Archaeal Signal Transduction: Impact of Protein Phosphatase Deletions on Cell Size, Motility, and Energy Metabolism in Sulfolobus acidocaldarius

• Published in: Molecular & cellular proteomics Vol. 12; no. 12; pp. 3908 - 3923
• Main Authors: Reimann, Julia, Esser, Dominik, Orell, Alvaro, Amman, Fabian, Pham, Trong Khoa, Noirel, Josselin, Lindås, Ann-Christin, Bernander, Rolf, Wright, Phillip C., Siebers, Bettina, Albers, Sonja-Verena
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.12.2013; The American Society for Biochemistry and Molecular Biology
• Subjects: 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
• ISSN: 1535-9476; 1535-9484; 1535-9484
• DOI: 10.1074/mcp.M113.027375

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.