Halobacterium salinarum NRC-1 PeptideAtlas: Toward Strategies for Targeted Proteomics and Improved Proteome CoverageClick to copy article linkArticle link copied!
- Phu T. Van
- Amy K. Schmid
- Nichole L. King
- Amardeep Kaur
- Min Pan
- Kenia Whitehead
- Tie Koide
- Marc T. Facciotti
- Young Ah Goo
- Eric W. Deutsch
- David J. Reiss
- Parag Mallick
- Nitin S. Baliga
Abstract

The relatively small numbers of proteins and fewer possible post-translational modifications in microbes provide a unique opportunity to comprehensively characterize their dynamic proteomes. We have constructed a PeptideAtlas (PA) covering 62.7% of the predicted proteome of the extremely halophilic archaeon Halobacterium salinarum NRC-1 by compiling approximately 636 000 tandem mass spectra from 497 mass spectrometry runs in 88 experiments. Analysis of the PA with respect to biophysical properties of constituent peptides, functional properties of parent proteins of detected peptides, and performance of different mass spectrometry approaches has highlighted plausible strategies for improving proteome coverage and selecting signature peptides for targeted proteomics. Notably, discovery of a significant correlation between absolute abundances of mRNAs and proteins has helped identify low abundance of proteins as the major limitation in peptide detection. Furthermore, we have discovered that iTRAQ labeling for quantitative proteomic analysis introduces a significant bias in peptide detection by mass spectrometry. Therefore, despite identifying at least one proteotypic peptide for almost all proteins in the PA, a context-dependent selection of proteotypic peptides appears to be the most effective approach for targeted proteomics.
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This article is cited by 37 publications.
- Jochen M. Schwenk, Gilbert S. Omenn, Zhi Sun, David S. Campbell, Mark S. Baker, Christopher M. Overall, Ruedi Aebersold, Robert L. Moritz, and Eric W. Deutsch . The Human Plasma Proteome Draft of 2017: Building on the Human Plasma PeptideAtlas from Mass Spectrometry and Complementary Assays. Journal of Proteome Research 2017, 16
(12)
, 4299-4310. https://doi.org/10.1021/acs.jproteome.7b00467
- Terry Farrah, Eric W. Deutsch, Michael R. Hoopmann, Janice L. Hallows, Zhi Sun, Chung-Ying Huang, and Robert L. Moritz . The State of the Human Proteome in 2012 as Viewed through PeptideAtlas. Journal of Proteome Research 2013, 12
(1)
, 162-171. https://doi.org/10.1021/pr301012j
- Douglas W. Mahoney, Terry M. Therneau, Carrie J. Heppelmann, LeeAnn Higgins, Linda M. Benson, Roman M. Zenka, Pratik Jagtap, Gary L. Nelsestuen, H. Robert Bergen, III, and Ann L. Oberg . Relative Quantification: Characterization of Bias, Variability and Fold Changes in Mass Spectrometry Data from iTRAQ-Labeled Peptides. Journal of Proteome Research 2011, 10
(9)
, 4325-4333. https://doi.org/10.1021/pr2001308
- Ákos Végvári and György Marko-Varga . Clinical Protein Science and Bioanalytical Mass Spectrometry with an Emphasis on Lung Cancer. Chemical Reviews 2010, 110
(5)
, 3278-3298. https://doi.org/10.1021/cr100011x
- Ulrike Kusebauch, Alan P. R. Lorenzetti, David S. Campbell, Min Pan, David Shteynberg, Charu Kapil, Mukul K. Midha, Adrián López García de Lomana, Nitin S. Baliga, Robert L. Moritz. A comprehensive spectral assay library to quantify the Halobacterium salinarum NRC-1 proteome by DIA/SWATH-MS. Scientific Data 2023, 10
(1)
https://doi.org/10.1038/s41597-023-02590-5
- Alan P. R. Lorenzetti, Ulrike Kusebauch, Lívia S. Zaramela, Wei-Ju Wu, João P. P. de Almeida, Serdar Turkarslan, Adrián L. G. de Lomana, José V. Gomes-Filho, Ricardo Z. N. Vêncio, Robert L. Moritz, Tie Koide, Nitin S. Baliga, . A Genome-Scale Atlas Reveals Complex Interplay of Transcription and Translation in an Archaeon. mSystems 2023, 8
(2)
https://doi.org/10.1128/msystems.00816-22
- Evelyn Ayumi Onga, Ricardo Z. N. Vêncio, Tie Koide. Low Salt Influences Archaellum-Based Motility, Glycerol Metabolism, and Gas Vesicles Biogenesis in Halobacterium salinarum. Microorganisms 2022, 10
(12)
, 2442. https://doi.org/10.3390/microorganisms10122442
- Ian S Yunus, Taek Soon Lee. Applications of targeted proteomics in metabolic engineering: advances and opportunities. Current Opinion in Biotechnology 2022, 75 , 102709. https://doi.org/10.1016/j.copbio.2022.102709
- Ricardo L. Couto-Rodriguez, Daniel Gal, Lana J. McMillan, Jin Koh, Sixue Chen, Julie A. Maupin-Furlow. Quantitative Mass Spectrometry by SILAC in Haloferax volcanii. 2022, 255-266. https://doi.org/10.1007/978-1-0716-2445-6_16
- J.A. Reales-Calderón, Z. Sun, V. Mascaraque, E. Pérez-Navarro, V. Vialás, E.W. Deutsch, R.L. Moritz, C. Gil, J.L. Martínez, G. Molero. A wide-ranging Pseudomonas aeruginosa PeptideAtlas build: A useful proteomic resource for a versatile pathogen. Journal of Proteomics 2021, 239 , 104192. https://doi.org/10.1016/j.jprot.2021.104192
- Stefan Schulze, Zachary Adams, Micaela Cerletti, Rosana De Castro, Sébastien Ferreira-Cerca, Christian Fufezan, María Inés Giménez, Michael Hippler, Zivojin Jevtic, Robert Knüppel, Georgio Legerme, Christof Lenz, Anita Marchfelder, Julie Maupin-Furlow, Roberto A. Paggi, Friedhelm Pfeiffer, Ansgar Poetsch, Henning Urlaub, Mechthild Pohlschroder. The Archaeal Proteome Project advances knowledge about archaeal cell biology through comprehensive proteomics. Nature Communications 2020, 11
(1)
https://doi.org/10.1038/s41467-020-16784-7
- Živojin Jevtić, Britta Stoll, Friedhelm Pfeiffer, Kundan Sharma, Henning Urlaub, Anita Marchfelder, Christof Lenz. The Response of
Haloferax volcanii
to Salt and Temperature Stress: A Proteome Study by Label‐Free Mass Spectrometry. PROTEOMICS 2019, 19
(20)
https://doi.org/10.1002/pmic.201800491
- Felipe Ten-Caten, Ricardo Z. N. Vêncio, Alan Péricles R. Lorenzetti, Livia Soares Zaramela, Ana Carolina Santana, Tie Koide. Internal RNAs overlapping coding sequences can drive the production of alternative proteins in archaea. RNA Biology 2018, 23 , 1-14. https://doi.org/10.1080/15476286.2018.1509661
- Lana J. McMillan, Sungmin Hwang, Rawan E. Farah, Jin Koh, Sixue Chen, Julie A. Maupin‐Furlow. Multiplex quantitative SILAC for analysis of archaeal proteomes: a case study of oxidative stress responses. Environmental Microbiology 2018, 20
(1)
, 385-401. https://doi.org/10.1111/1462-2920.14014
- Mar Martinez-Pastor, Peter D. Tonner, Cynthia L. Darnell, Amy K. Schmid. Transcriptional Regulation in Archaea: From Individual Genes to Global Regulatory Networks. Annual Review of Genetics 2017, 51
(1)
, 143-170. https://doi.org/10.1146/annurev-genet-120116-023413
- Gerald Losensky, Klaus Jung, Henning Urlaub, Felicitas Pfeifer, Sabrina Fröls, Christof Lenz. Shedding light on biofilm formation of
Halobacterium salinarum
R1 by SWATH‐LC/MS/MS analysis of planktonic and sessile cells. PROTEOMICS 2017, 17
(7)
https://doi.org/10.1002/pmic.201600111
- Keely A. Dulmage, Horia Todor, Amy K. Schmid, . Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein. mBio 2015, 6
(5)
https://doi.org/10.1128/mBio.00649-15
- Rafael Silva-Rocha, Marjorie Cornejo Pontelli, Gilvan Pessoa Furtado, Livia Soares Zaramela, Tie Koide, . Development of New Modular Genetic Tools for Engineering the Halophilic Archaeon Halobacterium salinarum. PLOS ONE 2015, 10
(6)
, e0129215. https://doi.org/10.1371/journal.pone.0129215
- Horia Todor, Keely Dulmage, Nicholas Gillum, James R. Bain, Michael J. Muehlbauer, Amy K. Schmid. A transcription factor links growth rate and metabolism in the hypersaline adapted archaeon
H
alobacterium salinarum. Molecular Microbiology 2014, 93
(6)
, 1172-1182. https://doi.org/10.1111/mmi.12726
- Vital Vialas, Zhi Sun, Carla Verónica Loureiro y Penha, Montserrat Carrascal, Joaquín Abián, Lucía Monteoliva, Eric W. Deutsch, Ruedi Aebersold, Robert L. Moritz, Concha Gil. A Candida albicans PeptideAtlas. Journal of Proteomics 2014, 97 , 62-68. https://doi.org/10.1016/j.jprot.2013.06.020
- Mónica V. Orellana, Wyming L. Pang, Pierre M. Durand, Kenia Whitehead, Nitin S. Baliga, . A Role for Programmed Cell Death in the Microbial Loop. PLoS ONE 2013, 8
(5)
, e62595. https://doi.org/10.1371/journal.pone.0062595
- Kimberly M. Webb, Jerry Yu, Courtney K. Robinson, Tomiya Noboru, Yuan C. Lee, Jocelyne DiRuggiero. Effects of intracellular Mn on the radiation resistance of the halophilic archaeon Halobacterium salinarum. Extremophiles 2013, 17
(3)
, 485-497. https://doi.org/10.1007/s00792-013-0533-9
- Neil Andrew D. Bascos. Protein and Proteome Resources. 2013, 1766-1769. https://doi.org/10.1007/978-1-4419-9863-7_1043
- Kriti Sharma, Nicholas Gillum, J Lomax Boyd, Amy Schmid. The RosR transcription factor is required for gene expression dynamics in response to extreme oxidative stress in a hypersaline-adapted archaeon. BMC Genomics 2012, 13
(1)
https://doi.org/10.1186/1471-2164-13-351
- Ann L Oberg, Douglas W Mahoney. Statistical methods for quantitative mass spectrometry proteomic experiments with labeling. BMC Bioinformatics 2012, 13
(S16)
https://doi.org/10.1186/1471-2105-13-S16-S7
- Fabio Rodrigues, Douglas Galante, Ivan G. Paulino-Lima, Rubens T.D. Duarte, Amancio C.S. Friaça, Claudia Lage, Eduardo Janot-Pacheco, Ramachrisna Teixeira, Jorge E. Horvath. Astrobiology in Brazil: early history and perspectives. International Journal of Astrobiology 2012, 11
(4)
, 189-202. https://doi.org/10.1017/S1473550412000250
- Keith Richardson, Richard Denny, Chris Hughes, John Skilling, Jacek Sikora, Michał Dadlez, Angel Manteca, Hye Ryung Jung, Ole Nørregaard Jensen, Virginie Redeker, Ronald Melki, James I. Langridge, Johannes P.C. Vissers. A Probabilistic Framework for Peptide and Protein Quantification from Data-Dependent and Data-Independent LC-MS Proteomics Experiments. OMICS: A Journal of Integrative Biology 2012, 16
(9)
, 468-482. https://doi.org/10.1089/omi.2012.0019
- Julie A Maupin-Furlow, Matthew A Humbard, Phillip Aaron Kirkland. Extreme challenges and advances in archaeal proteomics. Current Opinion in Microbiology 2012, 15
(3)
, 351-356. https://doi.org/10.1016/j.mib.2012.02.002
- Mónica Calderón-Santiago, José María Mata-Granados, Feliciano Priego-Capote, José Manuel Quesada-Gómez, María Dolores Luque de Castro. Analytical platform for verification and quantitation of target peptides in human serum: Application to cathelicidin. Analytical Biochemistry 2011, 415
(1)
, 39-45. https://doi.org/10.1016/j.ab.2011.04.005
- Lennart Martens. Proteomics Databases and Repositories. 2011, 213-227. https://doi.org/10.1007/978-1-60761-977-2_14
- Marc T Facciotti, Wyming L Pang, Fang-yin Lo, Kenia Whitehead, Tie Koide, Ken-ichi Masumura, Min Pan, Amardeep Kaur, David J Larsen, David J Reiss, Linh Hoang, Ewa Kalisiak, Trent Northen, Sunia A Trauger, Gary Siuzdak, Nitin S Baliga. Large scale physiological readjustment during growth enables rapid, comprehensive and inexpensive systems analysis. BMC Systems Biology 2010, 4
(1)
https://doi.org/10.1186/1752-0509-4-64
- Christian H. Ahrens, Erich Brunner, Ermir Qeli, Konrad Basler, Ruedi Aebersold. Generating and navigating proteome maps using mass spectrometry. Nature Reviews Molecular Cell Biology 2010, 11
(11)
, 789-801. https://doi.org/10.1038/nrm2973
- Parag Mallick, Bernhard Kuster. Proteomics: a pragmatic perspective. Nature Biotechnology 2010, 28
(7)
, 695-709. https://doi.org/10.1038/nbt.1658
- Peter R. Jungblut, Franziska Schiele, Ursula Zimny-Arndt, Renate Ackermann, Monika Schmid, Sabine Lange, Robert Stein, Klaus-Peter Pleissner. Helicobacter pylori
proteomics by 2-DE/MS, 1-DE-LC/MS and functional data mining. PROTEOMICS 2010, 10
(2)
, 182-193. https://doi.org/10.1002/pmic.200900361
- Eric W. Deutsch. The PeptideAtlas Project. 2010, 285-296. https://doi.org/10.1007/978-1-60761-444-9_19
- Andreas Tebbe, Alexander Schmidt, Kosta Konstantinidis, Michaela Falb, Birgit Bisle, Christian Klein, Michalis Aivaliotis, Josef Kellermann, Frank Siedler, Friedhelm Pfeiffer, Friedrich Lottspeich, Dieter Oesterhelt. Life‐style changes of a halophilic archaeon analyzed by quantitative proteomics. PROTEOMICS 2009, 9
(15)
, 3843-3855. https://doi.org/10.1002/pmic.200800944
- Tie Koide, David J Reiss, J Christopher Bare, Wyming Lee Pang, Marc T Facciotti, Amy K Schmid, Min Pan, Bruz Marzolf, Phu T Van, Fang‐Yin Lo, Abhishek Pratap, Eric W Deutsch, Amelia Peterson, Dan Martin, Nitin S Baliga. Prevalence of transcription promoters within archaeal operons and coding sequences. Molecular Systems Biology 2009, 5
(1)
https://doi.org/10.1038/msb.2009.42
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