A review on recent developments in mass spectrometry instrumentation and quantitative tools advancing bacterial proteomics

Proteomics has evolved substantially since its early days, some 20 years ago. In this mini-review, we aim to provide an overview of general methodologies and more recent developments in mass spectrometric approaches used for relative and absolute quantitation of proteins. Enhancement of sensitivity of the mass spectrometers as well as improved sample preparation and protein fractionation methods are resulting in a more comprehensive analysis of proteomes. We also document some upcoming trends for quantitative proteomics such as the use of label-free quantification methods. Hopefully, microbiologists will continue to explore proteomics as a tool in their research to understand the adaptation of microorganisms to their ever changing environment. We encourage them to incorporate some of the described new developments in mass spectrometry to facilitate their analyses and improve the general knowledge of the fascinating world of microorganisms.

[1]  P. Schoenmakers,et al.  High-efficiency liquid chromatography-mass spectrometry separations with 50 mm, 250 mm, and 1 m long polymer-based monolithic capillary columns for the characterization of complex proteolytic digests. , 2010, Journal of chromatography. A.

[2]  John D. Venable,et al.  Automated approach for quantitative analysis of complex peptide mixtures from tandem mass spectra , 2004, Nature Methods.

[3]  M. Gorenstein,et al.  Quantitative proteomic analysis by accurate mass retention time pairs. , 2005, Analytical chemistry.

[4]  Jennifer A Mead,et al.  Recent developments in public proteomic MS repositories and pipelines , 2009, Proteomics.

[5]  M. Mann,et al.  Stable Isotope Labeling by Amino Acids in Cell Culture, SILAC, as a Simple and Accurate Approach to Expression Proteomics* , 2002, Molecular & Cellular Proteomics.

[6]  J. Musser,et al.  Multi High-Throughput Approach for Highly Selective Identification of Vaccine Candidates: the Group A Streptococcus Case , 2012, Molecular & Cellular Proteomics.

[7]  Ruedi Aebersold,et al.  Options and considerations when selecting a quantitative proteomics strategy , 2010, Nature Biotechnology.

[8]  E. Heinzle,et al.  A 2D reversed-phase × ion-pair reversed-phase HPLC-MALDI TOF/TOF-MS approach for shotgun proteome analysis , 2009, Analytical and bioanalytical chemistry.

[9]  S. Bhaduri,et al.  Simple and rapid method for disruption of bacteria for protein studies , 1983, Applied and environmental microbiology.

[10]  D. Goodlett,et al.  Shotgun collision‐induced dissociation of peptides using a time of flight mass analyzer , 2003, Proteomics.

[11]  V. O’Flaherty,et al.  Optimisation of protein extraction and 2‐DE for metaproteomics of microbial communities from anaerobic wastewater treatment biofilms , 2009, Electrophoresis.

[12]  R. Aebersold,et al.  Proteome-wide cellular protein concentrations of the human pathogen Leptospira interrogans , 2009, Nature.

[13]  Lin Guo,et al.  Quantitative proteomic analysis of Salmonella enterica serovar Typhimurium under PhoP/PhoQ activation conditions. , 2011, Journal of proteome research.

[14]  Shu-Hui Chen,et al.  Stable-isotope dimethyl labeling for quantitative proteomics. , 2003, Analytical chemistry.

[15]  Marc R. Wilkins,et al.  Proteomics data mining , 2009, Expert review of proteomics.

[16]  S. Gygi,et al.  Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  R. Bischoff,et al.  Multidimensional chromatography coupled to mass spectrometry in analysing complex proteomics samples. , 2010, Journal of separation science.

[18]  Lennart Martens,et al.  The minimum information about a proteomics experiment (MIAPE) , 2007, Nature Biotechnology.

[19]  Roman Szucs,et al.  Evaluation of ultra performance liquid chromatography. Part I. Possibilities and limitations. , 2006, Journal of chromatography. A.

[20]  Joshua J. Coon,et al.  Sub-part-per-million Precursor and Product Mass Accuracy for High-throughput Proteomics on an Electron Transfer Dissociation-enabled Orbitrap Mass Spectrometer* , 2010, Molecular & Cellular Proteomics.

[21]  M. Mann,et al.  Mass spectrometry–based proteomics turns quantitative , 2005, Nature chemical biology.

[22]  D. Linke,et al.  Efficient subfractionation of gram-negative bacteria for proteomics studies. , 2010, Journal of proteome research.

[23]  Antoine H P America,et al.  Comparative LC‐MS: A landscape of peaks and valleys , 2008, Proteomics.

[24]  M. Mann,et al.  Super-SILAC mix for quantitative proteomics of human tumor tissue , 2010, Nature Methods.

[25]  W. N. Chen,et al.  iTRAQ-coupled 2-D LC-MS/MS analysis of cytoplasmic protein profile in Escherichia coli incubated with apidaecin IB. , 2011, Journal of proteomics.

[26]  S. Cordwell,et al.  Comparative proteomics of bacterial pathogens , 2001, Proteomics.

[27]  John R Yates,et al.  Optimization of mass spectrometry-compatible surfactants for shotgun proteomics. , 2007, Journal of proteome research.

[28]  Michael Hecker,et al.  From complementarity to comprehensiveness – targeting the membrane proteome of growing Bacillus subtilis by divergent approaches , 2008, Proteomics.

[29]  J. Gebler,et al.  Orthogonality of separation in two-dimensional liquid chromatography. , 2005, Analytical chemistry.

[30]  R. Aebersold,et al.  Mass Spectrometry and Protein Analysis , 2006, Science.

[31]  A. Chakraborty,et al.  Use of an integrated MS--multiplexed MS/MS data acquisition strategy for high-coverage peptide mapping studies. , 2007, Rapid communications in mass spectrometry : RCM.

[32]  J. Shabanowitz,et al.  Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[33]  John Skilling,et al.  A probabilistic framework for peptide and protein quantification from data-dependent and data-independent LC-MS proteomics experiments. , 2012, Omics : a journal of integrative biology.

[34]  L. Rychlewski,et al.  Proteomics of the dissimilatory iron‐reducing bacterium Shewanella oneidensis MR‐1, using a matrix‐assisted laser desorption/ionization‐tandem‐time of flight mass spectrometer , 2003, Proteomics.

[35]  B. Chain,et al.  A Quantitative Proteomics Design for Systematic Identification of Protease Cleavage Events* , 2010, Molecular & Cellular Proteomics.

[36]  M. Gorenstein,et al.  Simultaneous Qualitative and Quantitative Analysis of theEscherichia coli Proteome , 2006, Molecular & Cellular Proteomics.

[37]  J. Jorgenson,et al.  In-Depth Characterization of Slurry Packed Capillary Columns with 1.0-μm Nonporous Particles Using Reversed-Phase Isocratic Ultrahigh-Pressure Liquid Chromatography , 2004 .

[38]  J. Gebler,et al.  Two-dimensional separation of peptides using RP-RP-HPLC system with different pH in first and second separation dimensions. , 2005, Journal of separation science.

[39]  B. Simons,et al.  Performance characteristics of a new hybrid quadrupole time-of-flight tandem mass spectrometer (TripleTOF 5600). , 2011, Analytical chemistry.

[40]  Natalie Leys,et al.  Differential proteomic analysis using isotope‐coded protein‐labeling strategies: Comparison, improvements and application to simulated microgravity effect on Cupriavidus metallidurans CH34 , 2010, Proteomics.

[41]  F. Cross,et al.  Accurate quantitation of protein expression and site-specific phosphorylation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Dan Golick,et al.  Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures , 2009, Proteomics.

[43]  A. Schmidt,et al.  A novel strategy for quantitative proteomics using isotope‐coded protein labels , 2005, Proteomics.

[44]  Marc R Wilkins,et al.  Hares and tortoises: The high‐ versus low‐throughput proteomic race , 2009, Electrophoresis.

[45]  D. Chelius,et al.  Quantitative profiling of proteins in complex mixtures using liquid chromatography and mass spectrometry. , 2002, Journal of proteome research.

[46]  J. Thelen,et al.  The proteomic future: where mass spectrometry should be taking us. , 2012, The Biochemical journal.

[47]  M. Doherty,et al.  Proteomics moves from expression to turnover: update and future perspective , 2011, Expert review of proteomics.

[48]  Matthias Mann,et al.  Use of stable isotope labeling by amino acids in cell culture as a spike-in standard in quantitative proteomics , 2011, Nature Protocols.

[49]  M. Mann,et al.  Proteomics on an Orbitrap Benchtop Mass Spectrometer Using All-ion Fragmentation , 2010, Molecular & Cellular Proteomics.

[50]  G. D. de Jong,et al.  Comparison of monolithic and 1.8-μm RP-18 silica capillary columns using chromatographic data and mass spectrometric identification scores for proteins. , 2011, Journal of separation science.

[51]  J. Armengaud Microbiology and proteomics, getting the best of both worlds! , 2013, Environmental microbiology.

[52]  M. Mann,et al.  Stable isotope labeling by amino acids in cell culture (SILAC) applied to quantitative proteomics of Bacillus subtilis. , 2010, Journal of proteome research.

[53]  K. Sandra,et al.  Highly efficient peptide separations in proteomics Part 1. Unidimensional high performance liquid chromatography. , 2008, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[54]  F. McLafferty,et al.  Electron Capture Dissociation of Multiply Charged Protein Cations. A Nonergodic Process , 1998 .

[55]  Benito Cañas,et al.  Trends in sample preparation for classical and second generation proteomics. , 2007, Journal of chromatography. A.

[56]  Y. Oda,et al.  Evaluation of comprehensive multidimensional separations using reversed-phase, reversed-phase liquid chromatography/mass spectrometry for shotgun proteomics. , 2008, Journal of proteome research.

[57]  Sabine Bahn,et al.  Quantification of proteins using data‐independent analysis (MSE) in simple andcomplex samples: A systematic evaluation , 2011, Proteomics.

[58]  J. Kim,et al.  Quantitative proteomic analysis of cell wall and plasma membrane fractions from multidrug-resistant Acinetobacter baumannii. , 2011, Journal of proteome research.

[59]  K. Parker,et al.  Multiplexed Protein Quantitation in Saccharomyces cerevisiae Using Amine-reactive Isobaric Tagging Reagents*S , 2004, Molecular & Cellular Proteomics.

[60]  Andrew H. Thompson,et al.  Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. , 2003, Analytical chemistry.

[61]  M. Mann,et al.  Mass Spectrometry-based Proteomics Using Q Exactive, a High-performance Benchtop Quadrupole Orbitrap Mass Spectrometer* , 2011, Molecular & Cellular Proteomics.

[62]  Ludovic C. Gillet,et al.  Targeted Data Extraction of the MS/MS Spectra Generated by Data-independent Acquisition: A New Concept for Consistent and Accurate Proteome Analysis* , 2012, Molecular & Cellular Proteomics.

[63]  E. Marcotte,et al.  Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation , 2007, Nature Biotechnology.

[64]  D. Chelius,et al.  Identification and relative quantitation of protein mixtures by enzymatic digestion followed by capillary reversed-phase liquid chromatography-tandem mass spectrometry. , 2002, Analytical chemistry.

[65]  Reinout Raijmakers,et al.  Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics , 2009, Nature Protocols.

[66]  Rachel M. Adams,et al.  Systematic comparison of label-free, metabolic labeling, and isobaric chemical labeling for quantitative proteomics on LTQ Orbitrap Velos. , 2012, Journal of proteome research.

[67]  Adam Godzik,et al.  Shotgun metaproteomics of the human distal gut microbiota , 2008, The ISME Journal.

[68]  R. Graham,et al.  Microbial proteomics: a mass spectrometry primer for biologists , 2007, Microbial cell factories.

[69]  J. Langridge,et al.  A novel precursor ion discovery method on a hybrid quadrupole orthogonal acceleration time-of-flight (Q-TOF) mass spectrometer for studying protein phosphorylation , 2002, Journal of the American Society for Mass Spectrometry.

[70]  D. Raoult,et al.  Prospects for the future using genomics and proteomics in clinical microbiology. , 2011, Annual review of microbiology.

[71]  J. Garin,et al.  Isotope dilution strategies for absolute quantitative proteomics. , 2009, Journal of proteomics.

[72]  R. Carlson,et al.  Identification and imaging of peptides and proteins on Enterococcus faecalis biofilms by matrix assisted laser desorption ionization mass spectrometry. , 2012, The Analyst.

[73]  Samuel I. Miller,et al.  Precursor acquisition independent from ion count: how to dive deeper into the proteomics ocean. , 2009, Analytical chemistry.

[74]  F. Vandenesch,et al.  Isotope-labeled Protein Standards , 2007, Molecular & Cellular Proteomics.

[75]  Christopher T. Steichen,et al.  Proteomic Analysis of Neisseria gonorrhoeae Biofilms Shows Shift to Anaerobic Respiration and Changes in Nutrient Transport and Outermembrane Proteins , 2012, PloS one.

[76]  I. Smith,et al.  Protein dynamics in iron-starved Mycobacterium tuberculosis revealed by turnover and abundance measurement using hybrid-linear ion trap-Fourier transform mass spectrometry. , 2008, Analytical chemistry.

[77]  G. Smirnov,et al.  Possibilities and Limitations , 1970 .

[78]  M. Gorenstein,et al.  Absolute Quantification of Proteins by LCMSE , 2006, Molecular & Cellular Proteomics.

[79]  T. Mascher,et al.  Antibiotic research in the age of omics: from expression profiles to interspecies communication. , 2011, The Journal of antimicrobial chemotherapy.

[80]  K. Bunai,et al.  Quantitation of de novo localized (15)N-labeled lipoproteins and membrane proteins having one and two transmembrane segments in a Bacillus subtilis secA temperature-sensitive mutant using 2D-PAGE and MALDI-TOF MS. , 2005, Journal of proteome research.

[81]  Jens M. Rick,et al.  Quantitative mass spectrometry in proteomics: a critical review , 2007, Analytical and bioanalytical chemistry.

[82]  Konstantinos Thalassinos,et al.  A comparison of labeling and label-free mass spectrometry-based proteomics approaches. , 2009, Journal of proteome research.

[83]  H. Pakrasi,et al.  2D‐isolation of pure plasma and thylakoid membranes from the cyanobacterium Synechocystis sp. PCC 6803 , 1998, FEBS letters.

[84]  Albert J R Heck,et al.  Benchmarking stable isotope labeling based quantitative proteomics. , 2013, Journal of proteomics.

[85]  R. Aebersold,et al.  Selected reaction monitoring–based proteomics: workflows, potential, pitfalls and future directions , 2012, Nature Methods.

[86]  Matthias Mann,et al.  A Dual Pressure Linear Ion Trap Orbitrap Instrument with Very High Sequencing Speed* , 2009, Molecular & Cellular Proteomics.

[87]  J. Yates,et al.  Multidimensional LC separations in shotgun proteomics. , 2008, Analytical chemistry.

[88]  J. Bernhardt,et al.  Global relative and absolute quantitation in microbial proteomics. , 2012, Current opinion in microbiology.

[89]  P. Schrotz-King,et al.  Comparison of surface proteomes of enterotoxigenic (ETEC) and commensal Escherichia coli strains. , 2010, Journal of microbiological methods.

[90]  Linfeng Wu,et al.  Role of spectral counting in quantitative proteomics , 2010, Expert review of proteomics.

[91]  Martin Eisenacher,et al.  Peek a peak: a glance at statistics for quantitative label-free proteomics , 2010, Expert review of proteomics.

[92]  M. Gorenstein,et al.  The detection, correlation, and comparison of peptide precursor and product ions from data independent LC‐MS with data dependant LC‐MS/MS , 2009, Proteomics.

[93]  J. Langridge,et al.  Comparison of one- and two-dimensional liquid chromatography approaches in the label-free quantitative analysis of Methylocella silvestris. , 2012, Journal of proteome research.

[94]  J. Yates,et al.  A model for random sampling and estimation of relative protein abundance in shotgun proteomics. , 2004, Analytical chemistry.

[95]  R. Aebersold,et al.  Mass spectrometry-based proteomics , 2003, Nature.

[96]  C. Bessant,et al.  Free computational resources for designing selected reaction monitoring transitions , 2010, Proteomics.

[97]  D. Wolters,et al.  Bacterial membrane proteomics , 2008, Proteomics.

[98]  M. Selbach,et al.  Global analysis of cellular protein translation by pulsed SILAC , 2009, Proteomics.

[99]  Chris Hughes,et al.  Using ion mobility data to improve peptide identification: intrinsic amino acid size parameters. , 2011, Journal of proteome research.

[100]  R. Aebersold,et al.  Increased Selectivity, Analytical Precision, and Throughput in Targeted Proteomics , 2010, Molecular & Cellular Proteomics.

[101]  A. Makarov,et al.  The Orbitrap: a new mass spectrometer. , 2005, Journal of mass spectrometry : JMS.

[102]  E. Nägele,et al.  Optimization of two-dimensional off-line LC/MS separations to improve resolution of complex proteomic samples. , 2004, Analytical chemistry.

[103]  Richard D. Smith,et al.  Stable isotope-coded proteomic mass spectrometry. , 2003, Current opinion in biotechnology.

[104]  J. Bandow,et al.  Proteomic signatures in antibiotic research , 2011, Proteomics.

[105]  C. Nilsson,et al.  New separation tools for comprehensive studies of protein expression by mass spectrometry. , 2000, Mass spectrometry reviews.

[106]  Frank Fischer,et al.  Toward the Complete Membrane Proteome , 2006, Molecular & Cellular Proteomics.

[107]  Robert J Beynon,et al.  QconCATs: design and expression of concatenated protein standards for multiplexed protein quantification , 2012, Analytical and Bioanalytical Chemistry.

[108]  J. Yates,et al.  Large-scale analysis of the yeast proteome by multidimensional protein identification technology , 2001, Nature Biotechnology.

[109]  H. Christofk,et al.  A label‐free quantification method by MS/MS TIC compared to SILAC and spectral counting in a proteomics screen , 2008, Proteomics.

[110]  Henry H. N. Lam,et al.  Absolute quantification of microbial proteomes at different states by directed mass spectrometry , 2011, Molecular systems biology.

[111]  Mehdi Mirzaei,et al.  Less label, more free: Approaches in label‐free quantitative mass spectrometry , 2011, Proteomics.

[112]  Differential proteomic analysis of the response of Stenotrophomonas maltophilia to imipenem , 2012, Applied Microbiology and Biotechnology.

[113]  M. Mann,et al.  Exponentially Modified Protein Abundance Index (emPAI) for Estimation of Absolute Protein Amount in Proteomics by the Number of Sequenced Peptides per Protein*S , 2005, Molecular & Cellular Proteomics.

[114]  M. Goshe,et al.  Improving protein and proteome coverage through data-independent multiplexed peptide fragmentation. , 2010, Journal of proteome research.

[115]  R. Cohen,et al.  Isotope-coded Affinity Tag Approach to Identify and Quantify Oxidant-sensitive Protein Thiols* , 2004, Molecular & Cellular Proteomics.

[116]  Inge Jonassen,et al.  High accuracy mass spectrometry analysis as a tool to verify and improve gene annotation using Mycobacterium tuberculosis as an example , 2008, BMC Genomics.

[117]  Lingjun Li,et al.  Comparison of two-dimensional fractionation techniques for shotgun proteomics. , 2008, Analytical chemistry.

[118]  M. Mann,et al.  Large-scale Proteomic Analysis of the Human Spliceosome References , 2006 .

[119]  Masaru Tomita,et al.  One-dimensional capillary liquid chromatographic separation coupled with tandem mass spectrometry unveils the Escherichia coli proteome on a microarray scale. , 2010, Analytical chemistry.

[120]  M. Mann,et al.  Mass Spectrometry-based Proteomics Using Q Exactive, a High-performance Benchtop , 2011 .

[121]  R. Beynon,et al.  Multiplexed absolute quantification in proteomics using artificial QCAT proteins of concatenated signature peptides , 2005, Nature Methods.

[122]  S. Gygi,et al.  MS3 eliminates ratio distortion in isobaric labeling-based multiplexed quantitative proteomics , 2011, Nature Methods.

[123]  E. Duchoslav,et al.  Multiple reaction monitoring as a method for identifying protein posttranslational modifications. , 2005, Journal of biomolecular techniques : JBT.

[124]  K. Williams,et al.  Improved 2‐DE of microorganisms after acidic extraction , 2006, Electrophoresis.

[125]  C. Horváth,et al.  The role of liquid chromatography in proteomics. , 2004, Journal of chromatography. A.

[126]  M. Mann,et al.  More than 100,000 detectable peptide species elute in single shotgun proteomics runs but the majority is inaccessible to data-dependent LC-MS/MS. , 2011, Journal of proteome research.

[127]  S. Gygi,et al.  Quantitative analysis of complex protein mixtures using isotope-coded affinity tags , 1999, Nature Biotechnology.

[128]  R. Hettich,et al.  Microbial metaproteomics: identifying the repertoire of proteins that microorganisms use to compete and cooperate in complex environmental communities. , 2012, Current opinion in microbiology.

[129]  K. Reardon,et al.  Environmental proteomics: applications of proteome profiling in environmental microbiology and biotechnology. , 2008, Briefings in functional genomics & proteomics.

[130]  N. Anderson,et al.  Proteome and proteomics: New technologies, new concepts, and new words , 1998, Electrophoresis.

[131]  Phillip C. Wright,et al.  An insight into iTRAQ: where do we stand now? , 2012, Analytical and Bioanalytical Chemistry.

[132]  Jérôme Garin,et al.  Protein Standard Absolute Quantification (PSAQ) for improved investigation of staphylococcal food poisoning outbreaks , 2008, Proteomics.

[133]  Richard D. Smith,et al.  MicroSPE-nanoLC-ESI-MS/MS using 10-microm-i.d. silica-based monolithic columns for proteomics. , 2007, Analytical chemistry.

[134]  A. Chinnaiyan,et al.  Current affairs in quantitative targeted proteomics: multiple reaction monitoring-mass spectrometry. , 2009, Briefings in functional genomics & proteomics.