Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 4, pp 1643–1658 | Cite as

Regulation of the phosphate metabolism in Streptomyces genus: impact on the secondary metabolites

  • Carlos BarreiroEmail author
  • Miriam Martínez-Castro
Mini-Review
  • 366 Downloads

Abstract

The analysis of the inorganic phosphate effect over the antibiotics production is a long-distance history in the Streptomyces genus, which began almost at the same time that Michael Ende published his book entitled The Neverending Story. In some way, the unveiling of the pho regulon and its influence over the secondary metabolites production is an unfinished story, which keeps this subject as a trending topic, nowadays. Up to date, different studies have been releasing knowledge about particular areas of the pho regulon of different Streptomyces species. Nevertheless, for the first time, these knowledge drops are grouped in a review presenting a broad overview of the phosphate regulation and its impact over the secondary metabolites production in industrially relevant species. Even though the genetic response against phosphate scarcity is similar, as a whole, in different Streptomyces species, the fine-tuning is species-specific. Thus, the response regulator PhoP directly controls the secondary metabolites production in some species, whereas it regulates them in an indirect manner in other species. This information, unraveled in this review, is the result of the intensive analysis along last decade in several species of the genus that is allowing to distinguish how the phosphate response is unleashed in Streptomyces coelicolor, Streptomyces lividans, Streptomyces natalensis, Streptomyces lydicus, Streptomyces avermitilis, and Streptomyces tsukubaensis.

Keywords

Streptomyces Phosphate Secondary metabolites pho regulon Regulation Antibiotics 

Notes

Acknowledgments

Special thanks to (i) the ProWood project (“Wood and derivatives protection by novel bio-coating solutions”; ERA IB 7th Joint Call) through the APCIN call of the Spanish Ministry of Economy and Competitiveness (MINECO, Spain) (Project ID: PCIN-2016-081), which is allowing to isolate new and industrially interesting Actinobacteria and (ii) to the Syntheroids project (“Synthetic biology for industrial production of steroids”; ERA CoBioTech 1st call) through the APCIN call of the Spanish Ministry of Science, Innovation and Universities (Project ID: PCI2018-093066), which is allowing a deeper understanding of the steroids production by Actinobacteria.

The authors also wish to thank the scientific and administrative staff involved, along last decades, in the Actinobacteria metabolism regulation and antibiotics production group of University of León (Spain) and INBIOTEC initially headed by Prof. Juan F. Martín and Prof. Paloma Liras and continued by the INBIOTEC research team, nowadays.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abrudan MI, Smakman F, Grimbergen AJ, Westhoff S, Miller EL, van Wezel GP, Rozen DE (2015) Socially mediated induction and suppression of antibiosis during bacterial coexistence. Proc Natl Acad Sci 112:11054–11059.  https://doi.org/10.1073/pnas.1504076112 Google Scholar
  2. Allenby NEE, Laing E, Bucca G, Kierzek AM, Smith CP (2012) Diverse control of metabolism and other cellular processes in Streptomyces coelicolor by the PhoP transcription factor: genome-wide identification of in vivo targets. Nucleic Acids Res 40:9543–9556.  https://doi.org/10.1093/nar/gks766 Google Scholar
  3. Alvarez-Álvarez R, Rodríguez-García A, Santamarta I, Pérez-Redondo R, Prieto-Domínguez A, Martínez-Burgo Y, Liras P (2014) Transcriptomic analysis of Streptomyces clavuligerus ΔccaR::tsr: effects of the cephamycin C-clavulanic acid cluster regulator CcaR on global regulation. Microb Biotechnol 7:221–231.  https://doi.org/10.1111/1751-7915.12109 Google Scholar
  4. Aminov RI (2013) Biotic acts of antibiotics. Front Microbiol 4:1–16.  https://doi.org/10.3389/fmicb.2013.00241 Google Scholar
  5. Anné J, Maldonado B, Van Impe J, Van Mellaert L, Bernaerts K (2012) Recombinant protein production and streptomycetes. J Biotechnol 158:159–167.  https://doi.org/10.1016/j.jbiotec.2011.06.028 Google Scholar
  6. Aparicio JF, Barreales EG, Payero TD, Vicente CM, de Pedro A, Santos-Aberturas J (2016) Biotechnological production and application of the antibiotic pimaricin: biosynthesis and its regulation. Appl Microbiol Biotechnol 100:61–78.  https://doi.org/10.1007/s00253-015-7077-0 Google Scholar
  7. Apel AK, Sola-Landa A, Rodríguez-García A, Martín JF (2007) Phosphate control of phoA, phoC and phoD gene expression in Streptomyces coelicolor reveals significant differences in binding of PhoP to their promoter regions. Microbiology 153:3527–3537.  https://doi.org/10.1099/mic.0.2007/007070-0 Google Scholar
  8. Arakawa K (2018) Manipulation of metabolic pathways controlled by signaling molecules, inducers of antibiotic production, for genome mining in Streptomyces spp. Antonie Van Leeuwenhoek 111:743–751.  https://doi.org/10.1007/s10482-018-1052-6 Google Scholar
  9. Ashley K, Cordell D, Mavinic D (2011) A brief history of phosphorus: from the philosopher’s stone to nutrient recovery and reuse. Chemosphere 84:737–746.  https://doi.org/10.1016/j.chemosphere.2011.03.001 Google Scholar
  10. Barreiro C, Martínez-Castro M (2014) Trends in the biosynthesis and production of the immunosuppressant tacrolimus (FK506). Appl Microbiol Biotechnol 98:497–507.  https://doi.org/10.1007/s00253-013-5362-3 Google Scholar
  11. Barreiro C, Martín JF, García-Estrada C (2012) Proteomics shows new faces for the old penicillin producer Penicillium chrysogenum. J Biomed Biotechnol 2012:105109–105115.  https://doi.org/10.1155/2012/105109 Google Scholar
  12. Bentley SD, Chater KF, Cerdeño-Tárraga A-M, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang C-H, Kieser T, Larke L, Murphy L, Oliver K, O’Neil S, Rabbinowitsch E, Rajandream M-A, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147.  https://doi.org/10.1038/417141a Google Scholar
  13. Bérdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot (Tokyo) 65:385–395.  https://doi.org/10.1038/ja.2012.27 Google Scholar
  14. Bibb MJ (2005) Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol 8:208–215.  https://doi.org/10.1016/j.mib.2005.02.016 Google Scholar
  15. Boukhris I, Dulermo T, Chouayekh H, Virolle M-J (2016) Evidence for the negative regulation of phytase gene expression in Streptomyces lividans and Streptomyces coelicolor. J Basic Microbiol 56:59–66.  https://doi.org/10.1002/jobm.201500417 Google Scholar
  16. Brzoska P, Boos W (1989) The ugp-encoded glycerophosphoryldiester phosphodiesterase, a transport-related enzyme of Escherichia coli. FEMS Microbiol Rev 5:115–124Google Scholar
  17. Butusov M, Jernelöv A (2013a) Phosphorus. An element that could have been called Lucifer. In: Butusov M, Jernelöv A (eds) Springer Briefs in Environmental Science, New York.  https://doi.org/10.1007/978-1-4614-6803-5
  18. Butusov M, Jernelöv A (2013b) The role of phosphorus in the origin of life and in evolution. In: Butusov M, Jernelöv A (eds) Phosphorus. An element that could have been called Lucifer. Springer Briefs in Environmental Science, New York, pp 1–12Google Scholar
  19. Butusov M, Jernelöv A (2013c) Phosphorus in the organic life: cells, tissues, organisms. In: Butusov M, Jernelöv A (eds) Phosphorus. An element that could have been called Lucifer. Springer Briefs in Environmental Science, New York, pp 13–18Google Scholar
  20. Chater KF (2016) Recent advances in understanding Streptomyces. F1000Research 5:2795.  https://doi.org/10.12688/f1000research.9534.1 Google Scholar
  21. Chaudhary AK, Dhakal D, Sohng JK (2013) An insight into the “-omics” based engineering of streptomycetes for secondary metabolite overproduction. Biomed Res Int 2013:968518–968515.  https://doi.org/10.1155/2013/968518 Google Scholar
  22. Chen G-Q, Lu F-P, Du L-X (2008) Natamycin production by Streptomyces gilvosporeus based on statistical optimization. J Agric Food Chem 56:5057–5061.  https://doi.org/10.1021/jf800479u Google Scholar
  23. Chen J, Liu M, Liu X, Miao J, Fu C, Gao H, Müller R, Zhang Q, Zhang L (2016) Interrogation of Streptomyces avermitilis for efficient production of avermectins. Synth Syst Biol 1:7–16.  https://doi.org/10.1016/j.synbio.2016.03.002 Google Scholar
  24. Cornforth DM, Foster KR (2015) Antibiotics and the art of bacterial war. Proc Natl Acad Sci U S A 112:10827–10828.  https://doi.org/10.1073/pnas.1513608112 Google Scholar
  25. Cruz-Morales P, Vijgenboom E, Iruegas-Bocardo F, Girard G, Yáñez-Guerra LA, Ramos-Aboites HE, Pernodet JL, Anné J, Van Wezel GP, Barona-Gómez F (2013) The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island. Genome Biol Evol 5:1165–1175.  https://doi.org/10.1093/gbe/evt082 Google Scholar
  26. Curdová E, Kremen A, Vanĕk Z, Hostálek Z (1976) Regulation and biosynthesis of secondary metabolites. XVIII. Adenylate level and chlorotetracycline production in Streptomyces aureofaciens. Folia Microbiol (Praha) 21:481–487Google Scholar
  27. de Lima Procópio RE, da Silva IR, Martins MK, de Azevedo JL, de Araújo JM (2012) Antibiotics produced by Streptomyces. Braz J Infect Dis 16:466–471.  https://doi.org/10.1016/j.bjid.2012.08.014 Google Scholar
  28. Demain AL (1979) Aminoglycosides, genes and regulation. Jpn J Antibiot 32(Suppl):S15–S20Google Scholar
  29. Demain AL, Sanchez S (2009) Microbial drug discovery: 80 years of progress. J Antibiot (Tokyo) 62:5–16.  https://doi.org/10.1038/ja.2008.16 Google Scholar
  30. Demain AL, Sánchez S (2018) Advancement of biotechnology by genetic modifications. Methods Mol Biol 1852:1–43.  https://doi.org/10.1007/978-1-4939-8742-9_1 Google Scholar
  31. Dick CF, Dos-Santos ALA, Meyer-Fernandes JR (2011) Inorganic phosphate as an important regulator of phosphatases. Enzyme Res 2011:1–7.  https://doi.org/10.4061/2011/103980 Google Scholar
  32. Eleazu CO, Eleazu KC, Chukwuma S, Essien UN (2013) Review of the mechanism of cell death resulting from streptozotocin challenge in experimental animals, its practical use and potential risk to humans. J Diabetes Metab Disord 12:60.  https://doi.org/10.1186/2251-6581-12-60 Google Scholar
  33. Esnault C, Dulermo T, Smirnov A, Askora A, David M, Deniset-Besseau A, Holland IB, Virolle MJ (2017) Strong antibiotic production is correlated with highly active oxidative metabolism in Streptomyces coelicolor M145. Sci Rep 7:1–10.  https://doi.org/10.1038/s41598-017-00259-9 Google Scholar
  34. Farhat MB, Boukhris I, Chouayekh H (2015) Mineral phosphate solubilization by Streptomyces sp.CTM396 involves the excretion of gluconic acid and is stimulated by humic acids. FEMS Microbiol Lett 362:1–8.  https://doi.org/10.1093/femsle/fnv008 Google Scholar
  35. Fernández-Martínez LT, Santos-Beneit F, Martín JF (2012) Is PhoR-PhoP partner fidelity strict? PhoR is required for the activation of the pho regulon in Streptomyces coelicolor. Mol Gen Genomics 287:565–573.  https://doi.org/10.1007/s00438-012-0698-4
  36. Flores FJ, Barreiro C, Coque JJR, Martín JF (2005) Functional analysis of two divalent metal-dependent regulatory genes dmdR1 and dmdR2 in Streptomyces coelicolor and proteome changes in deletion mutants. FEBS J 272:725–735.  https://doi.org/10.1111/j.1742-4658.2004.04509.x
  37. Fritz G, Mascher T (2014) A balancing act times two: sensing and regulating cell envelope homeostasis in Bacillus subtilis. Mol Microbiol 94:1201–1207.  https://doi.org/10.1111/mmi.12848 Google Scholar
  38. Fu L-F, Tao Y, Jin M-Y, Jiang H (2016) Improvement of FK506 production by synthetic biology approaches. Biotechnol Lett 38:2015–2021.  https://doi.org/10.1007/s10529-016-2202-4 Google Scholar
  39. Ghorbel S, Kormanec J, Artus A, Virolle M-J (2006) Transcriptional studies and regulatory interactions between the phoR-phoP operon and the phoU, mtpA, and ppk genes of Streptomyces lividans TK24. J Bacteriol 188:677–686.  https://doi.org/10.1128/JB.188.2.677-686.2006 Google Scholar
  40. Gomez-Escribano JP, Martín JF, Hesketh A, Bibb MJ, Liras P (2008) Streptomyces clavuligerus relA-null mutants overproduce clavulanic acid and cephamycin C: negative regulation of secondary metabolism by (p)ppGpp. Microbiology 154:744–755.  https://doi.org/10.1099/mic.0.2007/011890-0 Google Scholar
  41. Granata S, Dalla Gassa A, Carraro A, Brunelli M, Stallone G, Lupo A, Zaza G (2016) Sirolimus and everolimus pathway: reviewing candidate genes influencing their intracellular effects. Int J Mol Sci.  https://doi.org/10.3390/ijms17050735
  42. Guo J, Ma R, Su B, Li Y, Zhang J, Fang J (2016) Raising the avermectins production in Streptomyces avermitilis by utilizing nanosecond pulsed electric fields (nsPEFs). Sci Rep 6:1–10.  https://doi.org/10.1038/srep25949 Google Scholar
  43. Hackl S, Bechthold A (2015) The gene bldA, a regulator of morphological differentiation and antibiotic production in Streptomyces. Arch Pharm (Weinheim) 348:455–462.  https://doi.org/10.1002/ardp.201500073 Google Scholar
  44. Hoskisson PA, Fernández-Martínez LT (2018) Regulation of specialised metabolites in Actinobacteria—expanding the paradigms. Environ Microbiol Rep 10:231–238.  https://doi.org/10.1111/1758-2229.12629 Google Scholar
  45. Hutchings MI, Hoskisson PA, Chandra G, Buttner MJ (2004) Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2). Microbiology 150:2795–2806.  https://doi.org/10.1099/mic.0.27181-0 Google Scholar
  46. Khan MS, Zaidi A, Wani PA (2007) Role of phosphate-solubilizing microorganisms in sustainable agriculture—a review. Agron Sustain Dev 27:29–43.  https://doi.org/10.1051/agro:2006011 Google Scholar
  47. Kim MW, Lee B-R, You S, Kim E-J, Kim J-N, Song E, Yang Y-H, Hwang D, Kim B-G (2018) Transcriptome analysis of wild-type and afsS deletion mutant strains identifies synergistic transcriptional regulator of afsS for a high antibiotic-producing strain of Streptomyces coelicolor A3(2). Appl Microbiol Biotechnol 102:3243–3253.  https://doi.org/10.1007/s00253-018-8838-3 Google Scholar
  48. Kleinschnitz EM, Latus A, Sigle S, Maldener I, Wohlleben W, Muth G (2011) Genetic analysis of SCO2997, encoding a TagF homologue, indicates a role for wall teichoic acids in sporulation of Streptomyces coelicolor A3(2). J Bacteriol 193:6080–6085.  https://doi.org/10.1128/JB.05782-11 Google Scholar
  49. Kocan M, Schaffer S, Ishige T, Sorger-Herrmann U, Wendisch VF, Bott M (2006) Two-component systems of Corynebacterium glutamicum: deletion analysis and involvement of the PhoS-PhoR system in the phosphate starvation response. J Bacteriol 188:724–732.  https://doi.org/10.1128/JB.188.2.724-732.2006 Google Scholar
  50. Liras P, Rodríguez-García A (2000) Clavulanic acid, a beta-lactamase inhibitor: biosynthesis and molecular genetics. Appl Microbiol Biotechnol 54:467–475Google Scholar
  51. Manteca Á, Yagüe P (2018) Streptomyces differentiation in liquid cultures as a trigger of secondary metabolism. Antibiotics 7:41.  https://doi.org/10.3390/antibiotics7020041 Google Scholar
  52. Martín JF (2004) Phosphate control of the biosynthesis of antibiotics and other secondary metabolites is mediated by the PhoR-PhoP system: an unfinished story. J Bacteriol 186:5197–5201.  https://doi.org/10.1128/JB.186.16.5197-5201.2004 Google Scholar
  53. Martin JF, Demain AL (1976) Control by phosphate of candicidin production. Biochem Biophys Res Commun 71:1103–1109.  https://doi.org/10.3171/jns.1998.88.5.0817 Google Scholar
  54. Martin JF, Demain AL (1980) Control of antibiotic biosynthesis. Microbiol Rev 44:230–251Google Scholar
  55. Martín JF, Liras P (2012) Cascades and networks of regulatory genes that control antibiotic biosynthesis. Subcell Biochem 64:115–138.  https://doi.org/10.1007/978-94-007-5055-5_6 Google Scholar
  56. Martín JF, Liras P, Demain AL (1978) ATP and adenylate energy charge during phosphate-mediated control of antibiotic synthesis. Biochem Biophys Res Commun 83:822–828Google Scholar
  57. Martín JF, Santos-Beneit F, Rodríguez-García A, Sola-Landa A, Smith MCM, Ellingsen TE, Nieselt K, Burroughs NJ, Wellington EMH (2012) Transcriptomic studies of phosphate control of primary and secondary metabolism in Streptomyces coelicolor. Appl Microbiol Biotechnol 95:61–75.  https://doi.org/10.1007/s00253-012-4129-6 Google Scholar
  58. Martín JF, Rodríguez-García A, Liras P (2017) The master regulator PhoP coordinates phosphate and nitrogen metabolism, respiration, cell differentiation and antibiotic biosynthesis: comparison in Streptomyces coelicolor and Streptomyces avermitilis. J Antibiot (Tokyo) 70:534–541.  https://doi.org/10.1038/ja.2017.19 Google Scholar
  59. Martínez-Castro M, Barreiro C, Romero F, Fernández-Chimeno RI, Martín JF (2011) Streptomyces tacrolimicus sp. nov., a low producer of the immunosuppressant tacrolimus (FK506). Int J Syst Evol Microbiol 61:1084–1088.  https://doi.org/10.1099/ijs.0.024273-0 Google Scholar
  60. Martínez-Castro M, Salehi-Najafabadi Z, Romero F, Pérez-Sanchiz R, Fernández-Chimeno RI, Martín JF, Barreiro C (2013) Taxonomy and chemically semi-defined media for the analysis of the tacrolimus producer “Streptomyces tsukubaensis”. Appl Microbiol Biotechnol 97:2139–2152.  https://doi.org/10.1007/s00253-012-4364-x Google Scholar
  61. Martínez-Castro M, Barreiro C, Martín JF (2018) Analysis and validation of the pho regulon in the tacrolimus-producer strain Streptomyces tsukubaensis: differences with the model organism Streptomyces coelicolor. Appl Microbiol Biotechnol 102:7029–7045.  https://doi.org/10.1007/s00253-018-9140-0
  62. Martín-Martín S, Rodríguez-García A, Santos-Beneit F, Franco-Domínguez E, Sola-Landa A, Martín JF (2017) Self-control of the PHO regulon: the PhoP-dependent protein PhoU controls negatively expression of genes of PHO regulon in Streptomyces coelicolor. J Antibiot (Tokyo) 71:1–10.  https://doi.org/10.1038/ja.2017.130 Google Scholar
  63. McGuinness WA, Malachowa N, DeLeo FR (2017) Vancomycin resistance in Staphylococcus aureus. Yale J Biol Med 90:269–281Google Scholar
  64. Mendes MV, Tunca S, Antón N, Recio E, Sola-Landa A, Aparicio JF, Martín JF (2007) The two-component phoR-phoP system of Streptomyces natalensis: inactivation or deletion of phoP reduces the negative phosphate regulation of pimaricin biosynthesis. Metab Eng 9:217–227.  https://doi.org/10.1016/j.ymben.2006.10.003
  65. Méndez C, González-Sabín J, Morís F, Salas JA (2015) Expanding the chemical diversity of the antitumoral compound mithramycin by combinatorial biosynthesis and biocatalysis: the quest for mithralogs with improved therapeutic window. Planta Med 81:1326–1338.  https://doi.org/10.1055/s-0035-1557876 Google Scholar
  66. Nelson ML, Levy SB (2011) The history of the tetracyclines. Ann N Y Acad Sci 1241:17–32.  https://doi.org/10.1111/j.1749-6632.2011.06354.x Google Scholar
  67. Niu G, Chater KF, Tian Y, Zhang J, Tan H (2016) Specialised metabolites regulating antibiotic biosynthesis in Streptomyces spp. FEMS Microbiol Rev 40:554–573.  https://doi.org/10.1093/femsre/fuw012 Google Scholar
  68. Olano C, Lombó F, Méndez C, Salas JA (2008) Improving production of bioactive secondary metabolites in actinomycetes by metabolic engineering. Metab Eng 10:281–292.  https://doi.org/10.1016/j.ymben.2008.07.001 Google Scholar
  69. Ordóñez-Robles M, Santos-Beneit F, Rodríguez-García A, Martín JF (2017) Analysis of the pho regulon in Streptomyces tsukubaensis. Microbiol Res 205:80–87.  https://doi.org/10.1016/j.micres.2017.08.010
  70. Ordóñez-Robles M, Santos-Beneit F, Martín J (2018) Unraveling nutritional regulation of tacrolimus biosynthesis in Streptomyces tsukubaensis through omic approaches. Antibiotics 7:39.  https://doi.org/10.3390/antibiotics7020039 Google Scholar
  71. Paradkar A (2013) Clavulanic acid production by Streptomyces clavuligerus: biogenesis, regulation and strain improvement. J Antibiot (Tokyo) 66:411–420.  https://doi.org/10.1038/ja.2013.26 Google Scholar
  72. Rao NN, Torriani A (1990) Molecular aspects of phosphate transport in Escherichia coli. Mol Microbiol 4:1083–1090.  https://doi.org/10.1111/j.1365-2958.1990.tb00682.x Google Scholar
  73. Raven JA (2013) The evolution of autotrophy in relation to phosphorus requirement. J Exp Bot 64:4023–4046.  https://doi.org/10.1093/jxb/ert306 Google Scholar
  74. Reuther J, Wohlleben W (2006) Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J Mol Microbiol Biotechnol 12:139–146.  https://doi.org/10.1159/000096469 Google Scholar
  75. Rodríguez-García A, Barreiro C, Santos-Beneit F, Sola-Landa A, Martín JF (2007) Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant. Proteomics 7:2410–2429.  https://doi.org/10.1002/pmic.200600883 Google Scholar
  76. Rodríguez-García A, Sola-landa A, Apel K, Santos-Beneit F, Martín JF (2009) Phosphate control over nitrogen metabolism in Streptomyces coelicolor: direct and indirect negative control of glnR, glnA, glnII and amtB expression by the response regulator PhoP. Nucleic Acids Res 37:3230–3242.  https://doi.org/10.1093/nar/gkp162 Google Scholar
  77. Romero-Rodríguez A, Ruiz-Villafán B, Tierrafría VH, Rodríguez-Sanoja R, Sánchez S (2016) Carbon catabolite regulation of secondary metabolite formation and morphological differentiation in Streptomyces coelicolor. Appl Biochem Biotechnol 180:1152–1166.  https://doi.org/10.1007/s12010-016-2158-9 Google Scholar
  78. Romero-Rodríguez A, Maldonado-Carmona N, Ruiz-Villafán B, Koirala N, Rocha D, Sánchez S (2018) Interplay between carbon, nitrogen and phosphate utilization in the control of secondary metabolite production in Streptomyces. Antonie Van Leeuwenhoek 111:761–781.  https://doi.org/10.1007/s10482-018-1073-1 Google Scholar
  79. Salehghamari E, Hamedi J, Elahi E, Sepehrizadeh Z, Sadeghi M, Muth G (2012) Prediction of the pho regulon in Streptomyces clavuligerus DSM 738. New Microbiol 35:447–457Google Scholar
  80. Salehi-Najafabadi Z, Barreiro C, Martínez-Castro M, Solera E, Martín JF (2011) Characterisation of a γ-butyrolactone receptor of Streptomyces tacrolimicus: effect on sporulation and tacrolimus biosynthesis. Appl Microbiol Biotechnol 92:971–984.  https://doi.org/10.1007/s00253-011-3466-1 Google Scholar
  81. Salehi-Najafabadi Z, Barreiro C, Rodríguez-García A, Cruz A, López GE, Martín JF (2014) The gamma-butyrolactone receptors BulR1 and BulR2 of Streptomyces tsukubaensis: tacrolimus (FK506) and butyrolactone synthetases production control. Appl Microbiol Biotechnol 98:4919–4936.  https://doi.org/10.1007/s00253-014-5595-9 Google Scholar
  82. Santos-Beneit F (2015) The Pho regulon: a huge regulatory network in bacteria. Front Microbiol 6:402.  https://doi.org/10.3389/fmicb.2015.00402 Google Scholar
  83. Santos-Beneit F (2018) Genome sequencing analysis of Streptomyces coelicolor mutants that overcome the phosphate-depending vancomycin lethal effect. BMC Genomics 19:457.  https://doi.org/10.1186/s12864-018-4838-z
  84. Santos-Beneit F, Martín JF (2013) Vancomycin resistance in Streptomyces coelicolor is phosphate-dependent but is not mediated by the PhoP regulator. J Glob Antimicrob Resist 1:109–113.  https://doi.org/10.1016/j.jgar.2013.03.003 Google Scholar
  85. Santos-Beneit F, Rodríguez-García A, Franco-Domínguez E, Martín JF (2008) Phosphate-dependent regulation of the low- and high-affinity transport systems in the model actinomycete Streptomyces coelicolor. Microbiology 154:2356–2370.  https://doi.org/10.1099/mic.0.2008/019539-0 Google Scholar
  86. Santos-Beneit F, Rodríguez-García A, Apel AK, Martín JF (2009a) Phosphate and carbon source regulation of two PhoP-dependent glycerophosphodiester phosphodiesterase genes of Streptomyces coelicolor. Microbiology 155:1800–1811.  https://doi.org/10.1099/mic.0.026799-0 Google Scholar
  87. Santos-Beneit F, Rodríguez-García A, Sola-Landa A, Martín JF (2009b) Cross-talk between two global regulators in Streptomyces: PhoP and AfsR interact in the control of afsS, pstS and phoRP transcription. Mol Microbiol 72:53–68.  https://doi.org/10.1111/j.1365-2958.2009.06624.x Google Scholar
  88. Santos-Beneit F, Barriuso-Iglesias M, Fernández-Martínez LT, Martínez-Castro M, Sola-Landa A, Rodríguez-García A, Martín JF (2011) The RNA polymerase omega factor RpoZ is regulated by PhoP and has an important role in antibiotic biosynthesis and morphological differentiation in Streptomyces coelicolor. Appl Environ Microbiol 77:7586–7594.  https://doi.org/10.1128/AEM.00465-11 Google Scholar
  89. Santos-Beneit F, Fernández-Martínez LT, García AR, Martín-Martín S, Ordóñez-Robles M, Yagüe P, Manteca A, Martín JF (2014a) Transcriptional response to vancomycin in a highly vancomycin-resistant Streptomyces coelicolor mutant. Future Microbiol 9:603–622.  https://doi.org/10.2217/fmb.14.21 Google Scholar
  90. Santos-Beneit F, Martín JF, Barreiro C (2014b) Glycopeptides and bacterial cell walls. Antimicrob. Compd. Springer Berlin Heidelberg, Berlin, pp 285–311Google Scholar
  91. Schneider TD (1997) Information content of individual genetic sequences. J Theor Biol 189:427–441Google Scholar
  92. Seki T, Yoshikawa H, Takahashi H, Saito H (1987) Cloning and nucleotide sequence of phoP, the regulatory gene for alkaline phosphatase and phosphodiesterase in Bacillus subtilis. J Bacteriol 169:2913–2916.  https://doi.org/10.1128/jb.169.7.2913-2916.1987 Google Scholar
  93. Seki T, Yoshikawa H, Takahashi H, Saito H (1988) Nucleotide sequence of the Bacillus subtilis phoR gene. J Bacteriol 170:5935–5938.  https://doi.org/10.1099/13500872-141-2-321 Google Scholar
  94. Sharpley A, Jarvie H, Flaten D, Kleinman P (2018) Celebrating the 350th anniversary of phosphorus discovery: a conundrum of deficiency and excess. J Environ Qual 47:774.  https://doi.org/10.2134/jeq2018.05.0170 Google Scholar
  95. Smirnov A, Esnault C, Prigent M, Holland IB, Virolle M-J (2015) Phosphate homeostasis in conditions of phosphate proficiency and limitation in the wild type and the phoP mutant of Streptomyces lividans. PLoS One 10:e0126221.  https://doi.org/10.1371/journal.pone.0126221
  96. Sola-Landa A, Moura RS, Martín JF (2003) The two-component PhoR-PhoP system controls both primary metabolism and secondary metabolite biosynthesis in Streptomyces lividans. Proc Natl Acad Sci U S A 100:6133–6138.  https://doi.org/10.1073/pnas.0931429100 Google Scholar
  97. Sola-Landa A, Rodríguez-García A, Franco-Domínguez E, Martín JF (2005) Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol Microbiol 56:1373–1385.  https://doi.org/10.1111/j.1365-2958.2005.04631.x Google Scholar
  98. Sola-Landa A, Rodríguez-García A, Apel AK, Martín JF (2008) Target genes and structure of the direct repeats in the DNA-binding sequences of the response regulator PhoP in Streptomyces coelicolor. Nucleic Acids Res 36:1358–1368.  https://doi.org/10.1093/nar/gkm1150 Google Scholar
  99. Sola-Landa A, Rodríguez-García A, Amin R, Wohlleben W, Martín J (2013) Competition between the GlnR and PhoP regulators for the glnA and amtB promoters in Streptomyces coelicolor. Nucleic Acids Res 41:1767–1782.  https://doi.org/10.1093/nar/gks1203 Google Scholar
  100. Taylor SD, Palmer M (2016) The action mechanism of daptomycin. Bioorg Med Chem 24:6253–6268.  https://doi.org/10.1016/j.bmc.2016.05.052 Google Scholar
  101. Tenconi E, Jourdan S, Motte P, Virolle M-J, Rigali S (2012) Extracellular sugar phosphates are assimilated by Streptomyces in a PhoP-dependent manner. Antonie Van Leeuwenhoek 102:425–433.  https://doi.org/10.1007/s10482-012-9763-6 Google Scholar
  102. Tiffert Y, Supra P, Wurm R, Wohlleben W, Wagner R, Reuther J (2008) The Streptomyces coelicolor GlnR regulon: identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol Microbiol 67:861–880.  https://doi.org/10.1111/j.1365-2958.2007.06092.x Google Scholar
  103. Tommassen J, Lugtenberg B (1982) PHO-regulon of Escherichia coli K12: a minireview. Ann Microbiol (Paris) 133:243–249Google Scholar
  104. Tommassen J, de Geus P, Lugtenberg B, Hackett J, Reeves P (1982) Regulation of the pho regulon of Escherichia coli K-12. Cloning of the regulatory genes phoB and phoR and identification of their gene products. J Mol Biol 157:265–274Google Scholar
  105. Tunca S, Barreiro C, Sola-Landa A, Coque JJR, Martín JF (2007) Transcriptional regulation of the desferrioxamine gene cluster of Streptomyces coelicolor is mediated by binding of DmdR1 to an iron box in the promoter of the desA gene. FEBS J 274:1110–1122.  https://doi.org/10.1111/j.1742-4658.2007.05662.x Google Scholar
  106. Tunca S, Barreiro C, Coque J-JR, Martín JF (2009) Two overlapping antiparallel genes encoding the iron regulator DmdR1 and the Adm proteins control siderophore and antibiotic biosynthesis in Streptomyces coelicolor A3(2). FEBS J 276:4814–4827.  https://doi.org/10.1111/j.1742-4658.2009.07182.x Google Scholar
  107. Uguru GC, Stephens KE, Stead JA, Towle JE, Baumberg S, McDowall KJ (2005) Transcriptional activation of the pathway-specific regulator of the actinorhodin biosynthetic genes in Streptomyces coelicolor. Mol Microbiol 58:131–150.  https://doi.org/10.1111/j.1365-2958.2005.04817.x Google Scholar
  108. Urem M, Świątek-Połatyńska MA, Rigali S, van Wezel GP (2016) Intertwining nutrient-sensory networks and the control of antibiotic production in Streptomyces. Mol Microbiol 102:183–195.  https://doi.org/10.1111/mmi.13464 Google Scholar
  109. Van Wezel GP, McDowall KJ (2011) The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat Prod Rep 28:1311–1333.  https://doi.org/10.1039/c1np00003a Google Scholar
  110. Vehreschild MJGT, Haverkamp M, Biehl LM, Lemmen S, Fätkenheuer G (2018) Vancomycin-resistant enterococci (VRE): a reason to isolate? Infection.  https://doi.org/10.1007/s15010-018-1202-9
  111. Vu-Trong K, Bhuwapathanapun S, Gray PP (1981) Metabolic regulation in tylosin-producing Streptomyces fradiae: phosphate control of tylosin biosynthesis. Antimicrob Agents Chemother 19:209–212Google Scholar
  112. Wisniak J (2005) Phosphorus-from discovery to commodity. Indian J Chem Technol 12:108–122Google Scholar
  113. Wu H, Liu W, Shi L, Si K, Liu T, Dong D, Zhang T, Zhao J, Liu D, Tian Z, Yue Y, Zhang H, Xuelian B, Liang Y (2017) Comparative genomic and regulatory analyses of natamycin production of Streptomyces lydicus A02. Sci Rep 7:1–12.  https://doi.org/10.1038/s41598-017-09532-3 Google Scholar
  114. Xia M, Huang D, Li S, Wen J, Jia X, Chen Y (2013) Enhanced FK506 production in Streptomyces tsukubaensis by rational feeding strategies based on comparative metabolic profiling analysis. Biotechnol Bioeng 110:2717–2730.  https://doi.org/10.1002/bit.24941 Google Scholar
  115. Yang R, Liu X, Wen Y, Song Y, Chen Z, Li J (2015) The PhoP transcription factor negatively regulates avermectin biosynthesis in Streptomyces avermitilis. Appl Microbiol Biotechnol 99:10547–10557.  https://doi.org/10.1007/s00253-015-6921-6 Google Scholar
  116. Yoo YJ, Kim H, Park SR, Yoon YJ (2017) An overview of rapamycin: from discovery to future perspectives. J Ind Microbiol Biotechnol 44:537–553.  https://doi.org/10.1007/s10295-016-1834-7 Google Scholar
  117. Zubkov MV, Martin AP, Hartmann M, Grob C, Scanlan DJ (2015) Dominant oceanic bacteria secure phosphate using a large extracellular buffer. Nat Commun 6:7878.  https://doi.org/10.1038/ncomms8878 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Instituto de Biotecnología de León (INBIOTEC)LeónSpain
  2. 2.Departamento de Biología MolecularUniversidad de LeónPonferradaSpain
  3. 3.Facultad de Ciencias de la SaludUniversidad Isabel IBurgosSpain

Personalised recommendations