Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis

H.-L. Hyyryläinen, B. C. Marciniak, K. Dahncke, M. Pietiäinen, P. Courtin, Marika Vitikainen, R. Seppälä, A. Otto, D. Becher, M.-P. Chapot-Chartier, O. P. Kuipers, V. P. Kontinen (Corresponding Author)

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Abstract

The PrsA protein is a membrane‐anchored peptidyl‐prolyl cis‐trans isomerase in Bacillus subtilis and most other Gram‐positive bacteria. It catalyses the post‐translocational folding of exported proteins and is essential for normal growth of B. subtilis. We studied the mechanism behind this indispensability. We could construct a viable prsA null mutant in the presence of a high concentration of magnesium. Various changes in cell morphology in the absence of PrsA suggested that PrsA is involved in the biosynthesis of the cylindrical lateral wall. Consistently, four penicillin‐binding proteins (PBP2a, PBP2b, PBP3 and PBP4) were unstable in the absence of PrsA, while muropeptide analysis revealed a 2% decrease in the peptidoglycan cross‐linkage index. Misfolded PBP2a was detected in PrsA‐depleted cells, indicating that PrsA is required for the folding of this PBP either directly or indirectly. Furthermore, strongly increased uniform staining of cell wall with a fluorescent vancomycin was observed in the absence of PrsA. We also demonstrated that PrsA is a dimeric or oligomeric protein which is localized at distinct spots organized in a helical pattern along the cell membrane. These results suggest that PrsA is essential for normal growth most probably as PBP folding is dependent on this PPIase.
Original languageEnglish
Pages (from-to)108-127
Number of pages10
JournalMolecular Microbiology
Volume77
Issue number1
DOIs
Publication statusPublished - 2010
MoE publication typeA1 Journal article-refereed

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Peptidylprolyl Isomerase
Penicillin-Binding Proteins
Protein Folding
Bacillus subtilis
Proteins
Peptidoglycan
Vancomycin
Growth
Cell Wall
Magnesium
Cell Membrane
Staining and Labeling
Bacteria

Cite this

Hyyryläinen, H.-L. ; Marciniak, B. C. ; Dahncke, K. ; Pietiäinen, M. ; Courtin, P. ; Vitikainen, Marika ; Seppälä, R. ; Otto, A. ; Becher, D. ; Chapot-Chartier, M.-P. ; Kuipers, O. P. ; Kontinen, V. P. / Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis. In: Molecular Microbiology. 2010 ; Vol. 77, No. 1. pp. 108-127.
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title = "Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis",
abstract = "The PrsA protein is a membrane‐anchored peptidyl‐prolyl cis‐trans isomerase in Bacillus subtilis and most other Gram‐positive bacteria. It catalyses the post‐translocational folding of exported proteins and is essential for normal growth of B. subtilis. We studied the mechanism behind this indispensability. We could construct a viable prsA null mutant in the presence of a high concentration of magnesium. Various changes in cell morphology in the absence of PrsA suggested that PrsA is involved in the biosynthesis of the cylindrical lateral wall. Consistently, four penicillin‐binding proteins (PBP2a, PBP2b, PBP3 and PBP4) were unstable in the absence of PrsA, while muropeptide analysis revealed a 2{\%} decrease in the peptidoglycan cross‐linkage index. Misfolded PBP2a was detected in PrsA‐depleted cells, indicating that PrsA is required for the folding of this PBP either directly or indirectly. Furthermore, strongly increased uniform staining of cell wall with a fluorescent vancomycin was observed in the absence of PrsA. We also demonstrated that PrsA is a dimeric or oligomeric protein which is localized at distinct spots organized in a helical pattern along the cell membrane. These results suggest that PrsA is essential for normal growth most probably as PBP folding is dependent on this PPIase.",
author = "H.-L. Hyyryl{\"a}inen and Marciniak, {B. C.} and K. Dahncke and M. Pieti{\"a}inen and P. Courtin and Marika Vitikainen and R. Sepp{\"a}l{\"a} and A. Otto and D. Becher and M.-P. Chapot-Chartier and Kuipers, {O. P.} and Kontinen, {V. P.}",
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doi = "10.1111/j.1365-2958.2010.07188.x",
language = "English",
volume = "77",
pages = "108--127",
journal = "Molecular Microbiology",
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Hyyryläinen, H-L, Marciniak, BC, Dahncke, K, Pietiäinen, M, Courtin, P, Vitikainen, M, Seppälä, R, Otto, A, Becher, D, Chapot-Chartier, M-P, Kuipers, OP & Kontinen, VP 2010, 'Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis', Molecular Microbiology, vol. 77, no. 1, pp. 108-127. https://doi.org/10.1111/j.1365-2958.2010.07188.x

Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis. / Hyyryläinen, H.-L.; Marciniak, B. C.; Dahncke, K.; Pietiäinen, M.; Courtin, P.; Vitikainen, Marika; Seppälä, R.; Otto, A.; Becher, D.; Chapot-Chartier, M.-P.; Kuipers, O. P.; Kontinen, V. P. (Corresponding Author).

In: Molecular Microbiology, Vol. 77, No. 1, 2010, p. 108-127.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Penicillin-binding protein folding is dependent on the PrsA peptidyl-prolyl cis-trans isomerase in Bacillus subtilis

AU - Hyyryläinen, H.-L.

AU - Marciniak, B. C.

AU - Dahncke, K.

AU - Pietiäinen, M.

AU - Courtin, P.

AU - Vitikainen, Marika

AU - Seppälä, R.

AU - Otto, A.

AU - Becher, D.

AU - Chapot-Chartier, M.-P.

AU - Kuipers, O. P.

AU - Kontinen, V. P.

PY - 2010

Y1 - 2010

N2 - The PrsA protein is a membrane‐anchored peptidyl‐prolyl cis‐trans isomerase in Bacillus subtilis and most other Gram‐positive bacteria. It catalyses the post‐translocational folding of exported proteins and is essential for normal growth of B. subtilis. We studied the mechanism behind this indispensability. We could construct a viable prsA null mutant in the presence of a high concentration of magnesium. Various changes in cell morphology in the absence of PrsA suggested that PrsA is involved in the biosynthesis of the cylindrical lateral wall. Consistently, four penicillin‐binding proteins (PBP2a, PBP2b, PBP3 and PBP4) were unstable in the absence of PrsA, while muropeptide analysis revealed a 2% decrease in the peptidoglycan cross‐linkage index. Misfolded PBP2a was detected in PrsA‐depleted cells, indicating that PrsA is required for the folding of this PBP either directly or indirectly. Furthermore, strongly increased uniform staining of cell wall with a fluorescent vancomycin was observed in the absence of PrsA. We also demonstrated that PrsA is a dimeric or oligomeric protein which is localized at distinct spots organized in a helical pattern along the cell membrane. These results suggest that PrsA is essential for normal growth most probably as PBP folding is dependent on this PPIase.

AB - The PrsA protein is a membrane‐anchored peptidyl‐prolyl cis‐trans isomerase in Bacillus subtilis and most other Gram‐positive bacteria. It catalyses the post‐translocational folding of exported proteins and is essential for normal growth of B. subtilis. We studied the mechanism behind this indispensability. We could construct a viable prsA null mutant in the presence of a high concentration of magnesium. Various changes in cell morphology in the absence of PrsA suggested that PrsA is involved in the biosynthesis of the cylindrical lateral wall. Consistently, four penicillin‐binding proteins (PBP2a, PBP2b, PBP3 and PBP4) were unstable in the absence of PrsA, while muropeptide analysis revealed a 2% decrease in the peptidoglycan cross‐linkage index. Misfolded PBP2a was detected in PrsA‐depleted cells, indicating that PrsA is required for the folding of this PBP either directly or indirectly. Furthermore, strongly increased uniform staining of cell wall with a fluorescent vancomycin was observed in the absence of PrsA. We also demonstrated that PrsA is a dimeric or oligomeric protein which is localized at distinct spots organized in a helical pattern along the cell membrane. These results suggest that PrsA is essential for normal growth most probably as PBP folding is dependent on this PPIase.

U2 - 10.1111/j.1365-2958.2010.07188.x

DO - 10.1111/j.1365-2958.2010.07188.x

M3 - Article

VL - 77

SP - 108

EP - 127

JO - Molecular Microbiology

JF - Molecular Microbiology

SN - 0950-382X

IS - 1

ER -