas putida ANR global regulator. Environ Microbiol 2008; 10:1690–1702 [View Article] [PubMed]
     [Google Scholar]
  54. Tribelli PM, Lujan AM, Pardo A, Ibarra JG, Fernández Do Porto D et al. Core regulon of the global anaerobic regulator Anr targets central metabolism functions in Pseudomonas species. Sci Rep 2019; 9:9065 [View Article] [PubMed]
     [Google Scholar]
  55. Lu CD, Winteler H, Abdelal A, Haas D. The ArgR regulatory protein, a helper to the anaerobic regulator ANR during transcriptional activation of the arcD promoter in Pseudomonas aeruginosa. J Bacteriol 1999; 181:2459–2464 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001449
Loading
Gene expression reprogramming of Pseudomonas alloputida in response to arginine through the transcriptional regulator ArgR
Microbiology 170, 001449 (2024); https://doi.org/10.1099/mic.0.001449
/content/journal/micro/10.1099/mic.0.001449
/content/journal/micro/10.1099/mic.0.001449
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error