Identification and Functional Characterization of Small Alarmone Synthetases in Corynebacterium glutamicum

Ruwe M, Kalinowski J, Persicke M (2017)
Frontiers in Microbiology 8: 1601.

Download
OA 1.98 MB
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Volltext vorhanden für diesen Nachweis
Abstract / Bemerkung
The hyperphosphorylated guanosine derivatives ppGpp and pppGpp represent global regulators of the bacterial stress response, as they act as central elements of the stringent response system. Although it was assumed that both, (p)ppGpp synthesis and hydrolysis, are catalyzed by one bifunctional RSH-protein in the actinobacterial model organism Corynebacterium glutamicum ATCC 13032, two putative short alarmone synthetases (SASs) were identified by bioinformatic analyses. The predicted sequences of both enzymes, designated as RelP*Cg and RelSCg, exhibit high similarities to the conserved (p)ppGpp synthetase catalytic domain. In the context of sequence analysis, significant differences were found between the RelP variants of different C. glutamicum isolates. In contrast to the bifunctional RelA/SpoT homolog (RSH) protein RelCg, whose gene deletion results in a reduced growth rate, no change in growth characteristics were observed for deletion mutants of the putative SAS proteins under standard growth conditions. The growth deficit of the Δrel strain could be restored by the additional deletion of the gene encoding RelSCg, which clearly indicates a functional relationship between both enzymes. The predicted pyrophosphokinase activity of RelSCg was demonstrated by means of genetic complementation of an Escherichia coli ΔrelAΔspoT strain. For the expression of RelP*Cg, as well as the slightly differing variant RelPCg from C. glutamicum AS1.542, no complementation was observed, concluding that both RelP versions possess no significant pyrophosphokinase activity in vivo. The results were confirmed by in vitro characterization of the corresponding proteins. In the course of this investigation, the additional conversion of GMP to pGpp was determined for the enzyme RelSCg. Since the SAS species analyzed extend both the network of stringent response related enzymes and the number of substances involved, the study of this class of enzymes is an important component in understanding the bacterial stress response. In addition to the comprehension of important biological processes, such as growth rate regulation and the survival of pathogenic species in the host organism, SAS enzymes can be used to produce novel hyperphosphorylated nucleotide species, such as pGpp.
Erscheinungsjahr
Zeitschriftentitel
Frontiers in Microbiology
Band
8
Art.-Nr.
1601
eISSN
Finanzierungs-Informationen
Article Processing Charge funded by the Deutsche Forschungsgemeinschaft and the Open Access Publication Fund of Bielefeld University.
PUB-ID

Zitieren

Ruwe M, Kalinowski J, Persicke M. Identification and Functional Characterization of Small Alarmone Synthetases in Corynebacterium glutamicum. Frontiers in Microbiology. 2017;8: 1601.
Ruwe, M., Kalinowski, J., & Persicke, M. (2017). Identification and Functional Characterization of Small Alarmone Synthetases in Corynebacterium glutamicum. Frontiers in Microbiology, 8, 1601. doi:10.3389/fmicb.2017.01601
Ruwe, M., Kalinowski, J., and Persicke, M. (2017). Identification and Functional Characterization of Small Alarmone Synthetases in Corynebacterium glutamicum. Frontiers in Microbiology 8:1601.
Ruwe, M., Kalinowski, J., & Persicke, M., 2017. Identification and Functional Characterization of Small Alarmone Synthetases in Corynebacterium glutamicum. Frontiers in Microbiology, 8: 1601.
M. Ruwe, J. Kalinowski, and M. Persicke, “Identification and Functional Characterization of Small Alarmone Synthetases in Corynebacterium glutamicum”, Frontiers in Microbiology, vol. 8, 2017, : 1601.
Ruwe, M., Kalinowski, J., Persicke, M.: Identification and Functional Characterization of Small Alarmone Synthetases in Corynebacterium glutamicum. Frontiers in Microbiology. 8, : 1601 (2017).
Ruwe, Matthias, Kalinowski, Jörn, and Persicke, Marcus. “Identification and Functional Characterization of Small Alarmone Synthetases in Corynebacterium glutamicum”. Frontiers in Microbiology 8 (2017): 1601.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
This Item is protected by copyright and/or related rights. [...]
Volltext(e)
Access Level
OA Open Access
Zuletzt Hochgeladen
2017-09-20T13:13:23Z

2 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Functional Characterization of a Small Alarmone Hydrolase in Corynebacterium glutamicum.
Ruwe M, Rückert C, Kalinowski J, Persicke M., Front Microbiol 9(), 2018
PMID: 29867827

52 References

Daten bereitgestellt von Europe PubMed Central.

The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins.
Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, Burkovski A, Dusch N, Eggeling L, Eikmanns BJ, Gaigalat L, Goesmann A, Hartmann M, Huthmacher K, Kramer R, Linke B, McHardy AC, Meyer F, Mockel B, Pfefferle W, Puhler A, Rey DA, Ruckert C, Rupp O, Sahm H, Wendisch VF, Wiegrabe I, Tauch A., J. Biotechnol. 104(1-3), 2003
PMID: 12948626
The role of the Corynebacterium glutamicum rel gene in (p)ppGpp metabolism.
Wehmeier L, Schafer A, Burkovski A, Kramer R, Mechold U, Malke H, Puhler A, Kalinowski J., Microbiology (Reading, Engl.) 144 ( Pt 7)(), 1998
PMID: 9695918
(p)ppGpp: still magical?
Potrykus K, Cashel M., Annu. Rev. Microbiol. 62(), 2008
PMID: 18454629
Probing teichoic acid genetics with bioactive molecules reveals new interactions among diverse processes in bacterial cell wall biogenesis.
D'Elia MA, Millar KE, Bhavsar AP, Tomljenovic AM, Hutter B, Schaab C, Moreno-Hagelsieb G, Brown ED., Chem. Biol. 16(5), 2009
PMID: 19477419
Arabidopsis RelA/SpoT homologs implicate (p)ppGpp in plant signaling.
van der Biezen EA, Sun J, Coleman MJ, Bibb MJ, Jones JD., Proc. Natl. Acad. Sci. U.S.A. 97(7), 2000
PMID: 10725385
Residual guanosine 3',5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations.
Xiao H, Kalman M, Ikehara K, Zemel S, Glaser G, Cashel M., J. Biol. Chem. 266(9), 1991
PMID: 2005134
The complete genome sequence of Escherichia coli K-12.
Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y., Science 277(5331), 1997
PMID: 9278503
The ACT domain family.
Chipman DM, Shaanan B., Curr. Opin. Struct. Biol. 11(6), 2001
PMID: 11751050
Occurrence of pppApp-synthesizing activity in actinomycetes and isolation of purine nucleotide pyrophosphotransferase.
Oki T, Yoshimoto A, Ogasawara T, Sato S, Takamatsu A., Arch. Microbiol. 107(2), 1976
PMID: 1259517
Chassis organism from Corynebacterium glutamicum--a top-down approach to identify and delete irrelevant gene clusters.
Unthan S, Baumgart M, Radek A, Herbst M, Siebert D, Bruhl N, Bartsch A, Bott M, Wiechert W, Marin K, Hans S, Kramer R, Seibold G, Frunzke J, Kalinowski J, Ruckert C, Wendisch VF, Noack S., Biotechnol J 10(2), 2014
PMID: 25139579
Differential regulation by ppGpp versus pppGpp in Escherichia coli.
Mechold U, Potrykus K, Murphy H, Murakami KS, Cashel M., Nucleic Acids Res. 41(12), 2013
PMID: 23620295
Isolation of RNA polymerase suppressors of a (p)ppGpp deficiency.
Murphy H, Cashel M., Meth. Enzymol. 371(), 2003
PMID: 14712731
The nucleotide-binding site of bacterial translation initiation factor 2 (IF2) as a metabolic sensor.
Milon P, Tischenko E, Tomsic J, Caserta E, Folkers G, La Teana A, Rodnina MV, Pon CL, Boelens R, Gualerzi CO., Proc. Natl. Acad. Sci. U.S.A. 103(38), 2006
PMID: 16968770
The magic dance of the alarmones (p)ppGpp.
Steinchen W, Bange G., Mol. Microbiol. 101(4), 2016
PMID: 27149325
Three gene products govern (p)ppGpp production by Streptococcus mutans.
Lemos JA, Lin VK, Nascimento MM, Abranches J, Burne RA., Mol. Microbiol. 65(6), 2007
PMID: 17714452
MS_RHII-RSD, a dual-function RNase HII-(p)ppGpp synthetase from Mycobacterium smegmatis.
Murdeshwar MS, Chatterji D., J. Bacteriol. 194(15), 2012
PMID: 22636779
Nutritional control of elongation of DNA replication by (p)ppGpp.
Wang JD, Sanders GM, Grossman AD., Cell 128(5), 2007
PMID: 17350574
Construction of a prophage-free variant of Corynebacterium glutamicum ATCC 13032 for use as a platform strain for basic research and industrial biotechnology.
Baumgart M, Unthan S, Ruckert C, Sivalingam J, Grunberger A, Kalinowski J, Bott M, Noack S, Frunzke J., Appl. Environ. Microbiol. 79(19), 2013
PMID: 23892752
ppGpp: magic beyond RNA polymerase.
Dalebroux ZD, Swanson MS., Nat. Rev. Microbiol. 10(3), 2012
PMID: 22337166
From (p)ppGpp to (pp)pGpp: Characterization of Regulatory Effects of pGpp Synthesized by the Small Alarmone Synthetase of Enterococcus faecalis.
Gaca AO, Kudrin P, Colomer-Winter C, Beljantseva J, Liu K, Anderson B, Wang JD, Rejman D, Potrykus K, Cashel M, Hauryliuk V, Lemos JA., J. Bacteriol. 197(18), 2015
PMID: 26124242
The bacterial stringent response, conserved in chloroplasts, controls plant fertilization.
Masuda S, Mizusawa K, Narisawa T, Tozawa Y, Ohta H, Takamiya K., Plant Cell Physiol. 49(2), 2008
PMID: 18178586
MSI and MSII made on ribosome in idling step of protein synthesis.
Haseltine WA, Block R, Gilbert W, Weber K., Nature 238(5364), 1972
PMID: 4559580
Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli.
Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ, Rabinowitz JD., Nat. Chem. Biol. 5(8), 2009
PMID: 19561621
Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
Guzman LM, Belin D, Carson MJ, Beckwith J., J. Bacteriol. 177(14), 1995
PMID: 7608087
Mutational analysis of the (p)ppGpp synthetase activity of the Rel enzyme of Mycobacterium tuberculosis.
Bag S, Das B, Dasgupta S, Bhadra RK., Arch. Microbiol. 196(8), 2014
PMID: 24859914
A charge reversal differentiates (p)ppGpp synthesis by monofunctional and bifunctional Rel proteins.
Sajish M, Tiwari D, Rananaware D, Nandicoori VK, Prakash B., J. Biol. Chem. 282(48), 2007
PMID: 17911108
Efficient electrotransformation of corynebacterium diphtheriae with a mini-replicon derived from the Corynebacterium glutamicum plasmid pGA1.
Tauch A, Kirchner O, Loffler B, Gotker S, Puhler A, Kalinowski J., Curr. Microbiol. 45(5), 2002
PMID: 12232668
Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis.
Nanamiya H, Kasai K, Nozawa A, Yun CS, Narisawa T, Murakami K, Natori Y, Kawamura F, Tozawa Y., Mol. Microbiol. 67(2), 2007
PMID: 18067544
Direct binding targets of the stringent response alarmone (p)ppGpp.
Kanjee U, Ogata K, Houry WA., Mol. Microbiol. 85(6), 2012
PMID: 22812515
Enzymatic assembly of DNA molecules up to several hundred kilobases.
Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, Smith HO., Nat. Methods 6(5), 2009
PMID: 19363495
Recent functional insights into the role of (p)ppGpp in bacterial physiology.
Hauryliuk V, Atkinson GC, Murakami KS, Tenson T, Gerdes K., Nat. Rev. Microbiol. 13(5), 2015
PMID: 25853779
BLAST+: architecture and applications.
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL., BMC Bioinformatics 10(), 2009
PMID: 20003500
Relaxed rrn expression and amino acid requirement of a Corynebacterium glutamicum rel mutant defective in (p)ppGpp metabolism.
Tauch A, Wehmeier L, Gotker S, Puhler A, Kalinowski J., FEMS Microbiol. Lett. 201(1), 2001
PMID: 11445167
Diversity in (p)ppGpp metabolism and effectors.
Liu K, Bittner AN, Wang JD., Curr. Opin. Microbiol. 24(), 2015
PMID: 25636134
The significance of EXDD and RXKD motif conservation in Rel proteins.
Sajish M, Kalayil S, Verma SK, Nandicoori VK, Prakash B., J. Biol. Chem. 284(14), 2009
PMID: 19201753
Structural basis for transcription regulation by alarmone ppGpp.
Artsimovitch I, Patlan V, Sekine S, Vassylyeva MN, Hosaka T, Ochi K, Yokoyama S, Vassylyev DG., Cell 117(3), 2004
PMID: 15109491
Catalytic mechanism and allosteric regulation of an oligomeric (p)ppGpp synthetase by an alarmone.
Steinchen W, Schuhmacher JS, Altegoer F, Fage CD, Srinivasan V, Linne U, Marahiel MA, Bange G., Proc. Natl. Acad. Sci. U.S.A. 112(43), 2015
PMID: 26460002
Mg2+, K+, and the ribosome.
Nierhaus KH., J. Bacteriol. 196(22), 2014
PMID: 25225274
Comparative analysis of the Corynebacterium glutamicum group and complete genome sequence of strain R.
Yukawa H, Omumasaba CA, Nonaka H, Kos P, Okai N, Suzuki N, Suda M, Tsuge Y, Watanabe J, Ikeda Y, Vertes AA, Inui M., Microbiology (Reading, Engl.) 153(Pt 4), 2007
PMID: 17379713

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 28871248
PubMed | Europe PMC

Suchen in

Google Scholar