Control of mRNA translation by dynamic ribosome modification


Autoři: Lucia Grenga aff001;  Richard Howard Little aff001;  Govind Chandra aff001;  Stuart Daniel Woodcock aff001;  Gerhard Saalbach aff001;  Richard James Morris aff003;  Jacob George Malone aff001
Působiště autorů: Molecular Microbiology, John Innes Centre, Norwich, Norfolk, United Kingdom aff001;  School of Biological Sciences, University of East Anglia, Norwich, Norfolk, United Kingdom aff002;  Computational and Systems Biology, John Innes Centre, Norwich, Norfolk, United Kingdom aff003
Vyšlo v časopise: Control of mRNA translation by dynamic ribosome modification. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008837
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008837

Souhrn

Control of mRNA translation is a crucial regulatory mechanism used by bacteria to respond to their environment. In the soil bacterium Pseudomonas fluorescens, RimK modifies the C-terminus of ribosomal protein RpsF to influence important aspects of rhizosphere colonisation through proteome remodelling. In this study, we show that RimK activity is itself under complex, multifactorial control by the co-transcribed phosphodiesterase trigger enzyme (RimA) and a polyglutamate-specific protease (RimB). Furthermore, biochemical experimentation and mathematical modelling reveal a role for the nucleotide second messenger cyclic-di-GMP in coordinating these activities. Active ribosome regulation by RimK occurs by two main routes: indirectly, through changes in the abundance of the global translational regulator Hfq and directly, with translation of surface attachment factors, amino acid transporters and key secreted molecules linked specifically to RpsF modification. Our findings show that post-translational ribosomal modification functions as a rapid-response mechanism that tunes global gene translation in response to environmental signals.

Klíčová slova:

Adenosine triphosphatase – Glutamate – Ligases – Messenger RNA – Proteases – Protein translation – Proteomes – Ribosomes


Zdroje

1. Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi S, et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol. 2018;3(4):470–80. Epub 2018/03/21. doi: 10.1038/s41564-018-0129-3 29556109.

2. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, et al. Defining the core Arabidopsis thaliana root microbiome. Nature. 2012;488(7409):86–90. doi: 10.1038/nature11237 22859206; PubMed Central PMCID: PMC4074413.

3. Mauchline TH, Malone JG. Life in earth—the root microbiome to the rescue? Curr Opin Microbiol. 2017;37:23–8. doi: 10.1016/j.mib.2017.03.005 28437662.

4. Alsohim AS, Taylor TB, Barrett GA, Gallie J, Zhang XX, Altamirano-Junqueira AE, et al. The biosurfactant viscosin produced by Pseudomonas fluorescens SBW25 aids spreading motility and plant growth promotion. Environmental microbiology. 2014;16(7):2267–81. doi: 10.1111/1462-2920.12469 24684210.

5. Chin-A-Woeng TFC, de Priester W, van der Bij AJ, Lugtenberg BJJ. Description of the Colonization of a Gnotobiotic Tomato Rhizosphere by Pseudomonas fluorescens Biocontrol Strain WCS365, Using Scanning Electron Microscopy. Molecular Plant-Microbe Interactions. 1997;10(1):79–86. doi: 10.1094/mpmi.1997.10.1.79

6. Campilongo R, Fung RKY, Little RH, Grenga L, Trampari E, Pepe S, et al. One ligand, two regulators and three binding sites: How KDPG controls primary carbon metabolism in Pseudomonas. PLoS Genet. 2017;13(6):e1006839. doi: 10.1371/journal.pgen.1006839 28658302; PubMed Central PMCID: PMC5489143.

7. Grenga L, Chandra G, Saalbach G, Galmozzi CV, Kramer G, Malone JG. Analysing the complex regulatory landscape of Hfq—an integrative, multi-omics approach. Front Microbiol. 2017; (8):1784.

8. Martinez-Granero F, Navazo A, Barahona E, Redondo-Nieto M, Gonzalez de Heredia E, Baena I, et al. Identification of flgZ as a flagellar gene encoding a PilZ domain protein that regulates swimming motility and biofilm formation in Pseudomonas. PloS one. 2014;9(2):e87608. doi: 10.1371/journal.pone.0087608 24504373; PubMed Central PMCID: PMC3913639.

9. Jenal U, Reinders A, Lori C. Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol. 2017;15(5):271–84. doi: 10.1038/nrmicro.2016.190 28163311.

10. Barahona E, Navazo A, Martinez-Granero F, Zea-Bonilla T, Perez-Jimenez RM, Martin M, et al. Pseudomonas fluorescens F113 Mutant with Enhanced Competitive Colonization Ability and Improved Biocontrol Activity against Fungal Root Pathogens. Appl Environ Microbiol. 2011;77(15):5412–9. Epub 2011/06/21. AEM.00320-11 [pii] doi: 10.1128/AEM.00320-11 21685161; PubMed Central PMCID: PMC3147442.

11. Little RH, Woodcock SD, Campilongo R, Fung RKY, Heal R, Humphries L, et al. Differential Regulation of Genes for Cyclic-di-GMP Metabolism Orchestrates Adaptive Changes During Rhizosphere Colonization by Pseudomonas fluorescens. Frontiers in Microbiology. 2019;10. ARTN 108910.3389/fmicb.2019.01089. WOS:000468022400001.

12. O'Neal L, Akhter S, Alexandre G. A PilZ-Containing Chemotaxis Receptor Mediates Oxygen and Wheat Root Sensing in Azospirillum brasilense. Front Microbiol. 2019;10:312. Epub 2019/03/19. doi: 10.3389/fmicb.2019.00312 30881352; PubMed Central PMCID: PMC6406031.

13. Ramos-Gonzalez MI, Travieso ML, Soriano MI, Matilla MA, Huertas-Rosales O, Barrientos-Moreno L, et al. Genetic Dissection of the Regulatory Network Associated with High c-di-GMP Levels in Pseudomonas putida KT2440. Front Microbiol. 2016;7:1093. Epub 2016/08/05. doi: 10.3389/fmicb.2016.01093 27489550; PubMed Central PMCID: PMC4951495.

14. Grenga L, Little RH, Malone JG. Quick Change—post-transcriptional regulation in Pseudomonas. FEMS Microbiol Lett. 2017. doi: 10.1093/femsle/fnx125 28605536.

15. 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(24):12547–55. Epub 2016/04/30. doi: 10.1074/jbc.R115.711507 27129226; PubMed Central PMCID: PMC4933438.

16. Silby MW, Cerdeno-Tarraga AM, Vernikos GS, Giddens SR, Jackson RW, Preston GM, et al. Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol. 2009;10(5):R51. doi: 10.1186/gb-2009-10-5-r51 19432983.

17. Moscoso JA, Jaeger T, Valentini M, Hui K, Jenal U, Filloux A. The diguanylate cyclase SadC is a central player in Gac/Rsm-mediated biofilm formation in Pseudomonas aeruginosa. Journal of bacteriology. 2014;196(23):4081–8. doi: 10.1128/JB.01850-14 25225264; PubMed Central PMCID: PMC4248864.

18. Moscoso JA, Mikkelsen H, Heeb S, Williams P, Filloux A. The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environmental microbiology. 2011;13(12):3128–38. doi: 10.1111/j.1462-2920.2011.02595.x 21955777.

19. Little RH, Grenga L, Saalbach G, Howat AM, Pfeilmeier S, Trampari E, et al. Adaptive Remodeling of the Bacterial Proteome by Specific Ribosomal Modification Regulates Pseudomonas Infection and Niche Colonisation. PLoS Genet. 2016;12(2):e1005837. doi: 10.1371/journal.pgen.1005837 26845436.

20. Irie Y, Starkey M, Edwards AN, Wozniak DJ, Romeo T, Parsek MR. Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post-transcriptionally by RsmA. Molecular microbiology. 2010;78(1):158–72. Epub 2010/08/26. doi: 10.1111/j.1365-2958.2010.07320.x 20735777; PubMed Central PMCID: PMC2984543.

21. Brencic A, Lory S. Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Molecular microbiology. 2009;72(3):612–32. Epub 2009/05/12. MMI6670 [pii] doi: 10.1111/j.1365-2958.2009.06670.x 19426209.

22. Kino K, Arai T, Arimura Y. Poly-alpha-glutamic acid synthesis using a novel catalytic activity of RimK from Escherichia coli K-12. Appl Environ Microbiol. 2011;77(6):2019–25. Epub 2011/02/01. doi: 10.1128/AEM.02043-10 21278279; PubMed Central PMCID: PMC3067337.

23. Kaczanowska M, Ryden-Aulin M. Ribosome biogenesis and the translation process in Escherichia coli. Microbiol Mol Biol Rev. 2007;71(3):477–94. Epub 2007/09/07. doi: 10.1128/MMBR.00013-07 17804668; PubMed Central PMCID: PMC2168646.

24. Shen J, Meldrum A, Poole K. FpvA receptor involvement in pyoverdine biosynthesis in Pseudomonas aeruginosa. Journal of bacteriology. 2002;184(12):3268–75. Epub 2002/05/25. doi: 10.1128/jb.184.12.3268-3275.2002 12029043; PubMed Central PMCID: PMC135083.

25. Nait Chabane Y, Marti S, Rihouey C, Alexandre S, Hardouin J, Lesouhaitier O, et al. Characterisation of pellicles formed by Acinetobacter baumannii at the air-liquid interface. PloS one. 2014;9(10):e111660. Epub 2014/11/02. doi: 10.1371/journal.pone.0111660 25360550; PubMed Central PMCID: PMC4216135.

26. Poole P, Ramachandran V, Terpolilli J. Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol. 2018;16(5):291–303. Epub 2018/01/31. doi: 10.1038/nrmicro.2017.171 29379215.

27. Schulz S, Eckweiler D, Bielecka A, Nicolai T, Franke R, Dotsch A, et al. Elucidation of sigma factor-associated networks in Pseudomonas aeruginosa reveals a modular architecture with limited and function-specific crosstalk. PLoS Pathog. 2015;11(3):e1004744. Epub 2015/03/18. doi: 10.1371/journal.ppat.1004744 25780925; PubMed Central PMCID: PMC4362757.

28. Lindenberg S, Klauck G, Pesavento C, Klauck E, Hengge R. The EAL domain protein YciR acts as a trigger enzyme in a c-di-GMP signalling cascade in E. coli biofilm control. The EMBO journal. 2013;32(14):2001–14. Epub 2013/05/28. doi: 10.1038/emboj.2013.120 23708798; PubMed Central PMCID: PMC3715855.

29. Loveland AB, Korostelev AA. Structural dynamics of protein S1 on the 70S ribosome visualized by ensemble cryo-EM. Methods. 2018;137:55–66. Epub 2017/12/17. doi: 10.1016/j.ymeth.2017.12.004 29247757; PubMed Central PMCID: PMC5866760.

30. Duval M, Korepanov A, Fuchsbauer O, Fechter P, Haller A, Fabbretti A, et al. Escherichia coli ribosomal protein S1 unfolds structured mRNAs onto the ribosome for active translation initiation. PLoS Biol. 2013;11(12):e1001731. Epub 2013/12/18. doi: 10.1371/journal.pbio.1001731 24339747; PubMed Central PMCID: PMC3858243.

31. Sukhodolets MV, Garges S. Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq. Biochemistry. 2003;42(26):8022–34. Epub 2003/07/02. doi: 10.1021/bi020638i 12834354.

32. Kambara TK, Ramsey KM, Dove SL. Pervasive Targeting of Nascent Transcripts by Hfq. Cell Rep. 2018;23(5):1543–52. Epub 2018/05/03. doi: 10.1016/j.celrep.2018.03.134 29719264; PubMed Central PMCID: PMC5990048.

33. Carmichael GG, Weber K, Niveleau A, Wahba AJ. The host factor required for RNA phage Qbeta RNA replication in vitro. Intracellular location, quantitation, and purification by polyadenylate-cellulose chromatography. J Biol Chem. 1975;250(10):3607–612. Epub 1975/05/25. 805130.

34. Wahba AJ, Miller MJ, Niveleau A, Landers TA, Carmichael GG, Weber K, et al. Subunit I of G beta replicase and 30 S ribosomal protein S1 of Escherichia coli. Evidence for the identity of the two proteins. J Biol Chem. 1974;249(10):3314–6. Epub 1974/05/25. 4208476.

35. Inouye H, Pollack Y, Petre J. Physical and functional homology between ribosomal protein S1 and interference factor i. Eur J Biochem. 1974;45(1):109–17. Epub 1974/06/01. doi: 10.1111/j.1432-1033.1974.tb03535.x 4213953.

36. Kang WK, Icho T, Isono S, Kitakawa M, Isono K. Characterization of the gene rimK responsible for the addition of glutamic acid residues to the C-terminus of ribosomal protein S6 in Escherichia coli K12. Molecular & general genetics: MGG. 1989;217(2–3):281–8. Epub 1989/06/01. doi: 10.1007/BF02464894 2570347.

37. Miller JH. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York. 1972:352–5.

38. Little R, Salinas P, Slavny P, Clarke TA, Dixon R. Substitutions in the redox-sensing PAS domain of the NifL regulatory protein define an inter-subunit pathway for redox signal transmission. Molecular microbiology. 2011;82(1):222–35. Epub 2011/08/23. doi: 10.1111/j.1365-2958.2011.07812.x 21854469.

39. Scott TA, Heine D, Qin Z, Wilkinson B. An L-threonine transaldolase is required for L-threo-beta-hydroxy-alpha-amino acid assembly during obafluorin biosynthesis. Nat Commun. 2017;8. ARTN 1593510.1038/ncomms15935. WOS:000404029700001.

40. King EO, Ward MK, Raney DE. Two simple media for the demonstration of pyocyanin and fluorescin. The Journal of laboratory and clinical medicine. 1954;44(2):301–7. Epub 1954/08/01. 13184240.

41. Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47(D1):D442–D50. Epub 2018/11/06. doi: 10.1093/nar/gky1106 30395289; PubMed Central PMCID: PMC6323896.

42. Oh E BA, Sandikci A, Huber D, Chaba R, Gloge F, Nichols RJ, Typas A, Gross CA, Kramer G, Weissman JS, Bukau B. Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell. 2011;147(6):1295–308. doi: 10.1016/j.cell.2011.10.044 22153074

43. Becker AH, Oh E, Weissman JS, Kramer G, Bukau B. Selective ribosome profiling as a tool for studying the interaction of chaperones and targeting factors with nascent polypeptide chains and ribosomes. Nat Protoc. 2013;8(11):2212–39. doi: 10.1038/nprot.2013.133 WOS:000326164100010. 24136347

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2020 Číslo 6

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×