Lipidomic discovery of deoxysiderophores reveals a revised mycobactin biosynthesis pathway in Mycobacterium tuberculosis
Open accessAbstract
To measure molecular changes underlying pathogen adaptation, we generated a searchable dataset of more than 12,000 mass spectrometry events, corresponding to lipids and small molecules that constitute a lipidome for Mycobacterium tuberculosis. Iron is essential for M. tuberculosis survival, and the organism imports this metal using mycobactin and carboxymycobactin siderophores. Detection of an unexpected siderophore variant and deletions of genes for iron scavenging has led to a revised mycobactin biosynthesis model. An organism-wide search of the M. tuberculosis database for hypothetical compounds predicted by this model led to the discovery of two families of previously unknown lipids, designated monodeoxymycobactins and monodeoxycarboxymycobactins. These molecules suggest a revised biosynthetic model that alters the substrates and order of action of enzymes through the mycobactin biosynthetic pathway. We tested this model genetically by solving M. tuberculosis lipidomes after deletion of the iron-dependent regulator (ideR), mycobactin synthase B (mbtB), or mycobactin synthase G (mbtG). These studies show that deoxymycobactins are actively regulated during iron starvation, and also define essential roles of MbtG in converting deoxymycobactins to mycobactin and in promoting M. tuberculosis growth. Thus, lipidomics is an efficient discovery tool that informs genetic relationships, leading to a revised general model for the biosynthesis of these virulence-conferring siderophores.
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Mycobacteria acquire iron through multiple avenues including acquisition from transferrin via the endocytic pathway, by directly binding iron-loaded transferrin via specific receptors, by uptake of cytoplasmic iron or heme iron by specific transporters, or by production of siderophores such as mycobactin.
“Mycobacteria acquire iron through multiple avenues including the acquisition of the metal from transferrin via the endocytic pathway, by directly binding iron-loaded transferrin via specific receptors, by uptake of cytoplasmic iron or heme iron by specific transporters, or by the production of siderophores such as mycobactin, which can bind iron and re-utilize the metal (174–177).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [175]
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Targeted Lipidomics of Mycobacterial Lipids and Glycolipids
Layre, E. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1460-0_24 · Cited by 2 · see citing works
Self-citationMaier, A., Fast, D., Sakalo, D., Mguni, L. M., & Tischler, D. (2025) · ChemBioChem · doi:10.1002/cbic.202500574 · Cited by 1 · see citing works
Lipidomic Analysis of Lower Organisms
Řezanka, T., Kolouchová, I., Gharwalová, L., Palyzová, A., & Sigler, K. (2018) · Springer eBooks · doi:10.1007/978-3-319-54529-5_3-1 · Cited by 1 · see citing works
Examination of the SigC regulon and cobalamin biosynthesis in Mycobacterium tuberculosis
Grosse-Siestrup, B. T. (2012) · Cited by 1 · see citing works
Prithviraj, M., Kado, T., Mayfield, J. A., Young, D. C., Huang, A. D., Motooka, D., Nakamura, S., Siegrist, M. S., Moody, D. B., & Morita, Y. S. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.17.504266
Self-citationMapping unsolved lipidomes accelerates lipid discovery in major bacterial pathogensPreprint
Nair, Y. M., Menon, A. R., Lin, Z., Vossenberg, M. R. L., Munsamy, V., Young, D. C., Xet-Mull, A. M., Babunovic, G. H., Cheng, T., Raman, S., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.06.685907 · Cited by 1 · see citing works
Self-citation
- Authors
- Madigan, C. A., Cheng, T.-Y., Layre, E., Young, D. C., McConnell, M. J., Debono, C. A., Murry, J. P., Wei, J.-R., Barry, C. E., Rodriguez, G. M., Matsunaga, I., Rubin, E. J., & Moody, D. B.
- Affiliations
- Brigham and Women's Hospital (US)
- Harvard University (US)
- National Institute of Allergy and Infectious Diseases (US)
- Public Health Research Institute Center and Department of Medicine, University of Medicine and Dentistry of New Jersey, Newark, NJ 07103; and
- Kyoto University (JP)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-01-09
- Volume
- 109
- Issue
- 4
- Pages
- 1257-1262
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3268331
- OpenAlex
- W2062910696
- Cited by
- 65
- References
- 28
- Citations by year
- 2025: 2 · 2024: 3 · 2023: 3 · 2022: 1 · 2021: 3 · 2020: 2 · 2019: 5 · 2018: 6 · 2017: 1 · 2016: 8 · 2015: 8 · 2014: 12 · 2013: 5 · 2012: 6
- FWCI
- 6.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (R01AI044856, R01AI071155, U19AI076217, R01AI071881)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR 048632, R01AR048632)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Health Sciences › Medicine › Pharmacology › Microbial Natural Products and Biosynthesis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Mycobacterium tuberculosis, siderophores, lipidomics, iron acquisition, iron starvation, IdeR, virulence factors, lipidome
- MeSH terms
- Chromatography, High Pressure Liquid, Iron, Lipids, Models, Biological, Mycobacterium tuberculosis, Oxazoles, Mass Spectrometry, Databases, Factual, Siderophores, DNA Primers, Biosynthetic Pathways
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