Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa


Autoři: Stuart D. Woodcock aff001;  Karl Syson aff002;  Richard H. Little aff001;  Danny Ward aff001;  Despoina Sifouna aff003;  James K. M. Brown aff004;  Stephen Bornemann aff002;  Jacob G. Malone aff001
Působiště autorů: Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom aff001;  Department of Biological Chemistry, John Innes Centre, Norwich, United Kingdom aff002;  School of Biological Sciences, University of East Anglia, Norwich, United Kingdom aff003;  Department of Crop Genetics, John Innes Centre, Norwich, United Kingdom aff004
Vyšlo v časopise: Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa. PLoS Genet 17(4): e1009524. doi:10.1371/journal.pgen.1009524
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009524

Souhrn

An important prelude to bacterial infection is the ability of a pathogen to survive independently of the host and to withstand environmental stress. The compatible solute trehalose has previously been connected with diverse abiotic stress tolerances, particularly osmotic shock. In this study, we combine molecular biology and biochemistry to dissect the trehalose metabolic network in the opportunistic human pathogen Pseudomonas aeruginosa PAO1 and define its role in abiotic stress protection. We show that trehalose metabolism in PAO1 is integrated with the biosynthesis of branched α-glucan (glycogen), with mutants in either biosynthetic pathway significantly compromised for survival on abiotic surfaces. While both trehalose and α-glucan are important for abiotic stress tolerance, we show they counter distinct stresses. Trehalose is important for the PAO1 osmotic stress response, with trehalose synthesis mutants displaying severely compromised growth in elevated salt conditions. However, trehalose does not contribute directly to the PAO1 desiccation response. Rather, desiccation tolerance is mediated directly by GlgE-derived α-glucan, with deletion of the glgE synthase gene compromising PAO1 survival in low humidity but having little effect on osmotic sensitivity. Desiccation tolerance is independent of trehalose concentration, marking a clear distinction between the roles of these two molecules in mediating responses to abiotic stress.

Klíčová slova:

Biosynthesis – Glucose – Glycogens – NMR spectroscopy – Osmotic shock – Pseudomonas – Pseudomonas aeruginosa – Trehalose


Zdroje

1. Liu W-P, Tian Y-Q, Hai Y-T, Zheng Z-N, Cao Q-L. Prevalence survey of nosocomial infections in the Inner Mongolia Autonomous Region of China [2012–2014]. Journal of Thoracic Disease. 2015;7(9):1650–7. doi: 10.3978/j.issn.2072-1439.2015.09.41 26543614

2. Centres for Disease Control and Prevention. Antibiotic Resistance Threats in the United States, 2013. Atlanta: Centres for Disease Control and Prevention, 2013.

3. Kielhofner M, Atmar RL, Hamill RJ, Musher DM. Life-Threatening Pseudomonas aeruginosa Infections in Patients with Human Immunodeficiency Virus Infection. Clinical Infectious Diseases. 1992;14(2):403–11. doi: 10.1093/clinids/14.2.403 1554824

4. Chitkara YK, Feierabend TC. Endogenous and exogenous infection with Pseudomonas aeruginosa in a burns unit. International surgery. 1981;66(3):237–40. Epub 1981/07/01. 6797982.

5. Shigemura K, Arakawa S, Sakai Y, Kinoshita S, Tanaka K, Fujisawa M. Complicated urinary tract infection caused by Pseudomonas aeruginosa in a single institution (1999–2003). International Journal of Urology. 2006;13(5):538–42. doi: 10.1111/j.1442-2042.2006.01359.x 16771722

6. Williams BJ, Dehnbostel J, Blackwell TS. Pseudomonas aeruginosa: host defence in lung diseases. Respirology (Carlton, Vic). 2010;15(7):1037–56. Epub 2010/08/21. doi: 10.1111/j.1440-1843.2010.01819.x 20723140.

7. Pressler T, Bohmova C, Conway S, Dumcius S, Hjelte L, Høiby N, et al. Chronic Pseudomonas aeruginosa infection definition: EuroCareCF Working Group report. Journal of Cystic Fibrosis. 2011;10:S75–S8. doi: 10.1016/S1569-1993(11)60011-8 21658646

8. Henry RL, Mellis CM, Petrovic L. Mucoid Pseudomonas aeruginosa is a marker of poor survival in cystic fibrosis. Pediatric Pulmonology. 1992;12(3):158–61. doi: 10.1002/ppul.1950120306 1641272

9. Conway SP, Lee TW. Prevention of chronic Pseudomonas aeruginosa infection in people with cystic fibrosis. Expert Review of Respiratory Medicine. 2009;3(4):349–61. Epub 2010/05/19. doi: 10.1586/ers.09.26 20477327.

10. Beales N. Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: A review. Comprehensive Reviews in Food Science and Food Safety. 2004;3(1):1–20. doi: 10.1111/j.1541-4337.2004.tb00057.x 33430556

11. Pérez V, Hengst M, Kurte L, Dorador C, Jeffrey WH, Wattiez R, et al. Bacterial Survival under Extreme UV Radiation: A Comparative Proteomics Study of Rhodobacter sp., Isolated from High Altitude Wetlands in Chile. Frontiers in microbiology. 2017;8:1173–. doi: 10.3389/fmicb.2017.01173 28694800.

12. Bhagirath AY, Li Y, Somayajula D, Dadashi M, Badr S, Duan K. Cystic fibrosis lung environment and Pseudomonas aeruginosa infection. BMC Pulmonary Medicine. 2016;16(1):174. doi: 10.1186/s12890-016-0339-5 27919253

13. Mann EE, Wozniak DJ. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiology Reviews. 2012;36(4):893–916. Epub 2012/01/23. doi: 10.1111/j.1574-6976.2011.00322.x 22212072.

14. Deng X, Li Z, Zhang W. Transcriptome sequencing of Salmonella enterica serovar Enteritidis under desiccation and starvation stress in peanut oil. Food Microbiology. 2012;30(1):311–5. doi: 10.1016/j.fm.2011.11.001 22265317

15. Kintz E, Goldberg JB. Regulation of lipopolysaccharide O antigen expression in Pseudomonas aeruginosa. Future Microbiol. 2008;3(2):191–203. Epub 2008/03/28. doi: 10.2217/17460913.3.2.191 18366339.

16. Battista JR, Park M-J, McLemore AE. Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology. 2001;43(2):133–9. doi: 10.1006/cryo.2001.2357 11846468

17. Wood JM. Bacterial responses to osmotic challenges. The Journal of General Physiology. 2015;145(5):381–8. doi: 10.1085/jgp.201411296 25870209

18. Elbein AD, Pan YT, Pastuszak I, Carroll D. New insights on trehalose: a multifunctional molecule. Glycobiology. 2003;13(4):17R–27R. doi: 10.1093/glycob/cwg047 12626396

19. Larsen PI, Sydnes LK, Landfald B, Strøm AR. Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose. Archives of microbiology. 1987;147(1):1–7. doi: 10.1007/BF00492896 2883950

20. Reina-Bueno M, Argandoña M, Salvador M, Rodríguez-Moya J, Iglesias-Guerra F, Csonka LN, et al. Role of Trehalose in Salinity and Temperature Tolerance in the Model Halophilic Bacterium Chromohalobacter salexigens. PLoS ONE. 2012;7(3):e33587. doi: 10.1371/journal.pone.0033587 22448254

21. Zhang Q, Yan T. Correlation of intracellular trehalose concentration with desiccation resistance of soil Escherichia coli populations. Appl Environ Microbiol. 2012;78(20):7407–13. Epub 2012/08/14. doi: 10.1128/AEM.01904-12 22885754; PubMed Central PMCID: PMC3457116.

22. Vílchez JI, García-Fontana C, Román-Naranjo D, González-López J, Manzanera M. Plant Drought Tolerance Enhancement by Trehalose Production of Desiccation-Tolerant Microorganisms. Frontiers in Microbiology. 2016;7:1577. doi: 10.3389/fmicb.2016.01577 PMC5043138. 27746776

23. Sugawara M, Cytryn EJ, Sadowsky MJ. Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Appl Environ Microbiol. 2010;76(4):1071–81. Epub 2009/12/22. doi: 10.1128/AEM.02483-09 20023090; PubMed Central PMCID: PMC2820964.

24. Kuczynska-Wisnik D, Stojowska K, Matuszewska E, Leszczynska D, Algara MM, Augustynowicz M, et al. Lack of intracellular trehalose affects formation of Escherichia coli persister cells. Microbiol-Sgm. 2015;161:786–96. doi: 10.1099/mic.0.000012 WOS:000355366600010. 25500492

25. Murphy HN, Stewart GR, Mischenko VV, Apt AS, Harris R, McAlister MS, et al. The OtsAB pathway is essential for trehalose biosynthesis in Mycobacterium tuberculosis. J Biol Chem. 2005;280(15):14524–9. Epub 2005/02/11. doi: 10.1074/jbc.M414232200 15703182.

26. Kalscheuer R, Syson K, Veeraraghavan U, Weinrick B, Biermann KE, Liu Z, et al. Self-poisoning of Mycobacterium tuberculosis by targeting GlgE in an alpha-glucan pathway. Nature Chemical Biology. 2010;6(5):376–84. doi: 10.1038/nchembio.340 WOS:000276823200017. 20305657

27. Piazza A, Zimaro T, Garavaglia BS, Ficarra FA, Thomas L, Marondedze C, et al. The dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses. J Exp Bot. 2015;66(9):2795–811. Epub 2015/03/17. doi: 10.1093/jxb/erv095 25770587; PubMed Central PMCID: PMC4986880.

28. Pazos-Rojas LA, Munoz-Arenas LC, Rodriguez-Andrade O, Lopez-Cruz LE, Lopez-Ortega O, Lopes-Olivares F, et al. Desiccation-induced viable but nonculturable state in Pseudomonas putida KT2440, a survival strategy. Plos One. 2019;14(7). ARTN e0219554 doi: 10.1371/journal.pone.0219554 WOS:000484971300010

29. De Smet KAL, Weston A, Brown IN, Young DB, Robertson BD. Three pathways for trehalose biosynthesis in mycobacteria. Microbiology. 2000;146(1):199–208. doi: 10.1099/00221287-146-1-199 10658666

30. Giaever HM, Styrvold OB, Kaasen I, Strom AR. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. Journal of Bacteriology. 1988;170(6):2841–9. Epub 1988/06/01. doi: 10.1128/jb.170.6.2841-2849.1988 3131312; PubMed Central PMCID: PMC211211.

31. Wang TF, Jia SR, Dai K, Liu HJ, Wang RM. Cloning and expression of a trehalose synthase from Pseudomonas putida KT2440 for the scale-up production of trehalose from maltose. Canadian journal of microbiology. 2014;60(9):599–604. doi: 10.1139/cjm-2014-0330 WOS:000341919200006. 25204684

32. Miah F, Koliwer-Brandl H, Rejzek M, Field Robert A, Kalscheuer R, Bornemann S. Flux through Trehalose Synthase Flows from Trehalose to the Alpha Anomer of Maltose in Mycobacteria. Chemistry & biology. 2013;20(4):487–93. doi: 10.1016/j.chembiol.2013.02.014 PMC3918855. 23601637

33. Maruta K, Nakada T, Kubota M, Chaen H, Sugimoto T, Kurimoto M, et al. Formation of trehalose from maltooligosaccharides by a novel enzymatic system. Bioscience, Biotechnology, and Biochemistry. 1995;59(10):1829–34. doi: 10.1271/bbb.59.1829 8534970

34. Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G. Insights on the evolution of trehalose biosynthesis. BMC Evolutionary Biology. 2006;6:109–. doi: 10.1186/1471-2148-6-109 17178000.

35. Edstrom RD. Structure of a low molecular weight form of glycogen isolated from the liver in a case of glycogen storage disease. J Biol Chem. 1972;247(5):1360–7. Epub 1972/03/10. 4334997.

36. Sambou T, Dinadayala P, Stadthagen G, Barilone N, Bordat Y, Constant P, et al. Capsular glucan and intracellular glycogen of Mycobacterium tuberculosis: biosynthesis and impact on the persistence in mice. Molecular Microbiology. 2008;70(3):762–74. doi: 10.1111/j.1365-2958.2008.06445.x 18808383

37. Koliwer-Brandl H, Syson K, van de Weerd R, Chandra G, Appelmelk B, Alber M, et al. Metabolic network for the biosynthesis of intra- and extracellular α-glucans required for virulence of Mycobacterium tuberculosis. PLOS Pathogens. 2016;12(8):e1005768. doi: 10.1371/journal.ppat.1005768 27513637

38. Preiss J. Bacterial glycogen synthesis and its regulation. Annual review of microbiology. 1984;38:419–58. Epub 1984/01/01. doi: 10.1146/annurev.mi.38.100184.002223 6093684.

39. Espada J. Enzymic Synthesis of Adenosine Diphosphate Glucose from Glucose 1-Phosphate and Adenosine Triphosphate. Journal of Biological Chemistry. 1962;237(12):3577–81.

40. Baecker PA, Furlong CE, Preiss J. Biosynthesis of bacterial glycogen. Primary structure of Escherichia coli ADP-glucose synthetase as deduced from the nucleotide sequence of the glgC gene. Journal of Biological Chemistry. 1983;258(8):5084–8.

41. Fox J, Kawaguchi K, Greenberg E, Preiss J. Biosynthesis of bacterial glycogen. Purification and properties of the Escherichia coli B ADPglucose:1,4-alpha-D-glucan 4-alpha-glucosyltransferase. Biochemistry. 1976;15(4):849–57. Epub 1976/02/24. doi: 10.1021/bi00649a019 2288.

42. Kumar A, Larsen CE, Preiss J. Biosynthesis of bacterial glycogen. Primary structure of Escherichia coli ADP-glucose:alpha-1,4-glucan, 4-glucosyltransferase as deduced from the nucleotide sequence of the glgA gene. J Biol Chem. 1986;261(34):16256–9. Epub 1986/12/05. 3097003.

43. Larner J. The action of branching enzymes on outer chains of glycogen. J Biol Chem. 1953;202(2):491–503. Epub 1953/06/01. 13061474.

44. Abad MC, Binderup K, Rios-Steiner J, Arni RK, Preiss J, Geiger JH. The X-ray crystallographic structure of Escherichia coli branching enzyme. J Biol Chem. 2002;277(44):42164–70. Epub 2002/08/28. doi: 10.1074/jbc.M205746200 12196524.

45. Dauvillee D, Kinderf IS, Li Z, Kosar-Hashemi B, Samuel MS, Rampling L, et al. Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol. 2005;187(4):1465–73. Epub 2005/02/03. doi: 10.1128/JB.187.4.1465-1473.2005 15687211; PubMed Central PMCID: PMC545640.

46. Alonso-Casajús N, Dauvillée D, Viale AM, Muñoz FJ, Baroja-Fernández E, Morán-Zorzano MT, et al. Glycogen Phosphorylase, the Product of the glgP Gene, Catalyzes Glycogen Breakdown by Removing Glucose Units from the Nonreducing Ends in Escherichia coli. Journal of Bacteriology. 2006;188(14):5266–72. doi: 10.1128/JB.01566-05 PMC1539952. 16816199

47. Elbein AD, Pastuszak I, Tackett AJ, Wilson T, Pan YT. Last step in the conversion of trehalose to glycogen: a mycobacterial enzyme that transfers maltose from maltose 1-phosphate to glycogen. J Biol Chem. 2010;285(13):9803–12. Epub 2010/02/02. doi: 10.1074/jbc.M109.033944 20118231; PubMed Central PMCID: PMC2843229.

48. Chandra G, Chater KF, Bornemann S. Unexpected and widespread connections between bacterial glycogen and trehalose metabolism. Microbiology. 2011;157(Pt 6):1565–72. Epub 2011/04/09. doi: 10.1099/mic.0.044263-0 21474533.

49. Freeman BC, Chen C, Beattie GA. Identification of the trehalose biosynthetic loci of Pseudomonas syringae and their contribution to fitness in the phyllosphere. Environmental Microbiology. 2010;12(6):1486–97. Epub 2010/03/03. doi: 10.1111/j.1462-2920.2010.02171.x 20192963.

50. Djonović S, Urbach JM, Drenkard E, Bush J, Feinbaum R, Ausubel JL, et al. Trehalose biosynthesis promotes Pseudomonas aeruginosa pathogenicity in plants. PLoS Pathogens. 2013;9(3):e1003217. doi: 10.1371/journal.ppat.1003217 23505373

51. Harty CE, Martins D, Doing G, Mould DL, Clay ME, Occhipinti P, et al. Ethanol Stimulates Trehalose Production through a SpoT-DksA-AlgU-Dependent Pathway in Pseudomonas aeruginosa. Journal of Bacteriology. 2019;201(12). doi:ARTN e00794 doi: 10.1128/JB.00794-18 WOS:000468610700012. 30936375

52. Behrends V, Ryall B, Wang XZ, Bundy JG, Williams HD. Metabolic profiling of Pseudomonas aeruginosa demonstrates that the anti-sigma factor MucA modulates osmotic stress tolerance. Molecular bioSystems. 2010;6(3):562–9. doi: 10.1039/b918710c WOS:000274654400013. 20174684

53. Behrends V, Ryall B, Zlosnik JEA, Speert DP, Bundy JG, Williams HD. Metabolic adaptations of Pseudomonas aeruginosa during cystic fibrosis chronic lung infections. Environmental Microbiology. 2013;15(2):398–408. doi: 10.1111/j.1462-2920.2012.02840.x WOS:000314211100009. 22882524

54. Mao F, Dam P, Chou J, Olman V, Xu Y. DOOR: a database for prokaryotic operons. Nucleic Acids Res. 2009;37(Database issue):D459–63. Epub 2008/11/08. doi: 10.1093/nar/gkn757 18988623; PubMed Central PMCID: PMC2686520.

55. Freeman BC, Chen C, Beattie GA. Identification of the trehalose biosynthetic loci of Pseudomonas syringae and their contribution to fitness in the phyllosphere. Environ Microbiol. 2010;12(6):1486–97. doi: 10.1111/j.1462-2920.2010.02171.x 20192963.

56. Winsor GL, Griffiths EJ, Lo R, Dhillon BK, Shay JA, Brinkman FS. Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the Pseudomonas genome database. Nucleic Acids Res. 2016;44(D1):D646–53. Epub 2015/11/19. doi: 10.1093/nar/gkv1227 26578582; PubMed Central PMCID: PMC4702867.

57. Syson K, Stevenson CEM, Rejzek M, Fairhurst SA, Nair A, Bruton CJ, et al. Structure of Streptomyces Maltosyltransferase GlgE, a Homologue of a Genetically Validated Anti-tuberculosis Target. Journal of Biological Chemistry. 2011;286(44):38298–310. doi: 10.1074/jbc.M111.279315 WOS:000296594200043. 21914799

58. Kartal O, Mahlow S, Skupin A, Ebenhoh O. Carbohydrate-active enzymes exemplify entropic principles in metabolism. Mol Syst Biol. 2011;7:542. Epub 2011/10/27. doi: 10.1038/msb.2011.76 22027553; PubMed Central PMCID: PMC3261701.

59. Bailey JM, Whelan WJ. Physical properties of starch. I. Relationship between iodine stain and chain length. J Biol Chem. 1961;236:969–73. Epub 1961/04/01. 13685959.

60. Rashid AM, Batey SFD, Syson K, Koliwer-Brandl H, Miah F, Barclay JE, et al. Assembly of alpha-Glucan by GlgE and GlgB in Mycobacteria and Streptomycetes. Biochemistry. 2016;55(23):3270–84. doi: 10.1021/acs.biochem.6b00209 WOS:000378016500012. 27221142

61. Holden PA. Biofilms in unsaturated environments. In: Doyle RJ, editor. Methods in Enzymology. 337: Academic Press; 2001. p. 125–43. doi: 10.1016/s0076-6879(01)37011-8 11398425

62. Van De Mortel M, Halverson LJ. Cell envelope components contributing to biofilm growth and survival of Pseudomonas putida in low-water-content habitats. Molecular Microbiology. 2004;52(3):735–50. doi: 10.1111/j.1365-2958.2004.04008.x 15101980

63. Manzanera M, García-Fontana C, Vílchez JI, Narváez-Reinaldo JJ, González-López J. Genome sequence of Microbacterium sp. Strain 3J1, a highly desiccation-tolerant bacterium that promotes plant growth. Genome Announcements. 2015;3(4):e00713–15. doi: 10.1128/genomeA.00713-15 PMC4551875. 26316631

64. Klähn S, Hagemann M. Compatible solute biosynthesis in cyanobacteria. Environmental Microbiology. 2011;13(3):551–62. doi: 10.1111/j.1462-2920.2010.02366.x 21054739

65. Yoshida T, Sakamoto T. Water-stress induced trehalose accumulation and control of trehalase in the cyanobacterium Nostoc punctiforme IAM M-15. The Journal of General and Applied Microbiology. 2009;55(2):135–45. doi: 10.2323/jgam.55.135 19436130

66. Gulez G, Dechesne A, Workman CT, Smets BF. Transcriptome dynamics of Pseudomonas putida KT2440 under water stress. Appl Environ Microb. 2012;78(3):676–83. Epub 2011/12/06. doi: 10.1128/AEM.06150-11 22138988; PubMed Central PMCID: PMC3264132.

67. Freeman BC, Chen C, Yu X, Nielsen L, Peterson K, Beattie GA. Physiological and transcriptional responses to osmotic stress of two Pseudomonas syringae strains that differ in their epiphytic fitness and osmotolerance. Journal of Bacteriology. 2013. doi: 10.1128/JB.00787-13 23955010

68. Preiss J. Biochemistry and Molecular Biology of Glycogen Synthesis in Bacteria and Mammals and Starch Synthesis in Plants. In: Liu H-W, Mander L, editors. Comprehensive Natural Products II. Oxford: Elsevier; 2010. p. 429–91.

69. Geurtsen J, Chedammi S, Mesters J, Cot M, Driessen NN, Sambou T, et al. Identification of Mycobacterial α-Glucan as a novel ligand for DC-SIGN: involvement of mycobacterial capsular polysaccharides in host immune modulation. The Journal of Immunology. 2009;183(8):5221–31. doi: 10.4049/jimmunol.0900768 19783687

70. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, et al. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature. 2000;406. doi: 10.1038/35023079 10984043

71. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, et al. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A. 2003;100(18):10181–6. Epub 2003/08/21. doi: 10.1073/pnas.1731982100 12928499; PubMed Central PMCID: PMC193536.

72. Quiles F, Polyakov P, Humbert F, Francius G. Production of extracellular glycogen by Pseudomonas fluorescens: spectroscopic evidence and conformational analysis by biomolecular recognition. Biomacromolecules. 2012;13(7):2118–27. Epub 2012/06/13. doi: 10.1021/bm300497c 22686500.

73. Aspedon A, Palmer K, Whiteley M. Microarray analysis of the osmotic stress response in Pseudomonas aeruginosa. J Bacteriol. 2006;188. doi: 10.1128/JB.188.7.2721-2725.2006 16547062

74. Miller JH. Experiments in molecular genetics: Cold Spring Harbor Laboratory; 1972.

75. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual: Cold Spring Harbor Laboratory; 1989.

76. Voisard C, Bull CT, Keel C, Laville J, Maurhofer M, Schnider U, et al. Biocontrol of Root Diseases by Pseudomonas fluorescens CHA0: Current Concepts and Experimental Approaches. Molecular Ecology of Rhizosphere Microorganisms: Wiley-VCH Verlag GmbH; 1994. p. 67–89. doi: 10.1016/0167-5273(94)90206-2 8181884

77. Choi KH, Kumar A, Schweizer HP. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods. 2006;64(3):391–7. Epub 2005/07/01. doi: 10.1016/j.mimet.2005.06.001 15987659.

78. Malone JG, Jaeger T, Spangler C, Ritz D, Spang A, Arrieumerlou C, et al. YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa. PLoS Pathog. 2010;6(3):e1000804. doi: 10.1371/journal.ppat.1000804 20300602.

79. Heeb S, Itoh Y, Nishijyo T, Schnider U, Keel C, Wade J, et al. Small, stable shuttle vectors based on the minimal pVS1 replicon for use in gram-negative, plant-associated bacteria. Molecular plant-microbe interactions: MPMI. 2000;13(2):232–7. doi: 10.1094/MPMI.2000.13.2.232 10659714.

80. Choi K-H, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, et al. A Tn7-based broad-range bacterial cloning and expression system. Nature methods. 2005;2:443. doi: 10.1038/nmeth765 https://www.nature.com/articles/nmeth765#supplementary-information. 15908923

81. Studier FW. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif. 2005;41(1):207–34. Epub 2005/05/26. doi: 10.1016/j.pep.2005.01.016 15915565.

82. Usui T, Yokoyama M, Yamaoka N, Matsuda K, Tuzimura K, Sugiyama H, et al. Proton magnetic resonance spectra of D-gluco-oligosaccharides and D-glucans. Carbohydrate research. 1974;33(1):105–16. doi:http://dx.doi.org/10.1016/S0008-6215(00)82944-4

83. De Goffau MC, Yang X, Van Dijl JM, Harmsen HJM. Bacterial pleomorphism and competition in a relative humidity gradient. Environmental Microbiology. 2009;11(4):809–22. doi: 10.1111/j.1462-2920.2008.01802.x 19040453


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