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Vol. 11, Issue 9, 1484-1502, September 2001

A Proteomic View on Genome-Based Signal Peptide Predictions

Haike Antelmann,1 Harold Tjalsma,2 Birgit Voigt,1 Steffen Ohlmeier,1 Sierd Bron,2 Jan Maarten van Dijl,3,4 and Michael Hecker1

1 Institut für Mikrobiologie und Molekularbiologie, Ernst-Moritz-Arndt-Universiät Greifswald, D-17487 Greifswald, Germany; 2 Department of Genetics, Groningen Biomolecular Sciences and Biotechnology Institute, 9751 NN Haren, The Netherlands; 3 Department of Pharmaceutical Biology, University of Groningen, Groningen, The Netherlands

The availability of complete genome sequences has allowed the prediction of all exported proteins of the corresponding organisms with dedicated algorithms. Even though numerous studies report on genome-based predictions of signal peptides and cell retention signals, they lack a proteomic verification. For example, 180 secretory and 114 lipoprotein signal peptides were predicted recently for the Gram-positive eubacterium Bacillus subtilis. In the present studies, proteomic approaches were used to define the extracellular complement of the B. subtilis secretome. Using different growth conditions and a hyper-secreting mutant, ~200 extracellular proteins were visualized by two-dimensional (2D) gel electrophoresis, of which 82 were identified by mass spectrometry. These include 41 proteins that have a potential signal peptide with a type I signal peptidase (SPase) cleavage site, and lack a retention signal. Strikingly, the remaining 41 proteins were predicted previously to be cell associated because of the apparent absence of a signal peptide (22), or the presence of specific cell retention signals in addition to an export signal (19). To test the importance of the five type I SPases and the unique lipoprotein-specific SPase of B. subtilis, the extracellular proteome of (multiple) SPase mutants was analyzed. Surprisingly, only the processing of the polytopic membrane protein YfnI was strongly inhibited in Spase I mutants, showing for the first time that a native eubacterial membrane protein is a genuine Spase I substrate. Furthermore, a mutation affecting lipoprotein modification and processing resulted in the shedding of at least 23 (lipo-)proteins into the medium. In conclusion, our observations show that genome-based predictions reflect the actual composition of the extracellular proteome for ~50%. Major problems are currently encountered with the prediction of extracellular proteins lacking signal peptides (including cytoplasmic proteins) and lipoproteins.

4 Corresponding author.

11:1484-1502 ©2001 by Cold Spring Harbor Laboratory Press  ISSN 1088-9051/01 $5.00
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