Cryo-EM structure of the Mycobacterium smegmatis MmpL5-AcpM complex

ABSTRACT Mycobacterium tuberculosis, the causative agent of the airborne infection tuberculosis (TB), contains 13 mycobacterial membrane protein large (MmpL) transporters that can be divided into two distinct subclasses. These MmpL proteins play important functional roles within the mycobacterium an...

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Main Authors: Rakesh Maharjan, Zhemin Zhang, Philip A. Klenotic, William D. Gregor, Georgiana E. Purdy, Edward W. Yu
Format: Article
Language:English
Published: American Society for Microbiology 2024-12-01
Series:mBio
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Online Access:https://journals.asm.org/doi/10.1128/mbio.03035-24
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author Rakesh Maharjan
Zhemin Zhang
Philip A. Klenotic
William D. Gregor
Georgiana E. Purdy
Edward W. Yu
author_facet Rakesh Maharjan
Zhemin Zhang
Philip A. Klenotic
William D. Gregor
Georgiana E. Purdy
Edward W. Yu
author_sort Rakesh Maharjan
collection DOAJ
description ABSTRACT Mycobacterium tuberculosis, the causative agent of the airborne infection tuberculosis (TB), contains 13 mycobacterial membrane protein large (MmpL) transporters that can be divided into two distinct subclasses. These MmpL proteins play important functional roles within the mycobacterium and subsequently are considered attractive drug targets to combat TB infection. Previously, we reported both X-ray and cryo-electron microscopy (cryo-EM) structures of the MmpL3 transporter, providing high-resolution structural information for this subclass of the MmpL proteins. Thus far, there is no structural information available for the other subclass, which includes MmpL5, an inner membrane transporter that plays a critical role in iron hemostasis. Here, we report the first cryo-EM structure of the Mycobacterium smegmatis MmpL5 transporter bound with the meromycolate extension acyl carrier protein M (AcpM) to a resolution of 2.81 Å. Our structural data reveals that MmpL5 and AcpM interact in the cytoplasm to form a complex, and this allows us to propose that MmpL5 may also associate with the mycobactin L (MbtL) protein in a similar fashion to form a heterocomplex important for iron acquisition, which enables the survival and replication of the mycobacterium.IMPORTANCEThe emergence and spread of multidrug-resistant tuberculosis (TB) present enormous challenges to the global public health. The causative agent, Mycobacterium tuberculosis, has now infected more than one-third of the world's population. Here, we report the first structure of the mycobacterial membrane protein large 5 (MmpL5), an essential transporter for iron acquisition, bound with the meromycolate extension acyl carrier protein M (AcpM), indicating a plausible pathway for mycobactin translocation. Our studies will ultimately inform an era in structure-guided drug design to combat TB infection.
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spelling doaj-art-21c5aa30ccdd47e085f99cbabfb58f762025-08-20T01:58:59ZengAmerican Society for MicrobiologymBio2150-75112024-12-01151210.1128/mbio.03035-24Cryo-EM structure of the Mycobacterium smegmatis MmpL5-AcpM complexRakesh Maharjan0Zhemin Zhang1Philip A. Klenotic2William D. Gregor3Georgiana E. Purdy4Edward W. Yu5Department of Pharmacology, Case Western Reserve University School of Medicine, Cleveland, Ohio, USADepartment of Pharmacology, Case Western Reserve University School of Medicine, Cleveland, Ohio, USADepartment of Pharmacology, Case Western Reserve University School of Medicine, Cleveland, Ohio, USADepartment of Pharmacology, Case Western Reserve University School of Medicine, Cleveland, Ohio, USADepartment of Molecular Microbiology and Immunology, Oregon Health and Science University, Portland, Oregon, USADepartment of Pharmacology, Case Western Reserve University School of Medicine, Cleveland, Ohio, USAABSTRACT Mycobacterium tuberculosis, the causative agent of the airborne infection tuberculosis (TB), contains 13 mycobacterial membrane protein large (MmpL) transporters that can be divided into two distinct subclasses. These MmpL proteins play important functional roles within the mycobacterium and subsequently are considered attractive drug targets to combat TB infection. Previously, we reported both X-ray and cryo-electron microscopy (cryo-EM) structures of the MmpL3 transporter, providing high-resolution structural information for this subclass of the MmpL proteins. Thus far, there is no structural information available for the other subclass, which includes MmpL5, an inner membrane transporter that plays a critical role in iron hemostasis. Here, we report the first cryo-EM structure of the Mycobacterium smegmatis MmpL5 transporter bound with the meromycolate extension acyl carrier protein M (AcpM) to a resolution of 2.81 Å. Our structural data reveals that MmpL5 and AcpM interact in the cytoplasm to form a complex, and this allows us to propose that MmpL5 may also associate with the mycobactin L (MbtL) protein in a similar fashion to form a heterocomplex important for iron acquisition, which enables the survival and replication of the mycobacterium.IMPORTANCEThe emergence and spread of multidrug-resistant tuberculosis (TB) present enormous challenges to the global public health. The causative agent, Mycobacterium tuberculosis, has now infected more than one-third of the world's population. Here, we report the first structure of the mycobacterial membrane protein large 5 (MmpL5), an essential transporter for iron acquisition, bound with the meromycolate extension acyl carrier protein M (AcpM), indicating a plausible pathway for mycobactin translocation. Our studies will ultimately inform an era in structure-guided drug design to combat TB infection.https://journals.asm.org/doi/10.1128/mbio.03035-24Mycobacterial membrane protein LargeMmpL5acyl carrier protein Mmycobactin Lsiderophore exportiron acquisition
spellingShingle Rakesh Maharjan
Zhemin Zhang
Philip A. Klenotic
William D. Gregor
Georgiana E. Purdy
Edward W. Yu
Cryo-EM structure of the Mycobacterium smegmatis MmpL5-AcpM complex
mBio
Mycobacterial membrane protein Large
MmpL5
acyl carrier protein M
mycobactin L
siderophore export
iron acquisition
title Cryo-EM structure of the Mycobacterium smegmatis MmpL5-AcpM complex
title_full Cryo-EM structure of the Mycobacterium smegmatis MmpL5-AcpM complex
title_fullStr Cryo-EM structure of the Mycobacterium smegmatis MmpL5-AcpM complex
title_full_unstemmed Cryo-EM structure of the Mycobacterium smegmatis MmpL5-AcpM complex
title_short Cryo-EM structure of the Mycobacterium smegmatis MmpL5-AcpM complex
title_sort cryo em structure of the mycobacterium smegmatis mmpl5 acpm complex
topic Mycobacterial membrane protein Large
MmpL5
acyl carrier protein M
mycobactin L
siderophore export
iron acquisition
url https://journals.asm.org/doi/10.1128/mbio.03035-24
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