A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis

Medema MH, Zhou M, van Hijum SAFT, Gloerich J, Wessels HJCT, Siezen RJ, Strous M (2010)
BMC Genomics 11(1): 299.

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Background Anaerobic ammonium-oxidizing (anammox) bacteria perform a key step in global nitrogen cycling. These bacteria make use of an organelle to oxidize ammonia anaerobically to nitrogen (N2) and so contribute ~50% of the nitrogen in the atmosphere. It is currently unknown which proteins constitute the organellar proteome and how anammox bacteria are able to specifically target organellar and cell-envelope proteins to their correct final destinations. Experimental approaches are complicated by the absence of pure cultures and genetic accessibility. However, the genome of the anammox bacterium Candidatus "Kuenenia stuttgartiensis" has recently been sequenced. Here, we make use of these genome data to predict the organellar sub-proteome and address the molecular basis of protein sorting in anammox bacteria. Results Two training sets representing organellar (30 proteins) and cell envelope (59 proteins) proteins were constructed based on previous experimental evidence and comparative genomics. Random forest (RF) classifiers trained on these two sets could differentiate between organellar and cell envelope proteins with ~89% accuracy using 400 features consisting of frequencies of two adjacent amino acid combinations. A physicochemically distinct organellar sub-proteome containing 562 proteins was predicted with the best RF classifier. This set included almost all catabolic and respiratory factors encoded in the genome. Apparently, the cytoplasmic membrane performs no catabolic functions. We predict that the Tat-translocation system is located exclusively in the organellar membrane, whereas the Sec-translocation system is located on both the organellar and cytoplasmic membranes. Canonical signal peptides were predicted and validated experimentally, but a specific (N- or C-terminal) signal that could be used for protein targeting to the organelle remained elusive. Conclusions A physicochemically distinct organellar sub-proteome was predicted from the genome of the anammox bacterium K. stuttgartiensis. This result provides strong in silico support for the existing experimental evidence for the existence of an organelle in this bacterium, and is an important step forward in unravelling a geochemically relevant case of cytoplasmic differentiation in bacteria. The predicted dual location of the Sec-translocation system and the apparent absence of a specific N- or C-terminal signal in the organellar proteins suggests that additional chaperones may be necessary that act on an as-yet unknown property of the targeted proteins.
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Medema MH, Zhou M, van Hijum SAFT, et al. A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis. BMC Genomics. 2010;11(1):299.
Medema, M. H., Zhou, M., van Hijum, S. A. F. T., Gloerich, J., Wessels, H. J. C. T., Siezen, R. J., & Strous, M. (2010). A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis. BMC Genomics, 11(1), 299. doi:10.1186/1471-2164-11-299
Medema, M. H., Zhou, M., van Hijum, S. A. F. T., Gloerich, J., Wessels, H. J. C. T., Siezen, R. J., and Strous, M. (2010). A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis. BMC Genomics 11, 299.
Medema, M.H., et al., 2010. A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis. BMC Genomics, 11(1), p 299.
M.H. Medema, et al., “A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis”, BMC Genomics, vol. 11, 2010, pp. 299.
Medema, M.H., Zhou, M., van Hijum, S.A.F.T., Gloerich, J., Wessels, H.J.C.T., Siezen, R.J., Strous, M.: A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis. BMC Genomics. 11, 299 (2010).
Medema, Marnix H., Zhou, Miaomiao, van Hijum, Sacha A. F. T., Gloerich, Jolein, Wessels, Hans J. C. T, Siezen, Roland J., and Strous, Marc. “A predicted physicochemically distinct sub-proteome associated with the intracellular organelle of the anammox bacterium Kuenenia stuttgartiensis”. BMC Genomics 11.1 (2010): 299.
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9 Zitationen in Europe PMC

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Subcellular localization of an ATPase in anammox bacteria using proteomics and immunogold electron microscopy.
Karlsson R, Karlsson A, Bäckman O, Johansson BR, Hulth S., FEMS Microbiol Lett 354(1), 2014
PMID: 24635406
The metagenome of the marine anammox bacterium 'Candidatus Scalindua profunda' illustrates the versatility of this globally important nitrogen cycle bacterium.
van de Vossenberg J, Woebken D, Maalcke WJ, Wessels HJ, Dutilh BE, Kartal B, Janssen-Megens EM, Roeselers G, Yan J, Speth D, Gloerich J, Geerts W, van der Biezen E, Pluk W, Francoijs KJ, Russ L, Lam P, Malfatti SA, Tringe SG, Haaijer SC, Op den Camp HJ, Stunnenberg HG, Amann R, Kuypers MM, Jetten MS., Environ Microbiol 15(5), 2013
PMID: 22568606
Data mining in the Life Sciences with Random Forest: a walk in the park or lost in the jungle?
Touw WG, Bayjanov JR, Overmars L, Backus L, Boekhorst J, Wels M, van Hijum SA., Brief Bioinform 14(3), 2013
PMID: 22786785
How to make a living from anaerobic ammonium oxidation.
Kartal B, de Almeida NM, Maalcke WJ, Op den Camp HJ, Jetten MS, Keltjens JT., FEMS Microbiol Rev 37(3), 2013
PMID: 23210799
Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties.
van Niftrik L, Jetten MS., Microbiol Mol Biol Rev 76(3), 2012
PMID: 22933561

101 References

Daten bereitgestellt von Europe PubMed Central.

Anaerobic oxidation of methane and ammonium
AUTHOR UNKNOWN, 2004
Biochemistry and molecular biology of anammox bacteria
AUTHOR UNKNOWN, 2009
Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation
AUTHOR UNKNOWN, 2005
Global impact and application of the anaerobic ammonium-oxidizing (anammox) bacteria
AUTHOR UNKNOWN, 2006
Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell
AUTHOR UNKNOWN, 2001
Intracellular compartmentation in planctomycetes
AUTHOR UNKNOWN, 2005
The anammoxosome: an intracytoplasmic compartment in anammox bacteria.
van Niftrik LA, Fuerst JA, Sinninghe Damste JS, Kuenen JG, Jetten MS, Strous M., FEMS Microbiol. Lett. 233(1), 2004
PMID: 15098544
Deciphering the evolution and metabolism of an anammox bacterium from a community genome.
Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Medigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJ, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MS, Wagner M, Le Paslier D., Nature 440(7085), 2006
PMID: 16598256
Identification of key proteins involved in the anammox reaction.
Karlsson R, Karlsson A, Backman O, Johansson BR, Hulth S., FEMS Microbiol. Lett. 297(1), 2009
PMID: 19558586
Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome C proteins.
van Niftrik L, Geerts WJ, van Donselaar EG, Humbel BM, Webb RI, Fuerst JA, Verkleij AJ, Jetten MS, Strous M., J. Bacteriol. 190(2), 2007
PMID: 17993524
Molecular mechanisms of magnetosome formation
AUTHOR UNKNOWN, 2007

AUTHOR UNKNOWN, 1995
Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria.
van Niftrik L, Geerts WJ, van Donselaar EG, Humbel BM, Yakushevska A, Verkleij AJ, Jetten MS, Strous M., J. Struct. Biol. 161(3), 2007
PMID: 17604181
Cell division ring, a new cell division protein and vertical inheritance of a bacterial organelle in anammox planctomycetes.
van Niftrik L, Geerts WJ, van Donselaar EG, Humbel BM, Webb RI, Harhangi HR, Camp HJ, Fuerst JA, Verkleij AJ, Jetten MS, Strous M., Mol. Microbiol. 73(6), 2009
PMID: 19708922
Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes
AUTHOR UNKNOWN, 1996
Protein import into peroxisomes and biogenesis of the organelle.
Subramani S., Annu. Rev. Cell Biol. 9(), 1993
PMID: 8280468
Nuclear targeting signal recognition: a key control point in nuclear transport?
Jans DA, Xiao CY, Lam MH., Bioessays 22(6), 2000
PMID: 10842307
Import of proteins into mitochondria and chloroplasts.
Haucke V, Schatz G., Trends Cell Biol. 7(3), 1997
PMID: 17708917
Versatility of the mitochondrial protein import machinery
AUTHOR UNKNOWN, 2001
Mutational analysis of Salmonella translocated effector members SifA and SopD2 reveals domains implicated in translocation, subcellular localization and function.
Brown NF, Szeto J, Jiang X, Coombes BK, Finlay BB, Brumell JH., Microbiology (Reading, Engl.) 152(Pt 8), 2006
PMID: 16849798
The surprising complexity of signal sequences.
Hegde RS, Bernstein HD., Trends Biochem. Sci. 31(10), 2006
PMID: 16919958
Signal sequence directs localized secretion of bacterial surface proteins.
Carlsson F, Stalhammar-Carlemalm M, Flardh K, Sandin C, Carlemalm E, Lindahl G., Nature 442(7105), 2006
PMID: 16929299
Proteins in different Synechocystis compartments have distinguishing N-terminal features: a combined proteomics and multivariate sequence analysis.
Rajalahti T, Huang F, Klement MR, Pisareva T, Edman M, Sjostrom M, Wieslander A, Norling B., J. Proteome Res. 6(7), 2007
PMID: 17508731
Evolutionary conservation of dual Sec translocases in the cyanelles of Cyanophora paradoxa.
Yusa F, Steiner JM, Loffelhardt W., BMC Evol. Biol. 8(), 2008
PMID: 18976493
An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by 31P NMR.
van der Star WR, Dijkema C, de Waard P, Picioreanu C, Strous M, van Loosdrecht MC., Appl. Microbiol. Biotechnol. 86(1), 2009
PMID: 19862513
Persistent biases in the amino acid composition of prokaryotic proteins.
Pascal G, Medigue C, Danchin A., Bioessays 28(7), 2006
PMID: 16850406
Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway
AUTHOR UNKNOWN, 2002
PilFind
AUTHOR UNKNOWN, 0
Prediction of protein subcellular localization by support vector machines using multi-scale energy and pseudo amino acid composition
AUTHOR UNKNOWN, 2007
A computational approach for the identification of small GTPases based on preprocessed amino acid sequences.
Heider D, Appelmann J, Bayro T, Dreckmann W, Held A, Winkler J, Barnekow A, Borschbach M., Technol. Cancer Res. Treat. 8(5), 2009
PMID: 19754209
Sequence-based prediction of type III secreted proteins.
Arnold R, Brandmaier S, Kleine F, Tischler P, Heinz E, Behrens S, Niinikoski A, Mewes HW, Horn M, Rattei T., PLoS Pathog. 5(4), 2009
PMID: 19390696
SubCellProt: predicting protein subcellular localization using machine learning approaches.
Garg P, Sharma V, Chaudhari P, Roy N., In Silico Biol. (Gedrukt) 9(1-2), 2009
PMID: 19537160
DNA-Prot: identification of DNA binding proteins from protein sequence information using random forest.
Kumar KK, Pugalenthi G, Suganthan PN., J. Biomol. Struct. Dyn. 26(6), 2009
PMID: 19385697
Predicting disordered regions in proteins using the profiles of amino acid indices.
Han P, Zhang X, Feng ZP., BMC Bioinformatics 10 Suppl 1(), 2009
PMID: 19208144
Machine Learning Benchmarks and Random Forest Regression
AUTHOR UNKNOWN, 2004
Random Forests
AUTHOR UNKNOWN, 2001
Molecular mechanisms of cytochrome c biogenesis: three distinct systems
AUTHOR UNKNOWN, 1998
The Pfam protein families database.
Bateman A, Birney E, Durbin R, Eddy SR, Howe KL, Sonnhammer EL., Nucleic Acids Res. 28(1), 2000
PMID: 10592242
Combined structural and chemical analysis of the anammoxosome: A membrane-bounded intracytoplasmic compartment in anammox bacteria
AUTHOR UNKNOWN, 2008
Bifunctional TatA subunits in minimal Tat protein translocases.
Jongbloed JD, van der Ploeg R, van Dijl JM., Trends Microbiol. 14(1), 2005
PMID: 16303306
Sec-dependent protein translocation across biological membranes: evolutionary conservation of an essential protein transport pathway (review)
AUTHOR UNKNOWN, 2005
Structure and function of the bacterial Sec translocon
AUTHOR UNKNOWN, 2007
Bifunctional TatA subunits in minimal Tat protein translocases.
Jongbloed JD, van der Ploeg R, van Dijl JM., Trends Microbiol. 14(1), 2005
PMID: 16303306
Type I signal peptidase: an overview
AUTHOR UNKNOWN, 2005
Lipoprotein trafficking in Escherichia coli
AUTHOR UNKNOWN, 2004
The type 4 prepilin peptidases comprise a novel family of aspartic acid proteases
AUTHOR UNKNOWN, 2000
Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server.
Kall L, Krogh A, Sonnhammer EL., Nucleic Acids Res. 35(Web Server issue), 2007
PMID: 17483518
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
The HMMTOP transmembrane topology prediction server.
Tusnady GE, Simon I., Bioinformatics 17(9), 2001
PMID: 11590105
Look on the positive side! The orientation, identification and bioenergetics of 'Archaeal' membrane-bound nitrate reductases.
Martinez-Espinosa RM, Dridge EJ, Bonete MJ, Butt JN, Butler CS, Sargent F, Richardson DJ., FEMS Microbiol. Lett. 276(2), 2007
PMID: 17888006
WebLogo: a sequence logo generator.
Crooks GE, Hon G, Chandonia JM, Brenner SE., Genome Res. 14(6), 2004
PMID: 15173120

AUTHOR UNKNOWN, 1998
MEME: discovering and analyzing DNA and protein sequence motifs.
Bailey TL, Williams N, Misleh C, Li WW., Nucleic Acids Res. 34(Web Server issue), 2006
PMID: 16845028
Linearly concatenated cyclobutane lipids form a dense bacterial membrane.
Sinninghe Damste JS, Strous M, Rijpstra WI, Hopmans EC, Geenevasen JA, van Duin AC, van Niftrik LA, Jetten MS., Nature 419(6908), 2002
PMID: 12384695
A simple method for displaying the hydropathic character of a protein.
Kyte J, Doolittle RF., J. Mol. Biol. 157(1), 1982
PMID: 7108955
Signal-CF: a subsite-coupled and window-fusing approach for predicting signal peptides
AUTHOR UNKNOWN, 2007
Improved prediction of signal peptides: SignalP 3.0.
Bendtsen JD, Nielsen H, von Heijne G, Brunak S., J. Mol. Biol. 340(4), 2004
PMID: 15223320
PrediSi: prediction of signal peptides and their cleavage positions.
Hiller K, Grote A, Scheer M, Munch R, Jahn D., Nucleic Acids Res. 32(Web Server issue), 2004
PMID: 15215414
Signal-3L: A 3-layer approach for predicting signal peptides
AUTHOR UNKNOWN, 2007
Overflow of a hyper-produced secretory protein from the Bacillus Sec pathway into the Tat pathway for protein secretion as revealed by proteogenomics.
Kouwen TR, van der Ploeg R, Antelmann H, Hecker M, Homuth G, Mader U, van Dijl JM., Proteomics 9(4), 2009
PMID: 19180538
Methods of quantitative proteomics and their application to plant organelle characterization
AUTHOR UNKNOWN, 2006
Mass spectrometry-based quantitative proteomics
AUTHOR UNKNOWN, 2007
Control of cell shape and elongation by the rodA gene in Bacillus subtilis
AUTHOR UNKNOWN, 1998
Bacterial cell division and the Z ring
AUTHOR UNKNOWN, 1997
Serralysin and related bacterial proteinases.
Maeda H, Morihara K., Meth. Enzymol. 248(), 1995
PMID: 7674934
Alignment and structure prediction of divergent protein families: periplasmic and outer membrane proteins of bacterial efflux pumps
AUTHOR UNKNOWN, 1999
Multidrug resistance mechanisms: drug efflux across two membranes
AUTHOR UNKNOWN, 2000
AcrAB and related multidrug efflux pumps of Escherichia coli
AUTHOR UNKNOWN, 2001
Touch and go: tying TonB to transport
AUTHOR UNKNOWN, 2003
Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid
AUTHOR UNKNOWN, 1996
The versatile beta-barrel membrane protein
AUTHOR UNKNOWN, 2003
The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD)
AUTHOR UNKNOWN, 2000
Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria
AUTHOR UNKNOWN, 1993
Multiple roles of T7 RNA polymerase and T7 lysozyme during bacteriophage T7 infection
AUTHOR UNKNOWN, 2004
Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs
AUTHOR UNKNOWN, 1998
S-Layer proteins.
Sara M, Sleytr UB., J. Bacteriol. 182(4), 2000
PMID: 10648507
Structure of a fibronectin type III domain from tenascin phased by MAD analysis of the selenomethionyl protein.
Leahy DJ, Hendrickson WA, Aukhil I, Erickson HP., Science 258(5084), 1992
PMID: 1279805
Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily
AUTHOR UNKNOWN, 2003
MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences.
Campanella JJ, Bitincka L, Smalley J., BMC Bioinformatics 4(), 2003
PMID: 12854978
The RPSP: Web server for prediction of signal peptides
AUTHOR UNKNOWN, 2007
Classification and Regression by randomForest
AUTHOR UNKNOWN, 2002

AUTHOR UNKNOWN, 2009
Probability-based protein identification by searching sequence databases using mass spectrometry data.
Perkins DN, Pappin DJ, Creasy DM, Cottrell JS., Electrophoresis 20(18), 1999
PMID: 10612281
Basic local alignment search tool
AUTHOR UNKNOWN, 1990
Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production.
van de Vossenberg J, Rattray JE, Geerts W, Kartal B, van Niftrik L, van Donselaar EG, Sinninghe Damste JS, Strous M, Jetten MS., Environ. Microbiol. 10(11), 2008
PMID: 18462401
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ., Nucleic Acids Res. 25(17), 1997
PMID: 9254694
Finding functional features in Saccharomyces genomes by phylogenetic footprinting.
Cliften P, Sudarsanam P, Desikan A, Fulton L, Fulton B, Majors J, Waterston R, Cohen BA, Johnston M., Science 301(5629), 2003
PMID: 12775844
Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture.
Shimamura M, Nishiyama T, Shigetomo H, Toyomoto T, Kawahara Y, Furukawa K, Fujii T., Appl. Environ. Microbiol. 73(4), 2006
PMID: 17172456
Another multiheme protein, hydroxylamine oxidoreductase, abundantly produced in an anammox bacterium besides the hydrazine-oxidizing enzyme.
Shimamura M, Nishiyama T, Shinya K, Kawahara Y, Furukawa K, Fujii T., J. Biosci. Bioeng. 105(3), 2008
PMID: 18397776

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