Identification of a system required for the functional surface localization of sugar binding proteins with class III signal peptides in Sulfolobus solfataricus.
The hyperthermophilic archaeon Sulfolobus solfataricus contains an unusual large number of sugar binding proteins that are synthesized as precursors with a class III signal peptide. Such signal peptides are commonly used to direct archaeal flagellin subunits or bacterial (pseudo)pilins into extracellular macromolecular surface appendages. Likewise, S. solfataricus binding proteins have been suggested to assemble in higher ordered surface structures as well, tentatively termed the bindosome. Here we show that S. solfataricus contains a specific system that is needed for the functional surface localization of sugar binding proteins. This system, encoded by the bas (bindosome assembly system) operon, is composed of five proteins: basABC, three homologues of so-called bacterial (pseudo)pilins; BasE, a cytoplasmic ATPase; and BasF, an integral membrane protein. Deletion of either the three (pseudo)pilin genes or the basEF genes resulted in a severe defect of the cells to grow on substrates which are transported by sugar binding proteins containing class III signal peptides, while growth on glucose and maltose was restored when the corresponding genes were reintroduced in these cells. Concomitantly, DeltabasABC and DeltabasEF cells were severely impaired in glucose uptake even though the sugar binding proteins were normally secreted across the cytoplasmic membrane. These data underline the hypothesis that the bas operon is involved in the functional localization of sugar binding proteins at the cell surface of S. solfataricus. In contrast to surface structure assembly systems of Gram-negative bacteria, the bas operon seems to resemble an ancestral simplified form of these machineries.
Zolghadr
Behnam
B
Department of Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute and the Materials Science Centre Plus, University of Groningen, Kerklaan 30, 9751 NN HAREN, The Netherlands.
Weber
Stefan
S
Szabó
Zalán
Z
Driessen
Arnold J M
AJ
Albers
Sonja-Verena
SV
D018528:ATP-Binding Cassette Transporters / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D001089:Arabinose / Q000378:metabolism / Q000493:pharmacokinetics; D015139:Blotting, Southern; D015153:Blotting, Western; D002241:Carbohydrates / Q000493:pharmacokinetics; D002250:Carbon Radioisotopes; D002352:Carrier Proteins / Q000235:genetics / Q000378:metabolism* / Q000502:physiology; D004591:Electrophoresis, Polyacrylamide Gel; D017353:Gene Deletion; D005816:Genetic Complementation Test; D005947:Glucose / Q000378:metabolism / Q000493:pharmacokinetics; D008320:Maltose / Q000378:metabolism / Q000493:pharmacokinetics; D008954:Models, Biological; D009154:Mutation; D009876:Operon / Q000235:genetics; D011485:Protein Binding; D021382:Protein Sorting Signals; D048229:Sulfolobus solfataricus / Q000235:genetics / Q000378:metabolism*
D018528:ATP-Binding Cassette Transporters; D002241:Carbohydrates; D002250:Carbon Radioisotopes; D002352:Carrier Proteins; D021382:Protein Sorting Signals; D008320:Maltose; D001089:Arabinose; D005947:Glucose