Comprehensive subcellular topologies of polypeptides in Streptomyces

Tsolis KC, Tsare E-P, Orfanoudaki G, Busche T, Kanaki K, Ramakrishnan R, Rousseau F, Schymkowitz J, Rückert C, Kalinowski J, Anne J, et al. (2018)

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Tsolis, Konstantinos C.; Tsare, Evridiki-Pandora; Orfanoudaki, Georgia; Busche, TobiasUniBi; Kanaki, Katerina; Ramakrishnan, Reshmi; Rousseau, Frederic; Schymkowitz, Joost; Rückert, ChristianUniBi ; Kalinowski, JörnUniBi; Anne, Jozef; Karamanou, Spyridoula
Abstract / Bemerkung
Background: Members of the genus Streptomyces are Gram-positive bacteria that are used as important cell factories to produce secondary metabolites and secrete heterologous proteins. They possess some of the largest bacterial genomes and thus proteomes. Understanding their complex proteomes and metabolic regulation will improve any genetic engineering approach. Results: Here, we performed a comprehensive annotation of the subcellular localization of the proteome of Streptomyces lividans TK24 and developed the Subcellular Topology of Polypeptides in Streptomyces database (SToPSdb) to make this information widely accessible. We first introduced a uniform, improved nomenclature that re-annotated the names of similar to 4000 proteins based on functional and structural information. Then protein localization was assigned de novo using prediction tools and edited by manual curation for 7494 proteins, including information for 183 proteins that resulted from a recent genome re-annotation and are not available in current databases. The S. lividans proteome was also linked with those of other model bacterial strains including Streptomyces coelicolor A3(2) and Escherichia coli K-12, based on protein homology, and can be accessed through an open web interface. Finally, experimental data derived from proteomics experiments have been incorporated and provide validation for protein existence or topology for 579 proteins. Proteomics also reveals proteins released from vesicles that bleb off the membrane. All export systems known in S. lividans are also presented and exported proteins assigned export routes, where known. Conclusions: SToPSdb provides an updated and comprehensive protein localization annotation resource for S. lividans and other streptomycetes. It forms the basis for future linking to databases containing experimental data of proteomics, genomics and metabolomics studies for this organism.
S. lividans TK24; Proteome annotation; Protein subcellular topology; Protein subcellular localization; Database; Secretome; Membranome; Signal peptide; Sortase; Peptidoglycan; Sec system; TAT system
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Tsolis KC, Tsare E-P, Orfanoudaki G, et al. Comprehensive subcellular topologies of polypeptides in Streptomyces. MICROBIAL CELL FACTORIES. 2018;17(1): 12.
Tsolis, K. C., Tsare, E. - P., Orfanoudaki, G., Busche, T., Kanaki, K., Ramakrishnan, R., Rousseau, F., et al. (2018). Comprehensive subcellular topologies of polypeptides in Streptomyces. MICROBIAL CELL FACTORIES, 17(1), 12. doi:10.1186/s12934-018-0892-0
Tsolis, Konstantinos C., Tsare, Evridiki-Pandora, Orfanoudaki, Georgia, Busche, Tobias, Kanaki, Katerina, Ramakrishnan, Reshmi, Rousseau, Frederic, et al. 2018. “Comprehensive subcellular topologies of polypeptides in Streptomyces”. MICROBIAL CELL FACTORIES 17 (1): 12.
Tsolis, K. C., Tsare, E. - P., Orfanoudaki, G., Busche, T., Kanaki, K., Ramakrishnan, R., Rousseau, F., Schymkowitz, J., Rückert, C., Kalinowski, J., et al. (2018). Comprehensive subcellular topologies of polypeptides in Streptomyces. MICROBIAL CELL FACTORIES 17:12.
Tsolis, K.C., et al., 2018. Comprehensive subcellular topologies of polypeptides in Streptomyces. MICROBIAL CELL FACTORIES, 17(1): 12.
K.C. Tsolis, et al., “Comprehensive subcellular topologies of polypeptides in Streptomyces”, MICROBIAL CELL FACTORIES, vol. 17, 2018, : 12.
Tsolis, K.C., Tsare, E.-P., Orfanoudaki, G., Busche, T., Kanaki, K., Ramakrishnan, R., Rousseau, F., Schymkowitz, J., Rückert, C., Kalinowski, J., Anne, J., Karamanou, S., Klapa, M.I., Economou, A.: Comprehensive subcellular topologies of polypeptides in Streptomyces. MICROBIAL CELL FACTORIES. 17, : 12 (2018).
Tsolis, Konstantinos C., Tsare, Evridiki-Pandora, Orfanoudaki, Georgia, Busche, Tobias, Kanaki, Katerina, Ramakrishnan, Reshmi, Rousseau, Frederic, Schymkowitz, Joost, Rückert, Christian, Kalinowski, Jörn, Anne, Jozef, Karamanou, Spyridoula, Klapa, Maria I., and Economou, Anastassios. “Comprehensive subcellular topologies of polypeptides in Streptomyces”. MICROBIAL CELL FACTORIES 17.1 (2018): 12.

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The Cellular Mechanisms that Ensure an Efficient Secretion in Streptomyces.
Gullón S, Mellado RP., Antibiotics (Basel) 7(2), 2018
PMID: 29661993
Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions.
Rebets Y, Tsolis KC, Guðmundsdóttir EE, Koepff J, Wawiernia B, Busche T, Bleidt A, Horbal L, Myronovskyi M, Ahmed Y, Wiechert W, Rückert C, Hamed MB, Bilyk B, Anné J, Friðjónsson Ó, Kalinowski J, Oldiges M, Economou A, Luzhetskyy A., Front Microbiol 9(), 2018
PMID: 30619125

75 References

Daten bereitgestellt von Europe PubMed Central.

The taxonomy of Streptomyces and related genera.
Anderson AS, Wellington EM., Int. J. Syst. Evol. Microbiol. 51(Pt 3), 2001
PMID: 11411701
The complex extracellular biology of Streptomyces.
Chater KF, Biro S, Lee KJ, Palmer T, Schrempf H., FEMS Microbiol. Rev. 34(2), 2009
PMID: 20088961
Towards a new science of secondary metabolism.
Craney A, Ahmed S, Nodwell J., J. Antibiot. 66(7), 2013
PMID: 23612726
Discovery of microbial natural products by activation of silent biosynthetic gene clusters.
Rutledge PJ, Challis GL., Nat. Rev. Microbiol. 13(8), 2015
PMID: 26119570
Evaluation of a novel subtilisin inhibitor gene and mutant derivatives for the expression and secretion of mouse tumor necrosis factor alpha by Streptomyces lividans.
Lammertyn E, Van Mellaert L, Schacht S, Dillen C, Sablon E, Van Broekhoven A, Anne J., Appl. Environ. Microbiol. 63(5), 1997
PMID: 9143114
Functional large-scale production of a novel Jonesia sp. xyloglucanase by heterologous secretion from Streptomyces lividans.
Sianidis G, Pozidis C, Becker F, Vrancken K, Sjoeholm C, Karamanou S, Takamiya-Wik M, van Mellaert L, Schaefer T, Anne J, Economou A., J. Biotechnol. 121(4), 2005
PMID: 16168511
Large-scale production of a thermostable Rhodothermus marinus cellulase by heterologous secretion from Streptomyces lividans.
Hamed MB, Karamanou S, Olafsdottir S, Basilio JSM, Simoens K, Tsolis KC, Van Mellaert L, Guðmundsdottir EE, Hreggvidsson GO, Anne J, Bernaerts K, Fridjonsson OH, Economou A., Microb. Cell Fact. 16(1), 2017
PMID: 29274637
Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2).
Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O'Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA., Nature 417(6885), 2002
PMID: 12000953
Complete genome sequence of Streptomyces lividans TK24.
Ruckert C, Albersmeier A, Busche T, Jaenicke S, Winkler A, Friðjonsson OH, Hreggviðsson GO, Lambert C, Badcock D, Bernaerts K, Anne J, Economou A, Kalinowski J., J. Biotechnol. 199(), 2015
PMID: 25680930
Streptomyces lividans as host for heterologous protein production.
Anne J, Van Mellaert L., FEMS Microbiol. Lett. 114(2), 1993
PMID: 8282181
Recombinant protein production and streptomycetes.
Anne J, Maldonado B, Van Impe J, Van Mellaert L, Bernaerts K., J. Biotechnol. 158(4), 2011
PMID: 21777629

J, 2017
Production and secretion of proteins by streptomycetes.
Gilbert M, Morosoli R, Shareck F, Kluepfel D., Crit. Rev. Biotechnol. 15(1), 1995
PMID: 7736599
Protein export through the bacterial Sec pathway.
Tsirigotaki A, De Geyter J, Sostaric N, Economou A, Karamanou S., Nat. Rev. Microbiol. 15(1), 2016
PMID: 27890920
The twin-arginine translocation (Tat) protein export pathway.
Palmer T, Berks BC., Nat. Rev. Microbiol. 10(7), 2012
PMID: 22683878
Protein secretion biotechnology in Gram-positive bacteria with special emphasis on Streptomyces lividans.
Anne J, Vrancken K, Van Mellaert L, Van Impe J, Bernaerts K., Biochim. Biophys. Acta 1843(8), 2014
PMID: 24412306
StreptomeDB 2.0--an extended resource of natural products produced by streptomycetes.
Klementz D, Doring K, Lucas X, Telukunta KK, Erxleben A, Deubel D, Erber A, Santillana I, Thomas OS, Bechthold A, Gunther S., Nucleic Acids Res. 44(D1), 2015
PMID: 26615197
Universal seeds for cDNA-to-genome comparison.
Zhou L, Stanton J, Florea L., BMC Bioinformatics 9(), 2008
PMID: 18215286
Proteome-wide subcellular topologies of E. coli polypeptides database (STEPdb).
Orfanoudaki G, Economou A., Mol. Cell Proteomics 13(12), 2014
PMID: 25210196
SignalP 4.0: discriminating signal peptides from transmembrane regions.
Petersen TN, Brunak S, von Heijne G, Nielsen H., Nat. Methods 8(10), 2011
PMID: 21959131
Methods for the bioinformatic identification of bacterial lipoproteins encoded in the genomes of Gram-positive bacteria
Rahman O, Cummings SP, Harrington DJ, Sutcliffe IC., World J. Microbiol. Biotechnol. 24(11), 2008
PMID: IND44107313
Combined prediction of Tat and Sec signal peptides with hidden Markov models.
Bagos PG, Nikolaou EP, Liakopoulos TD, Tsirigos KD., Bioinformatics 26(22), 2010
PMID: 20847219
A combined transmembrane topology and signal peptide prediction method.
Kall L, Krogh A, Sonnhammer EL., J. Mol. Biol. 338(5), 2004
PMID: 15111065
Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
Krogh A, Larsson B, von Heijne G, Sonnhammer EL., J. Mol. Biol. 305(3), 2001
PMID: 11152613
InterPro in 2017-beyond protein family and domain annotations.
Finn RD, Attwood TK, Babbitt PC, Bateman A, Bork P, Bridge AJ, Chang HY, Dosztanyi Z, El-Gebali S, Fraser M, Gough J, Haft D, Holliday GL, Huang H, Huang X, Letunic I, Lopez R, Lu S, Marchler-Bauer A, Mi H, Mistry J, Natale DA, Necci M, Nuka G, Orengo CA, Park Y, Pesseat S, Piovesan D, Potter SC, Rawlings ND, Redaschi N, Richardson L, Rivoire C, Sangrador-Vegas A, Sigrist C, Sillitoe I, Smithers B, Squizzato S, Sutton G, Thanki N, Thomas PD, Tosatto SC, Wu CH, Xenarios I, Yeh LS, Young SY, Mitchell AL., Nucleic Acids Res. 45(D1), 2016
PMID: 27899635
The Pfam protein families database: towards a more sustainable future.
Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A., Nucleic Acids Res. 44(D1), 2015
PMID: 26673716
SMART: recent updates, new developments and status in 2015.
Letunic I, Doerks T, Bork P., Nucleic Acids Res. 43(Database issue), 2014
PMID: 25300481
EDGAR 2.0: an enhanced software platform for comparative gene content analyses.
Blom J, Kreis J, Spanig S, Juhre T, Bertelli C, Ernst C, Goesmann A., Nucleic Acids Res. 44(W1), 2016
PMID: 27098043
Basic local alignment search tool.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ., J. Mol. Biol. 215(3), 1990
PMID: 2231712
The Streptomyces subtilisin inhibitor (SSI) gene in Streptomyces coelicolor A3(2).
Kato JY, Hirano S, Ohnishi Y, Horinouchi S., Biosci. Biotechnol. Biochem. 69(8), 2005
PMID: 16116298
The Escherichia coli peripheral inner membrane proteome.
Papanastasiou M, Orfanoudaki G, Koukaki M, Kountourakis N, Sardis MF, Aivaliotis M, Karamanou S, Economou A., Mol. Cell Proteomics 12(3), 2012
PMID: 23230279
Rapid label-free quantitative analysis of the E. coli BL21(DE3) inner membrane proteome.
Papanastasiou M, Orfanoudaki G, Kountourakis N, Koukaki M, Sardis MF, Aivaliotis M, Tsolis KC, Karamanou S, Economou A., Proteomics 16(1), 2015
PMID: 26466526
The Roles of Moonlighting Proteins in Bacteria.
Wang G, Xia Y, Cui J, Gu Z, Song Y, Chen YQ, Chen H, Zhang H, Chen W., Curr Issues Mol Biol 16(), 2013
PMID: 23872606
Extracellular Streptomyces vesicles: amphorae for survival and defence.
Schrempf H, Koebsch I, Walter S, Engelhardt H, Meschke H., Microb Biotechnol 4(2), 2011
PMID: 21342473
Structural and genetic analyses reveal the protein SepF as a new membrane anchor for the Z ring.
Duman R, Ishikawa S, Celik I, Strahl H, Ogasawara N, Troc P, Lowe J, Hamoen LW., Proc. Natl. Acad. Sci. U.S.A. 110(48), 2013
PMID: 24218584
Function and evolution of two forms of SecDF homologs in Streptomyces coelicolor.
Zhou Z, Li Y, Sun N, Sun Z, Lv L, Wang Y, Shen L, Li YQ., PLoS ONE 9(8), 2014
PMID: 25140821
Genomic data mining reveals a rich repertoire of transport proteins in Streptomyces.
Zhou Z, Sun N, Wu S, Li YQ, Wang Y., BMC Genomics 17 Suppl 7(), 2016
PMID: 27557108
Structure and function of a membrane component SecDF that enhances protein export.
Tsukazaki T, Mori H, Echizen Y, Ishitani R, Fukai S, Tanaka T, Perederina A, Vassylyev DG, Kohno T, Maturana AD, Ito K, Nureki O., Nature 474(7350), 2011
PMID: 21562494
The importance of the Tat-dependent protein secretion pathway in Streptomyces as revealed by phenotypic changes in tat deletion mutants and genome analysis.
Schaerlaekens K, Van Mellaert L, Lammertyn E, Geukens N, Anne J., Microbiology (Reading, Engl.) 150(Pt 1), 2004
PMID: 14702394
The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor.
Widdick DA, Dilks K, Chandra G, Bottrill A, Naldrett M, Pohlschroder M, Palmer T., Proc. Natl. Acad. Sci. U.S.A. 103(47), 2006
PMID: 17093047
The twin arginine protein transport pathway exports multiple virulence proteins in the plant pathogen Streptomyces scabies.
Joshi MV, Mann SG, Antelmann H, Widdick DA, Fyans JK, Chandra G, Hutchings MI, Toth I, Hecker M, Loria R, Palmer T., Mol. Microbiol. 77(1), 2010
PMID: 20487278
Secretion of the Streptomyces tyrosinase is mediated through its trans-activator protein, MelC1.
Leu WM, Chen LY, Liaw LL, Lee YH., J. Biol. Chem. 267(28), 1992
PMID: 1400329
Secretion systems in Gram-negative bacteria: structural and mechanistic insights.
Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, Waksman G., Nat. Rev. Microbiol. 13(6), 2015
PMID: 25978706
Type VII secretion--mycobacteria show the way.
Abdallah AM, Gey van Pittius NC, Champion PA, Cox J, Luirink J, Vandenbroucke-Grauls CM, Appelmelk BJ, Bitter W., Nat. Rev. Microbiol. 5(11), 2007
PMID: 17922044
The ESX/type VII secretion system modulates development, but not virulence, of the plant pathogen Streptomyces scabies.
Fyans JK, Bignell D, Loria R, Toth I, Palmer T., Mol. Plant Pathol. 14(2), 2012
PMID: 23009676
Non classical secretion systems.
Lloubes R, Bernadac A, Houot L, Pommier S., Res. Microbiol. 164(6), 2013
PMID: 23542424
Non-classical protein secretion in bacteria.
Bendtsen JD, Kiemer L, Fausboll A, Brunak S., BMC Microbiol. 5(), 2005
PMID: 16212653
Architects at the bacterial surface - sortases and the assembly of pili with isopeptide bonds.
Hendrickx AP, Budzik JM, Oh SY, Schneewind O., Nat. Rev. Microbiol. 9(3), 2011
PMID: 21326273
Crystal Structure of the Streptomyces coelicolor Sortase E1 Transpeptidase Provides Insight into the Binding Mode of the Novel Class E Sorting Signal.
Kattke MD, Chan AH, Duong A, Sexton DL, Sawaya MR, Cascio D, Elliot MA, Clubb RT., PLoS ONE 11(12), 2016
PMID: 27936128
Sortase enzymes in Gram-positive bacteria.
Spirig T, Weiner EM, Clubb RT., Mol. Microbiol. 82(5), 2011
PMID: 22026821
Bacterial transmembrane proteins that lack N-terminal signal sequences.
Craney A, Tahlan K, Andrews D, Nodwell J., PLoS ONE 6(5), 2011
PMID: 21573234
Targeting pathways of C-tail-anchored proteins.
Borgese N, Fasana E., Biochim. Biophys. Acta 1808(3), 2010
PMID: 20646998
Signal sequence recognition and protein targeting.
Stroud RM, Walter P., Curr. Opin. Struct. Biol. 9(6), 1999
PMID: 10607673
Post-translocational folding of secretory proteins in Gram-positive bacteria.
Sarvas M, Harwood CR, Bron S, van Dijl JM., Biochim. Biophys. Acta 1694(1-3), 2004
PMID: 15546674
The BON domain: a putative membrane-binding domain.
Yeats C, Bateman A., Trends Biochem. Sci. 28(7), 2003
PMID: 12878000
Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G., Nat. Genet. 25(1), 2000
PMID: 10802651
Expansion of the Gene Ontology knowledgebase and resources.
The Gene Ontology Consortium., Nucleic Acids Res. 45(D1), 2016
PMID: 27899567
Influence of the culture medium composition on the excreted/secreted proteases from Streptomyces violaceoruber
Giarrizzo J, Bubis J, Taddei A., World J. Microbiol. Biotechnol. 23(4), 2007
PMID: IND43896585
Influence of culture conditions of Streptomyces sp. (strain S242) on chitinase production.
Saadoun I, Al-Omari R, Jaradat Z, Ababneh Q., Pol. J. Microbiol. 58(4), 2009
PMID: 20380144
Fast and reliable strain characterization of Streptomyces lividans through micro-scale cultivation.
Koepff J, Keller M, Tsolis KC, Busche T, Ruckert C, Hamed MB, Anne J, Kalinowski J, Wiechert W, Economou A, Oldiges M., Biotechnol. Bioeng. 114(9), 2017
PMID: 28436005
Quantitative Proteomics Analysis Confirmed Oxidative Metabolism Predominates in Streptomyces coelicolor versus Glycolytic Metabolism in Streptomyces lividans.
Millan-Oropeza A, Henry C, Blein-Nicolas M, Aubert-Frambourg A, Moussa F, Bleton J, Virolle MJ., J. Proteome Res. 16(7), 2017
PMID: 28560880
YidC/Oxa1p/Alb3: evolutionarily conserved mediators of membrane protein assembly.
Luirink J, Samuelsson T, de Gier JW., FEBS Lett. 501(1), 2001
PMID: 11457446
Independent gene duplications of the YidC/Oxa/Alb3 family enabled a specialized cotranslational function.
Funes S, Hasona A, Bauerschmitt H, Grubbauer C, Kauff F, Collins R, Crowley PJ, Palmer SR, Brady LJ, Herrmann JM., Proc. Natl. Acad. Sci. U.S.A. 106(16), 2009
PMID: 19366667
Sortagging: a versatile method for protein labeling.
Popp MW, Antos JM, Grotenbreg GM, Spooner E, Ploegh HL., Nat. Chem. Biol. 3(11), 2007
PMID: 17891153

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