Post-translational regulation of a developmental catalase, CatB, involves a metalloprotease, SmpA and contributes to proper differentiation and osmoprotection of Streptomyces coelicolor

Hyo Sub Kim, Eun-Jin Lee, You Hee Cho, Jung Hye Roe

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2 Citations (Scopus)

Abstract

Streptomyces coelicolor produces at least three different catalases (catalases A, B, and C) under different physiological conditions. Catalase B (CatB) is a developmentally regulated catalase required for proper differentiation and osmoprotection of S. coelicolor. We previously observed that the N-terminal 75. 22The 75 aa was once designated as 95 aa in our previous study (Cho et al., 2000), due to a mistaken duplication of 20 aa at the N-terminal region. amino acids (aa) of CatB are cleaved off, with the remaining 75-kDa processed CatB detectable in the extracellular fraction during sporulation. We here report that either the deletion of the N-terminal 75 aa or the arginine-to-alanine substitution (R75A) at the cleavage site, but not the histidine-to-alanine substitution (H131A) at the catalytic site, impaired both the secretion of CatB proteins and the proper differentiation of S. coelicolor cells. The proteolytic activity responsible for the cleavage of CatB was purified and then identified as a metalloprotease, which was named as SmpA (. Streptomyces metalloprotease A). The SmpA protein was newly detected after sporulation, coincident with the intracellular appearance of 75-kDa CatB, which was not detected in the smpA null mutant, confirming that SmpA indeed processes CatB in vivo. The smpA mutant was osmosensitive as catB mutant, but it displayed delayed sporulation, with the 75-kDa CatB still detectable in the extracellular milieu. Based on these results, we propose that the post-translational regulation of CatB, which cleaves the N-terminal 75 aa residues through SmpA is crucial for proper differentiation and osmoprotection of S. coelicolor. In the absence of SmpA, an alternative route for CatB processing may function to allow delayed sporulation.

Original languageEnglish
Pages (from-to)327-334
Number of pages8
JournalResearch in Microbiology
Volume164
Issue number4
DOIs
Publication statusPublished - 2013 May 1
Externally publishedYes

Fingerprint

Streptomyces coelicolor
Metalloproteases
Catalase
Amino Acids
Alanine
Streptomyces
Histidine

Keywords

  • Catalase
  • Differentiation
  • Metalloprotease
  • Osmotic stress
  • Processing
  • Streptomyces

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

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title = "Post-translational regulation of a developmental catalase, CatB, involves a metalloprotease, SmpA and contributes to proper differentiation and osmoprotection of Streptomyces coelicolor",
abstract = "Streptomyces coelicolor produces at least three different catalases (catalases A, B, and C) under different physiological conditions. Catalase B (CatB) is a developmentally regulated catalase required for proper differentiation and osmoprotection of S. coelicolor. We previously observed that the N-terminal 75. 22The 75 aa was once designated as 95 aa in our previous study (Cho et al., 2000), due to a mistaken duplication of 20 aa at the N-terminal region. amino acids (aa) of CatB are cleaved off, with the remaining 75-kDa processed CatB detectable in the extracellular fraction during sporulation. We here report that either the deletion of the N-terminal 75 aa or the arginine-to-alanine substitution (R75A) at the cleavage site, but not the histidine-to-alanine substitution (H131A) at the catalytic site, impaired both the secretion of CatB proteins and the proper differentiation of S. coelicolor cells. The proteolytic activity responsible for the cleavage of CatB was purified and then identified as a metalloprotease, which was named as SmpA (. Streptomyces metalloprotease A). The SmpA protein was newly detected after sporulation, coincident with the intracellular appearance of 75-kDa CatB, which was not detected in the smpA null mutant, confirming that SmpA indeed processes CatB in vivo. The smpA mutant was osmosensitive as catB mutant, but it displayed delayed sporulation, with the 75-kDa CatB still detectable in the extracellular milieu. Based on these results, we propose that the post-translational regulation of CatB, which cleaves the N-terminal 75 aa residues through SmpA is crucial for proper differentiation and osmoprotection of S. coelicolor. In the absence of SmpA, an alternative route for CatB processing may function to allow delayed sporulation.",
keywords = "Catalase, Differentiation, Metalloprotease, Osmotic stress, Processing, Streptomyces",
author = "Kim, {Hyo Sub} and Eun-Jin Lee and Cho, {You Hee} and Roe, {Jung Hye}",
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T1 - Post-translational regulation of a developmental catalase, CatB, involves a metalloprotease, SmpA and contributes to proper differentiation and osmoprotection of Streptomyces coelicolor

AU - Kim, Hyo Sub

AU - Lee, Eun-Jin

AU - Cho, You Hee

AU - Roe, Jung Hye

PY - 2013/5/1

Y1 - 2013/5/1

N2 - Streptomyces coelicolor produces at least three different catalases (catalases A, B, and C) under different physiological conditions. Catalase B (CatB) is a developmentally regulated catalase required for proper differentiation and osmoprotection of S. coelicolor. We previously observed that the N-terminal 75. 22The 75 aa was once designated as 95 aa in our previous study (Cho et al., 2000), due to a mistaken duplication of 20 aa at the N-terminal region. amino acids (aa) of CatB are cleaved off, with the remaining 75-kDa processed CatB detectable in the extracellular fraction during sporulation. We here report that either the deletion of the N-terminal 75 aa or the arginine-to-alanine substitution (R75A) at the cleavage site, but not the histidine-to-alanine substitution (H131A) at the catalytic site, impaired both the secretion of CatB proteins and the proper differentiation of S. coelicolor cells. The proteolytic activity responsible for the cleavage of CatB was purified and then identified as a metalloprotease, which was named as SmpA (. Streptomyces metalloprotease A). The SmpA protein was newly detected after sporulation, coincident with the intracellular appearance of 75-kDa CatB, which was not detected in the smpA null mutant, confirming that SmpA indeed processes CatB in vivo. The smpA mutant was osmosensitive as catB mutant, but it displayed delayed sporulation, with the 75-kDa CatB still detectable in the extracellular milieu. Based on these results, we propose that the post-translational regulation of CatB, which cleaves the N-terminal 75 aa residues through SmpA is crucial for proper differentiation and osmoprotection of S. coelicolor. In the absence of SmpA, an alternative route for CatB processing may function to allow delayed sporulation.

AB - Streptomyces coelicolor produces at least three different catalases (catalases A, B, and C) under different physiological conditions. Catalase B (CatB) is a developmentally regulated catalase required for proper differentiation and osmoprotection of S. coelicolor. We previously observed that the N-terminal 75. 22The 75 aa was once designated as 95 aa in our previous study (Cho et al., 2000), due to a mistaken duplication of 20 aa at the N-terminal region. amino acids (aa) of CatB are cleaved off, with the remaining 75-kDa processed CatB detectable in the extracellular fraction during sporulation. We here report that either the deletion of the N-terminal 75 aa or the arginine-to-alanine substitution (R75A) at the cleavage site, but not the histidine-to-alanine substitution (H131A) at the catalytic site, impaired both the secretion of CatB proteins and the proper differentiation of S. coelicolor cells. The proteolytic activity responsible for the cleavage of CatB was purified and then identified as a metalloprotease, which was named as SmpA (. Streptomyces metalloprotease A). The SmpA protein was newly detected after sporulation, coincident with the intracellular appearance of 75-kDa CatB, which was not detected in the smpA null mutant, confirming that SmpA indeed processes CatB in vivo. The smpA mutant was osmosensitive as catB mutant, but it displayed delayed sporulation, with the 75-kDa CatB still detectable in the extracellular milieu. Based on these results, we propose that the post-translational regulation of CatB, which cleaves the N-terminal 75 aa residues through SmpA is crucial for proper differentiation and osmoprotection of S. coelicolor. In the absence of SmpA, an alternative route for CatB processing may function to allow delayed sporulation.

KW - Catalase

KW - Differentiation

KW - Metalloprotease

KW - Osmotic stress

KW - Processing

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