Goals and Challenges in Bacterial Phosphoproteomics
Abstract
:1. Introduction
2. Bacterial Ser/Thr/Tyr Phosphoproteomics
2.1. Gel-Based Analyses
2.2. LC-MS/MS-Based Phosphoproteomic Analyses
2.2.1. Bacterial Ser/Thr/Tyr Nonquantitative LC-MS/MS-Based Phosphoproteomic Analyses
2.2.2. Bacterial Ser/Thr/Tyr LC-MS/MS-Based Quantitative Phosphoproteomic Analyses
3. Bacterial Proteins and Pathways Modulated by Ser/Thr/Tyr Phosphorylation
3.1. Bacterial Proteins Identified as Phosphorylated
3.2. Bacterial Ser/Thr/Tyr Phosphorylation Motifs
3.3. Bacterial Processes Demonstrated to be Modulated by Ser/Thr/Tyr Phosphorylation
4. Bacterial Histidine Protein Phosphorylation
4.1. Methodological Challenges
4.2. Bacterial Pathways Modulated by Histidine Phosphorylation
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
LC-MS/MS | liquid chromatography tandem mass spectrometry |
IMAC | immobilised metal affinity chromatography |
CPP | calcium phosphate precipitation |
SILAC | stable isotope labelling by amino acids in cell culture |
TMT | tandem mass tag |
sMRM | scheduled multiple reaction monitoring |
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Bacterium | Year | pSer (%) | pThr (%) | pTyr (%) | Reference |
---|---|---|---|---|---|
Bacillus subtillis | 2007 | 69.2 | 20.5 | 10.3 | [8] |
Escherichia coli (E. coli) | 2008 | 68 | 23 | 9 | [9] |
Lactococcus lactis | 2008 | 46.5 | 50.6 | 2.7 | [10] |
Klebsiella pneumoniae | 2009 | 31.2 | 15.1 | 25.8 | [7] |
Pseudomonas aeruginosa/putida | 2009 | 52.8 | 36.1 | 11.1 | [11] |
Halobacterium salinarum | 2009 | 84 | 16 | 0 | [12] |
Mycobacterium tuberculosis | 2010 | 40 | 60 | 0 | [3] |
Streptomyces coelicolor | 2010 | 34 | 52 | 14 | [13] |
Streptococcus pneumoniae | 2010 | 47 | 44 | 9 | [14] |
Bacillus subtilis | 2010 | n.r. | n.r. | n.r. | [15] |
Neisseria meningitidis | 2011 | n.r. | n.r. | n.r. | [16] |
Streptomyces coelicolor | 2011 | 46.8 | 48 | 5.2 | [17] |
Listeria monocytogenes | 2011 | 93 | 43 | 7 | [18] |
Helicobacter pylori | 2011 | 42.8 | 38.7 | 18.5 | [19] |
Clostridium acetobutylicum | 2012 | 40 | 50 | 10 | [20] |
Rhodopseudomonas palustris (Ch) | 2012 | 63.3 | 16.1 | 19.4 | [21] |
Thermus thermophilus | 2012 | 65.3 | 26 | 8.7 | [22] |
Thermus thermophilus | 2013 | 57 | 36 | 7 | [23] |
Synechococcus sp. | 2013 | 43.9 | 42.44 | 13.66 | [24] |
E. coli | 2013 | 75.9 | 16.7 | 7.4 | [25] |
Staphylococcus aureus | 2014 | n.r. | n.r. | n.r. | [26] |
Acinetobacter baumanii Abh12O-A2 | 2014 | 71.8 | 25.2 | 3.8 | [27] |
Acinetobacter baumanii ATCC 17879 | 2014 | 68.9 | 24.1 | 5.2 | [27] |
Pseudomonas aeruginosa | 2014 | 49 | 24 | 27 | [28] |
Listeria monocytogenes | 2014 | 64 | 31 | 5 | [29] |
Saccharopolyspora erythraea | 2014 | 47 | 45 | 8 | [30] |
Bacillus subtilis | 2014 | 74.6 | 18.6 | 7.3 | [31] |
Chlamydia caviae | 2015 | n.r. | n.r. | n.r. | [32] |
Sinorhizobium meliloti | 2015 | 63 | 28 | 5 | [33] |
E. coli | 2015 | n.r. | n.r. | n.r. | [34] |
Bacillus subtilis | 2015 | n.r. | n.r. | 22.6 | [35] |
Synechocystis sp. | 2015 | n.r. | n.r. | n.r. | [36] |
Acinetobacter baumannii SK17-S | 2016 | 47 | 27.6 | 12.4 | [6] |
Acinetobacter baumannii SK17-R | 2016 | 41.4 | 29.5 | 17.5 | [6] |
Mycobacterium smegmatis | 2017 | 27.79 | 73.97 | 1.24 | [37] |
Mycobacterium tuberculosis | 2017 | 68 | 29 | 3 | [38] |
Microcystis aeruginosa | 2018 | n.r | n.r. | n.r. | [39] |
Streptomyces coelicolor | 2018 | 50.6 | 47.4 | 2 | [40] |
Zymomonas mobilis | 2019 | 73 | 21 | 6 | [41] |
Streptococcus thermophilus | 2019 | 43 | 33 | 23 | [42] |
Average | 55.9 | 34.1 | 9.9 |
Bacterium | Year | Phosphoproteins | Phosphorylation Sites | Phosphoproteome | Reference |
---|---|---|---|---|---|
Neisseria meningitidis | 2011 | 51 | n.r. | Many biological processes | [16] |
Staphylococcus aureus | 2014 | 103 | 76 | Pathogenicity and virulence | [26] |
Chlamydia caviae (elementary body) | 2015 | 42 | n.r. | Virulence | [32] |
Chlamydia caviae (reticulate body) | 2015 | 34 | n.r. | Virulence | [32] |
Bacterium | Year | Phosphoproteins | Phosphorylation Sites | Phosphoproteome | Reference |
---|---|---|---|---|---|
Bacillus subtilis | 2007 | 78 | 78 | Carbohydrate metabolism | [8] |
E. coli | 2008 | 79 | 81 | Similar to Bacillus | [9] |
Lactococcus lactis | 2008 | 63 | 79 | Over-representation of phosphothreonines | [10] |
Klebsiella pneumoniae | 2009 | 81 | 93 | Capsular biosynthesis | [7] |
Pseudomonas aeruginosa | 2009 | 39 | 61 | Motility, transport and pathogenicity | [11] |
Pseudomonas putida | 2009 | 59 | 55 | Several biochemical pathways | [11] |
Halobacterium salinarum | 2009 | 26 | 31 | Phosphoproteome in Archaea | [12] |
Mycobacterium tuberculosis | 2010 | 301 | 500 | Several biochemical pathways | [3] |
Streptomyces coelicolor | 2010 | 40 | 46 | Housekeeping proteins | [13] |
Streptococcus pneumoniae | 2010 | 84 | 163 | Carbon/protein/nucleotide metabolisms, cell cycle and division | [14] |
Listeria monocytogenes | 2011 | 112 | 143 | Virulence, translation, carbohydrate metabolism and stress response | [18] |
Helicobacter pylori | 2011 | 67 | 126 | Virulence | [19] |
Clostridium acetobutylicum | 2012 | 61 | 107 | Carbon metabolism | [20] |
Rhodopseudomonas palustris (Ch) | 2012 | 54 | 63 | Carbon metabolism | [21] |
Rhodopseudomonas palustris (Ph) | 2012 | 42 | 59 | Carbon metabolism | [21] |
Thermus thermophilus | 2012 | 48 | 46 | Wide variety of cellular processes | [22] |
Thermus thermophilus | 2013 | 53 | 67 | Central metabolic pathways and protein/cell envelope biosynthesis | [23] |
Synechococcus sp. | 2013 | 245 | 410 | Two-component signalling pathway and photosynthesis | [24] |
Acinetobacter baumanii Abh12O-A2 | 2014 | 70 | 80 | Pathogenicity and drug resistance | [27] |
Acinetobacter baumanii ATCC 17879 | 2014 | 41 | 48 | Several biochemical pathways | [27] |
Pseudomonas aeruginosa | 2014 | 28 | 59 | Extracellular virulence factors | [28] |
Sinorhizobium meliloti | 2015 | 77 | 96 | Rhizobial adaptation | [33] |
Microcystis aeruginosa (nontoxic) | 2018 | 37 | n.r. | Several biochemical pathways | [39] |
Microcystis aeruginosa (toxic) | 2018 | 18 | n.r. | Regulation of toxin generation | [39] |
Bacterium | Year | Phosphoproteins | Phosphorylation Sites | Phosphoproteome | Method | Reference |
---|---|---|---|---|---|---|
Bacillus subtilis | 2010 | 27 | 45 | Phosphoproteome changes in different media | SILAC | [15] |
Streptomyces coelicolor | 2011 | 127 | 289 | Sporulation factors, transcriptional regulators, protein kinases and other regulatory proteins | Label-free | [17] |
E. coli | 2013 | 133 | 108 | Stationary phase | SILAC | [25] |
Bacillus subtilis | 2014 | 141 | 177 | Stationary phase | SILAC | [31] |
Listeria monocytogenes | 2014 | 191 | 242 | Purine biosynthesis regulated by PrfA phosphorylation | SILAC | [29] |
Saccharopolyspora erythraea | 2014 | 88 | 109 | Carbon metabolism, environmental stress and protein synthesis affected by phosphorylation | SRM | [30] |
E. coli | 2015 | 71 | n.r. | Phosphorylation varied during development | SRM | [34] |
Bacillus subtilis | 2015 | 124 | 155 | Spore-specific determinants | Label-free | [35] |
Synechocystis sp. | 2015 | 188 | 262 | Increased phosphorylation during nitrogen limitation | Dimethyl | [36] |
Acinetobacter baumannii SK17-S | 2016 | 248 | 410 | Antibiotic resistance | Label-free | [6] |
Acinetobacter baumannii SK17-R | 2016 | 211 | 285 | Antibiotic resistance | Label-free | [6] |
Mycobacterium smegmatis | 2017 | 154 | 224 | Transmembrane proteins | Label-free | [37] |
Mycobacterium tuberculosis | 2017 | 257 | 512 | Virulence | Tandem mass tag (TMT) | [38] |
Streptomyces coelicolor | 2018 | 48 | 85 | Regulatory proteins | TMT | [40] |
Zymomonas mobilis | 2019 | 125 | 177 | N2 fixing regulated by phosphorylation | Label-free | [41] |
Streptococcus thermophilus | 2019 | 106 | 161 | Divisome proteins phosphorylated by the PknB kinase | Dimethyl | [42] |
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Yagüe, P.; Gonzalez-Quiñonez, N.; Fernández-García, G.; Alonso-Fernández, S.; Manteca, A. Goals and Challenges in Bacterial Phosphoproteomics. Int. J. Mol. Sci. 2019, 20, 5678. https://doi.org/10.3390/ijms20225678
Yagüe P, Gonzalez-Quiñonez N, Fernández-García G, Alonso-Fernández S, Manteca A. Goals and Challenges in Bacterial Phosphoproteomics. International Journal of Molecular Sciences. 2019; 20(22):5678. https://doi.org/10.3390/ijms20225678
Chicago/Turabian StyleYagüe, Paula, Nathaly Gonzalez-Quiñonez, Gemma Fernández-García, Sergio Alonso-Fernández, and Angel Manteca. 2019. "Goals and Challenges in Bacterial Phosphoproteomics" International Journal of Molecular Sciences 20, no. 22: 5678. https://doi.org/10.3390/ijms20225678