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Determination of the collision cross sections of cardiolipins and phospholipids from Pseudomonas aeruginosa by traveling wave ion mobility spectrometry-mass spectrometry using a novel correction strategy

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Abstract

Collision cross section (CCS) values are descriptors of the 3D structure of ions which can be determined by ion mobility spectrometry (IMS). Currently, most lipidomic studies involving CCS value determination concern eukaryote samples (e.g. human, bovine) and to a lower extent prokaryote samples (e.g. bacteria). Here, we report CCS values obtained from traveling wave ion mobility spectrometry (TWCCSN2) measurements from the bacterial membrane of Pseudomonas aeruginosa—a bacterium ranked as priority 1 for the R&D of new antibiotics by the World Health Organization. In order to cover the lack of reference compounds which could cover the m/z and CCS ranges of the membrane lipids of P. aeruginosa, three calibrants (polyalanine, dextran and phospholipids) were used for the TWCCSN2 calibration. A shift from the published lipid CCS values was systematically observed (ΔCCS% up to 9%); thus, we proposed a CCS correction strategy. This correction strategy allowed a reduction in the shift (ΔCCS%) between our measurements and published values to less than 2%. This correction was then applied to determine the CCS values of Pseudomonas aeruginosa lipids which have not been published yet. As a result, 32 TWCCSN2 values for [M+H]+ ions and 24 TWCCSN2 values for [M−H]− ions were obtained for four classes of phospholipids (phosphatidylethanolamines (PE), phosphatidylcholines (PC), phosphatidylglycerols (PG) and diphosphatidylglycerols—known as cardiolipins (CL)).

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References

  1. Obritsch MD, Fish DN, MacLaren R, Jung R. Nosocomial infections due to multidrug-resistant Pseudomonas aeruginosa: epidemiology and treatment options. Pharmacotherapy. 2005;25(10):11.

    Article  Google Scholar 

  2. Curran CS, Bolig T, Torabi-Parizi P. Mechanisms and targeted therapies for Pseudomonas aeruginosa lung infection. Am J Respir Crit Care Med. 2018;197(6):708–27. https://doi.org/10.1164/rccm.201705-1043SO.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis. 2018;18(3):318–27. https://doi.org/10.1016/s1473-3099(17)30753-3.

    Article  PubMed  Google Scholar 

  4. Bassetti M, Vena A, Croxatto A, Righi E, Guery B. How to manage Pseudomonas aeruginosa infections. Drugs Context. 2018;7:212527. https://doi.org/10.7573/dic.212527.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Escriba PV. Membrane-lipid therapy: a new approach in molecular medicine. Trends Mol Med. 2006;12(1):34–43. https://doi.org/10.1016/j.molmed.2005.11.004.

    Article  CAS  PubMed  Google Scholar 

  6. Gaviard C, Jouenne T, Hardouin J. Proteomics of Pseudomonas aeruginosa: the increasing role of post-translational modifications. Expert Rev Proteomics. 2018;15(9):757–72. https://doi.org/10.1080/14789450.2018.1516550.

    Article  CAS  PubMed  Google Scholar 

  7. Kamath KS, Krisp C, Chick J, Pascovici D, Gygi SP, Molloy MP. Pseudomonas aeruginosa proteome under hypoxic stress conditions mimicking the cystic fibrosis lung. J Proteome Res. 2017;16(10):3917–28. https://doi.org/10.1021/acs.jproteome.7b00561.

    Article  CAS  PubMed  Google Scholar 

  8. Hare NJ, Solis N, Harmer C, Marzook NB, Rose B, Harbour C, et al. Proteomic profiling of Pseudomonas aeruginosa AES-1R, PAO1 and PA14 reveals potential virulence determinants associated with a transmissible cystic fibrosis-associated strain. BMC Microbiol. 2012;12:16. https://doi.org/10.1186/1471-2180-12-16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Benamara H, Rihouey C, Abbes I, Mlouka MAB, Hardouin J, Jouenne T, et al. Characterization of membrane lipidome changes in Pseudomonas aeruginosa during biofilm growth on glass wool. PloS One. 2014;9(9):9. https://doi.org/10.1371/journal.pone.0108478.g001.

    Article  Google Scholar 

  10. Benamara H, Rihouey C, Jouenne T, Alexandre S. Impact of the biofilm mode of growth on the inner membrane phospholipid composition and lipid domains in Pseudomonas aeruginosa. Biochim Biophys Acta. 2011;1808(1):98–105. https://doi.org/10.1016/j.bbamem.2010.09.004.

    Article  CAS  PubMed  Google Scholar 

  11. Ewing MA, Glover MS, Clemmer DE. Hybrid ion mobility and mass spectrometry as a separation tool. J Chromatogr A. 2016;1439:3–25. https://doi.org/10.1016/j.chroma.2015.10.080.

    Article  CAS  PubMed  Google Scholar 

  12. Cumeras R, Figueras E, Davis CE, Baumbach JI, Gracia I. Review on ion mobility spectrometry. Part 1: current instrumentation. Analyst. 2015;140(5):1376–90. https://doi.org/10.1039/c4an01100g.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Gabelica V, Marklund E. Fundamentals of ion mobility spectrometry. Curr Opin Chem Biol. 2018;42:51–9. https://doi.org/10.1016/j.cbpa.2017.10.022.

    Article  CAS  PubMed  Google Scholar 

  14. Plante PL, Francovic-Fontaine E, May JC, McLean JA, Baker ES, Laviolette F, et al. Predicting ion mobility collision cross-sections using a deep neural network: DeepCCS. Anal Chem. 2019;91(8):5191–9. https://doi.org/10.1021/acs.analchem.8b05821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Zhou Z, Tu J, Xiong X, Shen X, Zhu ZJ. LipidCCS: prediction of collision cross-section values for lipids with high precision to support ion mobility-mass spectrometry-based lipidomics. Anal Chem. 2017;89(17):9559–66. https://doi.org/10.1021/acs.analchem.7b02625.

    Article  CAS  PubMed  Google Scholar 

  16. Smith DP, Knapman TW, Campuzano I, Malham RW, Berryman JT, Radford SE, et al. Deciphering drift time measurements from travelling wave ion mobility spectrometry-mass spectrometry studies. Eur J Mass Spectrom (Chichester). 2009;15(2):113–30. https://doi.org/10.1255/ejms.947.

    Article  CAS  Google Scholar 

  17. Paglia G, Astarita G. Metabolomics and lipidomics using traveling-wave ion mobility-mass spectrometry. Nat Protoc. 2017;12(4):17. https://doi.org/10.1038/nprot.2017.013.

    Article  CAS  Google Scholar 

  18. Paglia G, Kliman M, Claude E, Geromanos S, Astarita G. Applications of ion-mobility mass spectrometry for lipid analysis. Anal Bioanal Chem. 2015;407:12.

    Article  Google Scholar 

  19. Paglia G, Williams JP, Menikarachchi L, Thompson JW, Tyldesley-Worster R, Halldorsson S, et al. Ion mobility derived collision cross sections to support metabolomics applications. Anal Chem. 2014;86(8):3985–93. https://doi.org/10.1021/ac500405x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hines KM, May JC, McLean JA, Xu L. Evaluation of collision cross section calibrants for structural analysis of lipids by traveling wave ion mobility-mass spectrometry. Anal Chem. 2016;88(14):7329–36. https://doi.org/10.1021/acs.analchem.6b01728.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Levy AJ, Oranzi NR, Ahmadireskety A, Kemperman RHJ, Wei MS, Yost RA. Recent progress in metabolomics using ion mobility-mass spectrometry. TrAC Trends Anal Chem. 2019;116:274–81. https://doi.org/10.1016/j.trac.2019.05.001.

    Article  CAS  Google Scholar 

  22. Tejada-Casado C, Hernandez-Mesa M, Monteau F, Lara FJ, Olmo-Iruela MD, Garcia-Campana AM, et al. Collision cross section (CCS) as a complementary parameter to characterize human and veterinary drugs. Anal Chim Acta. 2018;1043:52–63. https://doi.org/10.1016/j.aca.2018.09.065.

    Article  CAS  PubMed  Google Scholar 

  23. May JC, Morris CB, McLean JA. Ion mobility collision cross section compendium. Anal Chem. 2017;89(2):1032–44. https://doi.org/10.1021/acs.analchem.6b04905.

    Article  CAS  PubMed  Google Scholar 

  24. Schrimpe-Rutledge AC, Sherrod SD, McLean JA. Improving the discovery of secondary metabolite natural products using ion mobility-mass spectrometry. Curr Opin Chem Biol. 2018;42:160–6. https://doi.org/10.1016/j.cbpa.2017.12.004.

    Article  CAS  PubMed  Google Scholar 

  25. Hines KM, Xu L. Lipidomic consequences of phospholipid synthesis defects in Escherichia coli revealed by HILIC-ion mobility-mass spectrometry. Chem Phys Lipids. 2019;219:15–22. https://doi.org/10.1016/j.chemphyslip.2019.01.007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zheng X, Aly NA, Zhou Y, Dupuis KT, Bilbao A, Paurus VL, et al. A structural examination and collision cross section database for over 500 metabolites and xenobiotics using drift tube ion mobility spectrometry. Chem Sci. 2017;8(11):7724–36. https://doi.org/10.1039/c7sc03464d.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ridenour WB, Kliman M, McLean JA, Caprioli RM. Structural characterization of phospholipids and peptides directly from tissue sections by MALDI traveling-wave ion mobility-mass spectrometry. Anal Chem. 2010;82(5):1881–9. https://doi.org/10.1021/ac9026115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Jackson SN, Ugarov M, Post JD, Egan T, Langlais D, Schultz JA, et al. A study of phospholipids by ion mobility TOFMS. J Am Soc Mass Spectrom. 2008;19(11):1655–62. https://doi.org/10.1016/j.jasms.2008.07.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Harris RA, Leaptrot KL, May JC, McLean JA. New frontiers in lipidomics analyses using structurally selective ion mobility-mass spectrometry. TrAC Trends Anal Chem. 2019;116:316–23. https://doi.org/10.1016/j.trac.2019.03.031.

    Article  CAS  Google Scholar 

  30. Hinz C, Liggi S, Griffin JL. The potential of ion mobility mass spectrometry for high-throughput and high-resolution lipidomics. Curr Opin Chem Biol. 2018;42:42–50. https://doi.org/10.1016/j.cbpa.2017.10.018.

    Article  CAS  PubMed  Google Scholar 

  31. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37(8):7.

    Article  Google Scholar 

  32. Hofmann J, Struwe WB, Scarff CA, Scrivens JH, Harvey DJ, Pagel K. Estimating collision cross sections of negatively charged N-glycans using traveling wave ion mobility-mass spectrometry. Anal Chem. 2014;86(21):10789–95. https://doi.org/10.1021/ac5028353.

    Article  CAS  PubMed  Google Scholar 

  33. Pagel K, Harvey DJ. Ion mobility-mass spectrometry of complex carbohydrates: collision cross sections of sodiated N-linked glycans. Anal Chem. 2013;85(10):5138–45. https://doi.org/10.1021/ac400403d.

    Article  CAS  PubMed  Google Scholar 

  34. Bush MF, Campuzano ID, Robinson CV. Ion mobility mass spectrometry of peptide ions: effects of drift gas and calibration strategies. Anal Chem. 2012;84(16):7124–30. https://doi.org/10.1021/ac3014498.

    Article  CAS  PubMed  Google Scholar 

  35. Domalain V, Hubert-Roux M, Tognetti V, Joubert L, Lange CM, Rouden J, et al. Enantiomeric differentiation of aromatic amino acids using traveling wave ion mobility-mass spectrometry. Chem Sci. 2014;5(8):3234–9. https://doi.org/10.1039/c4sc00443d.

    Article  CAS  Google Scholar 

  36. Garrett TA, Kordestani R, Raetz CRH. Quantification of cardiolipin by liquid chromatography-electrospray ionization mass spectrometry. Method. Enzymol. 2007;433:213–30. https://doi.org/10.1016/s0076-6879(07)33012-7.

  37. Liebisch G, Vizcaino JA, Kofeler H, Trotzmuller M, Griffiths WJ, Schmitz G, et al. Shorthand notation for lipid structures derived from mass spectrometry. J Lipid Res. 2013;54(6):1523–30. https://doi.org/10.1194/jlr.M033506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Groessl M, Graf S, Knochenmuss R. High resolution ion mobility-mass spectrometry for separation and identification of isomeric lipids. Analyst. 2015;140(20):6904–11. https://doi.org/10.1039/c5an00838g.

    Article  CAS  PubMed  Google Scholar 

  39. Leaptrot KL, May JC, Dodds JN, McLean JA. Ion mobility conformational lipid atlas for high confidence lipidomics. Nat Commun. 2019;10(1):985. https://doi.org/10.1038/s41467-019-08897-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Chao J, Wolfaardt GM, Arts MT. Characterization of Pseudomonas aeruginosa fatty acid profiles in biofilms and batch planktonic cultures. Can J Microbiol. 2010;56(12):1028–39. https://doi.org/10.1139/W10-093.

    Article  CAS  PubMed  Google Scholar 

  41. Schlame M. Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes. J Lipid Res. 2008;49(8):1607–20. https://doi.org/10.1194/jlr.R700018-JLR200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kim HI, Kim H, Pang ES, Ryu EK, Beegle LW, Loo JA, et al. Structural characterization of unsaturated phosphatidylcholines using traveling wave ion mobility spectrometry. Anal Chem. 2009;81(20):8289–97. https://doi.org/10.1021/ac900672a.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. El Khoury M, Swain J, Sautrey G, Zimmermann L, Van Der Smissen P, Décout J-L, et al. Targeting bacterial cardiolipin enriched microdomains: an antimicrobial strategy used by amphiphilic aminoglycoside antibiotics. Sci Rep. 2017;7(1). https://doi.org/10.1038/s41598-017-10543-3.

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Funding

The authors gratefully acknowledge European Regional Development Fund (ERDF, no. HN0001343), Labex SynOrg (ANR-11-LABX-0029) and Région Normandie for their financial support.

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Authors and Affiliations

  1. Normandie Univ, COBRA, UMR 6014 and FR 3038, Université de Rouen, INSA de Rouen, CNRS, IRCOF, 1 rue Tesnière, 76821, Mont-Saint-Aignan Cedex, France

    Estelle Deschamps, Isabelle Schmitz-Afonso, Corinne Loutelier-Bourhis & Carlos Afonso

  2. Normandie Univ, PBS, UMR 6270 and FR 3038, Université de Rouen, INSA de Rouen, CNRS, CURIB, 25 Rue Lucien Tesnière, 76821, Mont-Saint-Aignan Cedex, France

    Estelle Deschamps, Annick Schaumann, Emmanuelle Dé & Stéphane Alexandre

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  1. Estelle Deschamps
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Deschamps, E., Schmitz-Afonso, I., Schaumann, A. et al. Determination of the collision cross sections of cardiolipins and phospholipids from Pseudomonas aeruginosa by traveling wave ion mobility spectrometry-mass spectrometry using a novel correction strategy. Anal Bioanal Chem 411, 8123–8131 (2019). https://doi.org/10.1007/s00216-019-02194-2

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