Archaeal Signal Transduction: Impact of Protein Phosphatase Deletions on Cell Size, Motility, and Energy Metabolism in Sulfolobus acidocaldarius
In this study, the in vitro and in vivo functions of the only two identified protein phosphatases, Saci-PTP and Saci-PP2A, in the crenarchaeal model organism Sulfolobus acidocaldarius were investigated. Biochemical characterization revealed that Saci-PTP is a dual-specific phosphatase (against pSer/...
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Published in | Molecular & cellular proteomics Vol. 12; no. 12; pp. 3908 - 3923 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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01.12.2013
The American Society for Biochemistry and Molecular Biology |
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Abstract | In this study, the in vitro and in vivo functions of the only two identified protein phosphatases, Saci-PTP and Saci-PP2A, in the crenarchaeal model organism Sulfolobus acidocaldarius were investigated. Biochemical characterization revealed that Saci-PTP is a dual-specific phosphatase (against pSer/pThr and pTyr), whereas Saci-PP2A exhibited specific pSer/pThr activity and inhibition by okadaic acid. Deletion of saci_pp2a resulted in pronounced alterations in growth, cell shape and cell size, which could be partially complemented. Transcriptome analysis of the three strains (Δsaci_ptp, Δsaci_pp2a and the MW001 parental strain) revealed 155 genes that were differentially expressed in the deletion mutants, and showed significant changes in expression of genes encoding the archaella (archaeal motility structure), components of the respiratory chain and transcriptional regulators. Phosphoproteome studies revealed 801 unique phosphoproteins in total, with an increase in identified phosphopeptides in the deletion mutants. Proteins from most functional categories were affected by phosphorylation, including components of the motility system, the respiratory chain, and regulatory proteins. In the saci_pp2a deletion mutant the up-regulation at the transcript level, as well as the observed phosphorylation pattern, resembled starvation stress responses. Hypermotility was also observed in the saci_pp2a deletion mutant. The results highlight the importance of protein phosphorylation in regulating essential cellular processes in the crenarchaeon S. acidocaldarius. |
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AbstractList | In this study, the in vitro and in vivo functions of the only two identified protein phosphatases, Saci-PTP and Saci-PP2A, in the crenarchaeal model organism Sulfolobus acidocaldarius were investigated. Biochemical characterization revealed that Saci-PTP is a dual-specific phosphatase (against pSer/pThr and pTyr), whereas Saci-PP2A exhibited specific pSer/pThr activity and inhibition by okadaic acid. Deletion of saci_pp2a resulted in pronounced alterations in growth, cell shape and cell size, which could be partially complemented. Transcriptome analysis of the three strains (Δ saci_ptp , Δ saci_pp2a and the MW001 parental strain) revealed 155 genes that were differentially expressed in the deletion mutants, and showed significant changes in expression of genes encoding the archaella (archaeal motility structure), components of the respiratory chain and transcriptional regulators. Phosphoproteome studies revealed 801 unique phosphoproteins in total, with an increase in identified phosphopeptides in the deletion mutants. Proteins from most functional categories were affected by phosphorylation, including components of the motility system, the respiratory chain, and regulatory proteins. In the saci_pp2a deletion mutant the up-regulation at the transcript level, as well as the observed phosphorylation pattern, resembled starvation stress responses. Hypermotility was also observed in the saci_pp2a deletion mutant. The results highlight the importance of protein phosphorylation in regulating essential cellular processes in the crenarchaeon S. acidocaldarius . In this study, the in vitro and in vivo functions of the only two identified protein phosphatases, Saci-PTP and Saci-PP2A, in the crenarchaeal model organism Sulfolobus acidocaldarius were investigated. Biochemical characterization revealed that Saci-PTP is a dual-specific phosphatase (against pSer/pThr and pTyr), whereas Saci-PP2A exhibited specific pSer/pThr activity and inhibition by okadaic acid. Deletion of saci_pp2a resulted in pronounced alterations in growth, cell shape and cell size, which could be partially complemented. Transcriptome analysis of the three strains (Δsaci_ptp, Δsaci_pp2a and the MW001 parental strain) revealed 155 genes that were differentially expressed in the deletion mutants, and showed significant changes in expression of genes encoding the archaella (archaeal motility structure), components of the respiratory chain and transcriptional regulators. Phosphoproteome studies revealed 801 unique phosphoproteins in total, with an increase in identified phosphopeptides in the deletion mutants. Proteins from most functional categories were affected by phosphorylation, including components of the motility system, the respiratory chain, and regulatory proteins. In the saci_pp2a deletion mutant the up-regulation at the transcript level, as well as the observed phosphorylation pattern, resembled starvation stress responses. Hypermotility was also observed in the saci_pp2a deletion mutant. The results highlight the importance of protein phosphorylation in regulating essential cellular processes in the crenarchaeon S. acidocaldarius. In this study, the in vitro and in vivo functions of the only two identified protein phosphatases, Saci-PTP and Saci-PP2A, in the crenarchaeal model organism Sulfolobus acidocaldarius were investigated. Biochemical characterization revealed that Saci-PTP is a dual-specific phosphatase (against pSer/pThr and pTyr), whereas Saci-PP2A exhibited specific pSer/pThr activity and inhibition by okadaic acid. Deletion of saci_pp2a resulted in pronounced alterations in growth, cell shape and cell size, which could be partially complemented. Transcriptome analysis of the three strains (Δ saci_ptp , Δ saci_pp2a and the MW001 parental strain) revealed 155 genes that were differentially expressed in the deletion mutants, and showed significant changes in expression of genes encoding the archaella (archaeal motility structure), components of the respiratory chain and transcriptional regulators. Phosphoproteome studies revealed 801 unique phosphoproteins in total, with an increase in identified phosphopeptides in the deletion mutants. Proteins from most functional categories were affected by phosphorylation, including components of the motility system, the respiratory chain, and regulatory proteins. In the saci_pp2a deletion mutant the up-regulation at the transcript level, as well as the observed phosphorylation pattern, resembled starvation stress responses. Hypermotility was also observed in the saci_pp2a deletion mutant. The results highlight the importance of protein phosphorylation in regulating essential cellular processes in the crenarchaeon S. acidocaldarius . |
Author | Wright, Phillip C. Lindås, Ann-Christin Amman, Fabian Noirel, Josselin Siebers, Bettina Reimann, Julia Orell, Alvaro Esser, Dominik Pham, Trong Khoa Bernander, Rolf Albers, Sonja-Verena |
Author_xml | – sequence: 1 givenname: Julia surname: Reimann fullname: Reimann, Julia organization: Molecular Biology of Archaea, Max Planck Institute for terrestrial Microbiology, Karl-von-Frisch Straβe 10, 35043 Marburg, Germany – sequence: 2 givenname: Dominik surname: Esser fullname: Esser, Dominik organization: Molecular Enzyme Technology and Biochemistry, Biofilm Centre, Faculty of Chemistry, University of Duisburg-Essen, Universitätsstrasse 5, D-45141 Essen, Germany – sequence: 3 givenname: Alvaro surname: Orell fullname: Orell, Alvaro organization: Molecular Biology of Archaea, Max Planck Institute for terrestrial Microbiology, Karl-von-Frisch Straβe 10, 35043 Marburg, Germany – sequence: 4 givenname: Fabian surname: Amman fullname: Amman, Fabian organization: Institute for Theoretical Chemistry, University of Vienna, Währingerstrasse 17, A-1090 Vienna, Austria – sequence: 5 givenname: Trong Khoa surname: Pham fullname: Pham, Trong Khoa organization: ChELSI Institute, Department of Chemical and Biological Engineering, The University of Sheffield, Mappin Street, Sheffield, S1 3JD, United Kingdom – sequence: 6 givenname: Josselin surname: Noirel fullname: Noirel, Josselin organization: ChELSI Institute, Department of Chemical and Biological Engineering, The University of Sheffield, Mappin Street, Sheffield, S1 3JD, United Kingdom – sequence: 7 givenname: Ann-Christin surname: Lindås fullname: Lindås, Ann-Christin organization: Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Svante Arrhenius väg 20C, SE-106 91, Stockholm, Sweden – sequence: 8 givenname: Rolf surname: Bernander fullname: Bernander, Rolf organization: Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Svante Arrhenius väg 20C, SE-106 91, Stockholm, Sweden – sequence: 9 givenname: Phillip C. surname: Wright fullname: Wright, Phillip C. organization: ChELSI Institute, Department of Chemical and Biological Engineering, The University of Sheffield, Mappin Street, Sheffield, S1 3JD, United Kingdom – sequence: 10 givenname: Bettina surname: Siebers fullname: Siebers, Bettina organization: Molecular Enzyme Technology and Biochemistry, Biofilm Centre, Faculty of Chemistry, University of Duisburg-Essen, Universitätsstrasse 5, D-45141 Essen, Germany – sequence: 11 givenname: Sonja-Verena surname: Albers fullname: Albers, Sonja-Verena email: albers@mpi-marburg.mpg.de organization: Molecular Biology of Archaea, Max Planck Institute for terrestrial Microbiology, Karl-von-Frisch Straβe 10, 35043 Marburg, Germany |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24078887$$D View this record in MEDLINE/PubMed https://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-101496$$DView record from Swedish Publication Index |
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Snippet | In this study, the in vitro and in vivo functions of the only two identified protein phosphatases, Saci-PTP and Saci-PP2A, in the crenarchaeal model organism... In this study, the in vitro and in vivo functions of the only two identified protein phosphatases, Saci-PTP and Saci-PP2A, in the crenarchaeal model organism... |
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SubjectTerms | Archaeal Proteins - genetics Archaeal Proteins - metabolism Electron Transport - genetics Energy Metabolism - genetics Gene Deletion Gene Expression Profiling Gene Expression Regulation, Archaeal Isoenzymes - genetics Isoenzymes - metabolism Kinetics Molecular Sequence Annotation Movement Phosphoproteins - genetics Phosphoproteins - metabolism Phosphorylation Protein Phosphatase 2 - genetics Protein Phosphatase 2 - metabolism Signal Transduction - genetics Sulfolobus acidocaldarius - enzymology Sulfolobus acidocaldarius - genetics Sulfolobus acidocaldarius - ultrastructure Transcriptome |
Title | Archaeal Signal Transduction: Impact of Protein Phosphatase Deletions on Cell Size, Motility, and Energy Metabolism in Sulfolobus acidocaldarius |
URI | https://dx.doi.org/10.1074/mcp.M113.027375 https://www.ncbi.nlm.nih.gov/pubmed/24078887 https://pubmed.ncbi.nlm.nih.gov/PMC3861733 https://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-101496 |
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