Identification of novel lipid modifications and intermembrane dynamics in Corynebacterium glutamicum using high-resolution mass spectrometry

Stephan Klatt, Rajini Brammananth, Sean O’Callaghan, Konstantinos A. Kouremenos, Dedreia Tull, Paul K. Crellin, Ross L. Coppel, Malcolm J. McConville

Research output: Contribution to journalArticleResearchpeer-review

5 Citations (Scopus)

Abstract

The complex cell envelopes of Corynebacterineae contribute to the virulence of pathogenic species (such as Mycobacterium tuberculosis and Corynebacterium diphtheriae) and capacity of nonpathogenic species (such as Corynebacterium glutamicum) to grow in diverse niches. The Corynebacterineae cell envelope comprises an asymmetric outer membrane that overlays the arabinogalactan-peptidoglycan complex and the inner cell membrane. Dissection of the lipid composition of the inner and outer membrane fractions is important for understanding the biogenesis of this multilaminate wall structure. Here, we have undertaken the first high-resolution analysis of C. glutamicum inner and outer membrane lipids. We identified 28 lipid (sub)classes (>233 molecular species), including new subclasses of acylated/ acetylated trehalose mono/dicorynomycolic acids, using high-resolution LC/MS/MS coupled with mass spectral library searches in MS-DIAL. All lipid subclasses exhibited polarized distributions across the inner and outer membrane fractions generated by differential solvent extraction. Strikingly, deletion of the TmaT protein, which is required for transport of trehalose corynomycolates across the inner membrane, led to the accumulation of triacylglycerols in the inner membrane and to suppressed synthesis of phosphatidylglycerol and alanylated lipids. These analyses indicate unanticipated connectivity in the synthesis and/or transport of different lipid classes in C. glutamicum.—Klatt, S., R. Brammananth, S. O’Callaghan, K. A. Kouremenos, D. Tull, P. K. Crellin, R. L. Coppel, and M. J. McConville. Identification of novel lipid modifications and intermembrane dynamics in Corynebacterium glutamicum using high-resolution mass spectrometry.

Original languageEnglish
Pages (from-to)1190-1204
Number of pages15
JournalJournal of Lipid Research
Volume59
Issue number7
DOIs
Publication statusPublished - Jul 2018

Keywords

  • Bacterial membranes
  • Lipidomics
  • Mycobacterium
  • Trehalose lipids

Cite this

Klatt, Stephan ; Brammananth, Rajini ; O’Callaghan, Sean ; Kouremenos, Konstantinos A. ; Tull, Dedreia ; Crellin, Paul K. ; Coppel, Ross L. ; McConville, Malcolm J. / Identification of novel lipid modifications and intermembrane dynamics in Corynebacterium glutamicum using high-resolution mass spectrometry. In: Journal of Lipid Research. 2018 ; Vol. 59, No. 7. pp. 1190-1204.
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abstract = "The complex cell envelopes of Corynebacterineae contribute to the virulence of pathogenic species (such as Mycobacterium tuberculosis and Corynebacterium diphtheriae) and capacity of nonpathogenic species (such as Corynebacterium glutamicum) to grow in diverse niches. The Corynebacterineae cell envelope comprises an asymmetric outer membrane that overlays the arabinogalactan-peptidoglycan complex and the inner cell membrane. Dissection of the lipid composition of the inner and outer membrane fractions is important for understanding the biogenesis of this multilaminate wall structure. Here, we have undertaken the first high-resolution analysis of C. glutamicum inner and outer membrane lipids. We identified 28 lipid (sub)classes (>233 molecular species), including new subclasses of acylated/ acetylated trehalose mono/dicorynomycolic acids, using high-resolution LC/MS/MS coupled with mass spectral library searches in MS-DIAL. All lipid subclasses exhibited polarized distributions across the inner and outer membrane fractions generated by differential solvent extraction. Strikingly, deletion of the TmaT protein, which is required for transport of trehalose corynomycolates across the inner membrane, led to the accumulation of triacylglycerols in the inner membrane and to suppressed synthesis of phosphatidylglycerol and alanylated lipids. These analyses indicate unanticipated connectivity in the synthesis and/or transport of different lipid classes in C. glutamicum.—Klatt, S., R. Brammananth, S. O’Callaghan, K. A. Kouremenos, D. Tull, P. K. Crellin, R. L. Coppel, and M. J. McConville. Identification of novel lipid modifications and intermembrane dynamics in Corynebacterium glutamicum using high-resolution mass spectrometry.",
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Identification of novel lipid modifications and intermembrane dynamics in Corynebacterium glutamicum using high-resolution mass spectrometry. / Klatt, Stephan; Brammananth, Rajini; O’Callaghan, Sean; Kouremenos, Konstantinos A.; Tull, Dedreia; Crellin, Paul K.; Coppel, Ross L.; McConville, Malcolm J.

In: Journal of Lipid Research, Vol. 59, No. 7, 07.2018, p. 1190-1204.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Klatt, Stephan

AU - Brammananth, Rajini

AU - O’Callaghan, Sean

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AB - The complex cell envelopes of Corynebacterineae contribute to the virulence of pathogenic species (such as Mycobacterium tuberculosis and Corynebacterium diphtheriae) and capacity of nonpathogenic species (such as Corynebacterium glutamicum) to grow in diverse niches. The Corynebacterineae cell envelope comprises an asymmetric outer membrane that overlays the arabinogalactan-peptidoglycan complex and the inner cell membrane. Dissection of the lipid composition of the inner and outer membrane fractions is important for understanding the biogenesis of this multilaminate wall structure. Here, we have undertaken the first high-resolution analysis of C. glutamicum inner and outer membrane lipids. We identified 28 lipid (sub)classes (>233 molecular species), including new subclasses of acylated/ acetylated trehalose mono/dicorynomycolic acids, using high-resolution LC/MS/MS coupled with mass spectral library searches in MS-DIAL. All lipid subclasses exhibited polarized distributions across the inner and outer membrane fractions generated by differential solvent extraction. Strikingly, deletion of the TmaT protein, which is required for transport of trehalose corynomycolates across the inner membrane, led to the accumulation of triacylglycerols in the inner membrane and to suppressed synthesis of phosphatidylglycerol and alanylated lipids. These analyses indicate unanticipated connectivity in the synthesis and/or transport of different lipid classes in C. glutamicum.—Klatt, S., R. Brammananth, S. O’Callaghan, K. A. Kouremenos, D. Tull, P. K. Crellin, R. L. Coppel, and M. J. McConville. Identification of novel lipid modifications and intermembrane dynamics in Corynebacterium glutamicum using high-resolution mass spectrometry.

KW - Bacterial membranes

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