Synthesis, Release, and Recapture of Compatible Solute Proline by Osmotically Stressed Bacillus subtilis Cells

Hoffmann T, von Blohn C, Stanek A, Moses S, Barzantny H, Bremer E (2012)
Applied and environmental microbiology 78(16): 5753-5762.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Hoffmann, Tamara; von Blohn, Carsten; Stanek, Agnieszka; Moses, Susanne; Barzantny, HelenaUniBi; Bremer, Erhard
Abstract / Bemerkung
Bacillus subtilis synthesizes large amounts of the compatible solute proline as a cellular defense against high osmolarity to ensure a physiologically appropriate level of hydration of the cytoplasm and turgor. It also imports proline for this purpose via the osmotically inducible OpuE transport system. Unexpectedly, an opuE mutant was at a strong growth disadvantage in high-salinity minimal media lacking proline. Appreciable amounts of proline were detected in the culture supernatant of the opuE mutant strain, and they rose concomitantly with increases in the external salinity. We found that the intracellular proline pool of severely salinity-stressed cells of the opuE mutant was considerably lower than that of its opuE(+) parent strain. This loss of proline into the medium and the resulting decrease in the intracellular proline content provide a rational explanation for the observed salt-sensitive growth phenotype of cells lacking OpuE. None of the known MscL- and MscS-type mechanosensitive channels of B. subtilis participated in the release of proline under permanently imposed high-salinity growth conditions. The data reported here show that the OpuE transporter not only possesses the previously reported role for the scavenging of exogenously provided proline as an osmoprotectant but also functions as a physiologically highly important recapturing device for proline that is synthesized de novo and subsequently released by salt-stressed B. subtilis cells. The wider implications of our findings for the retention of compatible solutes by osmotically challenged microorganisms and the roles of uptake systems for compatible solutes are considered.
Erscheinungsjahr
2012
Zeitschriftentitel
Applied and environmental microbiology
Band
78
Ausgabe
16
Seite(n)
5753-5762
ISSN
0099-2240
Page URI
https://pub.uni-bielefeld.de/record/2518279

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Hoffmann T, von Blohn C, Stanek A, Moses S, Barzantny H, Bremer E. Synthesis, Release, and Recapture of Compatible Solute Proline by Osmotically Stressed Bacillus subtilis Cells. Applied and environmental microbiology. 2012;78(16):5753-5762.
Hoffmann, T., von Blohn, C., Stanek, A., Moses, S., Barzantny, H., & Bremer, E. (2012). Synthesis, Release, and Recapture of Compatible Solute Proline by Osmotically Stressed Bacillus subtilis Cells. Applied and environmental microbiology, 78(16), 5753-5762. doi:10.1128/AEM.01040-12
Hoffmann, T., von Blohn, C., Stanek, A., Moses, S., Barzantny, H., and Bremer, E. (2012). Synthesis, Release, and Recapture of Compatible Solute Proline by Osmotically Stressed Bacillus subtilis Cells. Applied and environmental microbiology 78, 5753-5762.
Hoffmann, T., et al., 2012. Synthesis, Release, and Recapture of Compatible Solute Proline by Osmotically Stressed Bacillus subtilis Cells. Applied and environmental microbiology, 78(16), p 5753-5762.
T. Hoffmann, et al., “Synthesis, Release, and Recapture of Compatible Solute Proline by Osmotically Stressed Bacillus subtilis Cells”, Applied and environmental microbiology, vol. 78, 2012, pp. 5753-5762.
Hoffmann, T., von Blohn, C., Stanek, A., Moses, S., Barzantny, H., Bremer, E.: Synthesis, Release, and Recapture of Compatible Solute Proline by Osmotically Stressed Bacillus subtilis Cells. Applied and environmental microbiology. 78, 5753-5762 (2012).
Hoffmann, Tamara, von Blohn, Carsten, Stanek, Agnieszka, Moses, Susanne, Barzantny, Helena, and Bremer, Erhard. “Synthesis, Release, and Recapture of Compatible Solute Proline by Osmotically Stressed Bacillus subtilis Cells”. Applied and environmental microbiology 78.16 (2012): 5753-5762.

26 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Role of the Extremolytes Ectoine and Hydroxyectoine as Stress Protectants and Nutrients: Genetics, Phylogenomics, Biochemistry, and Structural Analysis.
Czech L, Hermann L, Stöveken N, Richter AA, Höppner A, Smits SHJ, Heider J, Bremer E., Genes (Basel) 9(4), 2018
PMID: 29565833
The complete genome sequence of Rhodobaca barguzinensis alga05 (DSM 19920) documents its adaptation for life in soda lakes.
Kopejtka K, Tomasch J, Bunk B, Spröer C, Wagner-Döbler I, Koblížek M., Extremophiles 22(6), 2018
PMID: 30022245
The GbsR Family of Transcriptional Regulators: Functional Characterization of the OpuAR Repressor.
Ronzheimer S, Warmbold B, Arnhold C, Bremer E., Front Microbiol 9(), 2018
PMID: 30405586
From substrate specificity to promiscuity: hybrid ABC transporters for osmoprotectants.
Teichmann L, Chen C, Hoffmann T, Smits SHJ, Schmitt L, Bremer E., Mol Microbiol 104(5), 2017
PMID: 28256787
The significance of proline and glutamate on butanol chaotropic stress in Bacillus subtilis 168.
Mahipant G, Paemanee A, Roytrakul S, Kato J, Vangnai AS., Biotechnol Biofuels 10(), 2017
PMID: 28503197
Functional Characterization of Four Putative δ1-Pyrroline-5-Carboxylate Reductases from Bacillus subtilis.
Forlani G, Nocek B, Chakravarthy S, Joachimiak A., Front Microbiol 8(), 2017
PMID: 28824574
Synthesis of the compatible solute proline by Bacillus subtilis: point mutations rendering the osmotically controlled proHJ promoter hyperactive.
Hoffmann T, Bleisteiner M, Sappa PK, Steil L, Mäder U, Völker U, Bremer E., Environ Microbiol 19(9), 2017
PMID: 28752945
Biocontrol agents promote growth of potato pathogens, depending on environmental conditions.
Cray JA, Connor MC, Stevenson A, Houghton JD, Rangel DE, Cooke LR, Hallsworth JE., Microb Biotechnol 9(3), 2016
PMID: 26880001
Uptake of amino acids and their metabolic conversion into the compatible solute proline confers osmoprotection to Bacillus subtilis.
Zaprasis A, Bleisteiner M, Kerres A, Hoffmann T, Bremer E., Appl Environ Microbiol 81(1), 2015
PMID: 25344233
Evolution of proline biosynthesis: enzymology, bioinformatics, genetics, and transcriptional regulation.
Fichman Y, Gerdes SY, Kovács H, Szabados L, Zilberstein A, Csonka LN., Biol Rev Camb Philos Soc 90(4), 2015
PMID: 25367752
Mutational activation of the RocR activator and of a cryptic rocDEF promoter bypass loss of the initial steps of proline biosynthesis in Bacillus subtilis.
Zaprasis A, Hoffmann T, Wünsche G, Flórez LA, Stülke J, Bremer E., Environ Microbiol 16(3), 2014
PMID: 23869754
The γ-aminobutyrate permease GabP serves as the third proline transporter of Bacillus subtilis.
Zaprasis A, Hoffmann T, Stannek L, Gunka K, Commichau FM, Bremer E., J Bacteriol 196(3), 2014
PMID: 24142252
Dimethylglycine provides salt and temperature stress protection to Bacillus subtilis.
Bashir A, Hoffmann T, Smits SH, Bremer E., Appl Environ Microbiol 80(9), 2014
PMID: 24561588
Small cationic antimicrobial peptides delocalize peripheral membrane proteins.
Wenzel M, Chiriac AI, Otto A, Zweytick D, May C, Schumacher C, Gust R, Albada HB, Penkova M, Krämer U, Erdmann R, Metzler-Nolte N, Straus SK, Bremer E, Becher D, Brötz-Oesterhelt H, Sahl HG, Bandow JE., Proc Natl Acad Sci U S A 111(14), 2014
PMID: 24706874
Adaptation of Bacillus subtilis carbon core metabolism to simultaneous nutrient limitation and osmotic challenge: a multi-omics perspective.
Kohlstedt M, Sappa PK, Meyer H, Maaß S, Zaprasis A, Hoffmann T, Becker J, Steil L, Hecker M, van Dijl JM, Lalk M, Mäder U, Stülke J, Bremer E, Völker U, Wittmann C., Environ Microbiol 16(6), 2014
PMID: 24571712
Microbial diversity and biogeochemical cycling in soda lakes.
Sorokin DY, Berben T, Melton ED, Overmars L, Vavourakis CD, Muyzer G., Extremophiles 18(5), 2014
PMID: 25156418
Osmoprotection of Bacillus subtilis through import and proteolysis of proline-containing peptides.
Zaprasis A, Brill J, Thüring M, Wünsche G, Heun M, Barzantny H, Hoffmann T, Bremer E., Appl Environ Microbiol 79(2), 2013
PMID: 23144141
Osmotic control of opuA expression in Bacillus subtilis and its modulation in response to intracellular glycine betaine and proline pools.
Hoffmann T, Wensing A, Brosius M, Steil L, Völker U, Bremer E., J Bacteriol 195(3), 2013
PMID: 23175650
Systems metabolic engineering of Corynebacterium glutamicum for production of the chemical chaperone ectoine.
Becker J, Schäfer R, Kohlstedt M, Harder BJ, Borchert NS, Stöveken N, Bremer E, Wittmann C., Microb Cell Fact 12(), 2013
PMID: 24228689

64 References

Daten bereitgestellt von Europe PubMed Central.

Ion channels from the Bacillus subtilis plasma membrane incorporated into planar lipid bilayers.
Alcayaga C, Venegas R, Carrasco A, Wolff D., FEBS Lett. 311(3), 1992
PMID: 1383039
Rapid determination of free proline for water-stress studies
Bates LS, Waldren RP, Teare ID., 1973
Multiple genes for the last step of proline biosynthesis in Bacillus subtilis.
Belitsky BR, Brill J, Bremer E, Sonenshein AL., J. Bacteriol. 183(14), 2001
PMID: 11418582
Mechanosensitive channels in bacteria: signs of closure?
Booth IR, Edwards MD, Black S, Schumann U, Miller S., Nat. Rev. Microbiol. 5(6), 2007
PMID: 17505523
The properties and contribution of the Corynebacterium glutamicum MscS variant to fine-tuning of osmotic adaptation.
Borngen K, Battle AR, Moker N, Morbach S, Marin K, Martinac B, Kramer R., Biochim. Biophys. Acta 1798(11), 2010
PMID: 20599688
Adaptation to changing osmolarity
Bremer E., 2002
Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solutes
Bremer E, Krämer R., 2000
T-box-mediated control of the anabolic proline biosynthetic genes of Bacillus subtilis.
Brill J, Hoffmann T, Putzer H, Bremer E., Microbiology (Reading, Engl.) 157(Pt 4), 2011
PMID: 21233158
Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism.
Buescher JM, Liebermeister W, Jules M, Uhr M, Muntel J, Botella E, Hessling B, Kleijn RJ, Le Chat L, Lecointe F, Mader U, Nicolas P, Piersma S, Rugheimer F, Becher D, Bessieres P, Bidnenko E, Denham EL, Dervyn E, Devine KM, Doherty G, Drulhe S, Felicori L, Fogg MJ, Goelzer A, Hansen A, Harwood CR, Hecker M, Hubner S, Hultschig C, Jarmer H, Klipp E, Leduc A, Lewis P, Molina F, Noirot P, Peres S, Pigeonneau N, Pohl S, Rasmussen S, Rinn B, Schaffer M, Schnidder J, Schwikowski B, Van Dijl JM, Veiga P, Walsh S, Wilkinson AJ, Stelling J, Aymerich S, Sauer U., Science 335(6072), 2012
PMID: 22383848
Engineering trehalose synthesis in Lactococcus lactis for improved stress tolerance.
Carvalho AL, Cardoso FS, Bohn A, Neves AR, Santos H., Appl. Environ. Microbiol. 77(12), 2011
PMID: 21515730
Physiological and genetic responses of bacteria to osmotic stress.
Csonka LN., Microbiol. Rev. 53(1), 1989
PMID: 2651863
Glycine betaine fluxes in Lactobacillus plantarum during osmostasis and hyper- and hypo-osmotic shock.
Glaasker E, Konings WN, Poolman B., J. Biol. Chem. 271(17), 1996
PMID: 8626562
Plasmids for ectopic integration in Bacillus subtilis.
Guerout-Fleury AM, Frandsen N, Stragier P., Gene 180(1-2), 1996
PMID: 8973347
A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation.
Hahne H, Mader U, Otto A, Bonn F, Steil L, Bremer E, Hecker M, Becher D., J. Bacteriol. 192(3), 2009
PMID: 19948795
Growth, maintenance and general techniques
Harwood CR, Archibald AR., 1990
Mechanosensitive channels: what can they do and how do they do it?
Haswell ES, Phillips R, Rees DC., Structure 19(10), 2011
PMID: 22000509
KtrAB and KtrCD: two K+ uptake systems in Bacillus subtilis and their role in adaptation to hypertonicity.
Holtmann G, Bakker EP, Uozumi N, Bremer E., J. Bacteriol. 185(4), 2003
PMID: 12562800
Osmoprotection of Escherichia coli by ectoine: uptake and accumulation characteristics.
Jebbar M, Talibart R, Gloux K, Bernard T, Blanco C., J. Bacteriol. 174(15), 1992
PMID: 1629159
The Na⁺/L-proline transporter PutP.
Jung H, Hilger D, Raba M., Front Biosci (Landmark Ed) 17(), 2012
PMID: 22201772
Role for glycine betaine transport in Vibrio cholerae osmoadaptation and biofilm formation within microbial communities.
Kapfhammer D, Karatan E, Pflughoeft KJ, Watnick PI., Appl. Environ. Microbiol. 71(7), 2005
PMID: 16000796
The surface stress theory of microbial morphogenesis.
Koch AL., Adv. Microb. Physiol. 24(), 1983
PMID: 6364728
Efflux of choline and glycine betaine from osmoregulating cells of Escherichia coli.
Lamark T, Styrvold OB, Strom AR., FEMS Microbiol. Lett. 75(2-3), 1992
PMID: 1398030
A short course in bacterial genetics: a laboratory manual and handbook for and related bacteria
Miller JH., 1992
Proline utilization by Bacillus subtilis: uptake and catabolism.
Moses S, Sinner T, Zaprasis A, Stoveken N, Hoffmann T, Belitsky BR, Sonenshein AL, Bremer E., J. Bacteriol. 194(4), 2011
PMID: 22139509
Defining the structure of the general stress regulon of Bacillus subtilis using targeted microarray analysis and random forest classification.
Nannapaneni P, Hertwig F, Depke M, Hecker M, Mader U, Volker U, Steil L, van Hijum SA., Microbiology (Reading, Engl.) 158(Pt 3), 2011
PMID: 22174379
Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis.
Nicolas P, Mader U, Dervyn E, Rochat T, Leduc A, Pigeonneau N, Bidnenko E, Marchadier E, Hoebeke M, Aymerich S, Becher D, Bisicchia P, Botella E, Delumeau O, Doherty G, Denham EL, Fogg MJ, Fromion V, Goelzer A, Hansen A, Hartig E, Harwood CR, Homuth G, Jarmer H, Jules M, Klipp E, Le Chat L, Lecointe F, Lewis P, Liebermeister W, March A, Mars RA, Nannapaneni P, Noone D, Pohl S, Rinn B, Rugheimer F, Sappa PK, Samson F, Schaffer M, Schwikowski B, Steil L, Stulke J, Wiegert T, Devine KM, Wilkinson AJ, van Dijl JM, Hecker M, Volker U, Bessieres P, Noirot P., Science 335(6072), 2012
PMID: 22383849
Actinopolyspora halophila has two separate pathways for betaine synthesis.
Nyyssola A, Leisola M., Arch. Microbiol. 176(4), 2001
PMID: 11685374
Proline excretion by Escherichia coli K12.
Rancourt DE, Stephenson JT, Vickell GA, Wood JM., Biotechnol. Bioeng. 26(1), 1984
PMID: 18551589
Continuous synthesis and excretion of the compatible solute ectoine by a transgenic, nonhalophilic bacterium.
Schubert T, Maskow T, Benndorf D, Harms H, Breuer U., Appl. Environ. Microbiol. 73(10), 2007
PMID: 17369334
Escherichia coli physiology in Luria-Bertani broth.
Sezonov G, Joseleau-Petit D, D'Ari R., J. Bacteriol. 189(23), 2007
PMID: 17905994
High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies.
Srivatsan A, Han Y, Peng J, Tehranchi AK, Gibbs R, Wang JD, Chen R., PLoS Genet. 4(8), 2008
PMID: 18670626
Genome-wide transcriptional profiling analysis of adaptation of Bacillus subtilis to high salinity.
Steil L, Hoffmann T, Budde I, Volker U, Bremer E., J. Bacteriol. 185(21), 2003
PMID: 14563871
A patch-clamp study of Bacillus subtilis.
Szabo I, Petronilli V, Zoratti M., Biochim. Biophys. Acta 1112(1), 1992
PMID: 1384708
Characterization of methionine export in Corynebacterium glutamicum.
Trotschel C, Deutenberg D, Bathe B, Burkovski A, Kramer R., J. Bacteriol. 187(11), 2005
PMID: 15901702
Architecture of peptidoglycan: more data and more models.
Vollmer W, Seligman SJ., Trends Microbiol. 18(2), 2010
PMID: 20060721
Levels and localization of mechanosensitive channel proteins in Bacillus subtilis.
Wahome PG, Cowan AE, Setlow B, Setlow P., Arch. Microbiol. 191(5), 2009
PMID: 19252899
The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis.
Whatmore AM, Chudek JA, Reed RH., J. Gen. Microbiol. 136(12), 1990
PMID: 2127802
Osmosensing by bacteria: signals and membrane-based sensors.
Wood JM., Microbiol. Mol. Biol. Rev. 63(1), 1999
PMID: 10066837
Osmosensing and osmoregulatory compatible solute accumulation by bacteria.
Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, van der Heide T, Smith LT., Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 130(3), 2001
PMID: 11913457

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