Dataset Information

Role of the Mycobacterium marinum ESX-1 Secretion System in Sliding Motility and Biofilm Formation.

ABSTRACT: Mycobacterium marinum is a close relative of Mycobacterium tuberculosis that can cause systemic tuberculosis-like infections in ectotherms and skin infections in humans. Sliding motility correlates with biofilm formation and virulence in most bacteria. In this study, we used a sliding motility assay to screen 2,304 transposon mutants of M. marinum NTUH-M6885 and identified five transposon mutants with decreased sliding motility. Transposons that interrupted the type VII secretion system (T7SS) ESX-1-related genes, espE (mmar_5439), espF (mmar_5440), and eccA1 (mmar_5443), were present in 3 mutants. We performed reverse-transcription polymerase chain reaction to verify genes from mmar_5438 to mmar_5450, which were found to belong to a single transcriptional unit. Deletion mutants of espE, espF, espG (mmar_5441), and espH (mmar_5442) displayed significant attenuation regarding sliding motility and biofilm formation. M. marinum NTUH-M6885 possesses a functional ESX-1 secretion system. However, deletion of espG or espH resulted in slightly decreased secretion of EsxB (which is also known as CFP-10). Thus, the M. marinum ESX-1 secretion system mediates sliding motility and is crucial for biofilm formation. These data provide new insight into M. marinum biofilm formation.

SUBMITTER: Lai LY

PROVIDER: S-EPMC5988883 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Role of the Mycobacterium marinum ESX-1 Secretion System in Sliding Motility and Biofilm Formation.

Lai Li-Yin LY Lin Tzu-Lung TL Chen Yi-Yin YY Hsieh Pei-Fang PF Wang Jin-Town JT

Frontiers in microbiology 20180530

Mycobacterium marinum is a close relative of Mycobacterium tuberculosis that can cause systemic tuberculosis-like infections in ectotherms and skin infections in humans. Sliding motility correlates with biofilm formation and virulence in most bacteria. In this study, we used a sliding motility assay to screen 2,304 transposon mutants of M. marinum NTUH-M6885 and identified five transposon mutants with decreased sliding motility. Transposons that interrupted the type VII secr ...[more]

PMID: 29899738

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Project description:Mycobacterium tuberculosis (Mtb) is transmitted through aerosols and primarily colonizes within the lung. The World Health Organization estimates that Mtb kills ~1.4 million people every year. A key aspect that makes Mtb such a successful pathogen is its ability to overcome iron limitation mounted by the host immune response. In our previous studies, we have shown that Mtb can utilize iron from heme, the largest source of iron in the human host, and that it uses two redundant heme utilization pathways. In this study, we show that the ESX-4 type VII secretion system (T7SS) is necessary for extracellular heme uptake into the Mtb cell through both heme utilization pathways. ESX-4 influences the secretion of the culture filtrate proteins Rv0125 and Rv1085c, which are also necessary for efficient heme utilization. We also discovered that deletion of the alternative sigma factor SigM significantly reduced Mtb heme utilization through both pathways and predict that SigM is a global positive regulator of core heme utilization genes of both pathways. Finally, we present the first direct evidence that some mycobacterial PPE (proline-proline-glutamate motif) proteins of the PPE protein family are pore-forming membrane proteins. Altogether, we identified core components of both Mtb Heme utilization pathways that were previously unknown and identified a novel channel-forming membrane protein of Mtb. IMPORTANCE M. tuberculosis (Mtb) is completely dependent on iron acquisition in the host to cause disease. The largest source of iron for Mtb in the human host is heme. Here, we show that the ancestral ESX-4 type VII secretion system is required for the efficient utilization of heme as a source of iron, which is an essential nutrient. This is another biological function identified for ESX-4 in Mtb, whose contribution to Mtb physiology is poorly understood. A most exciting finding is that some mycobacterial PPE (proline-proline-glutamate motif) proteins that have been implicated in the nutrient acquisition are membrane proteins that can form channels in a lipid bilayer. These observations have far-reaching implications because they support an emerging theme that PPE proteins can function as channel proteins in the outer mycomembrane for nutrient acquisition. Mtb has evolved a heme uptake system that is drastically different from all other known bacterial heme acquisition systems.

Project description:Mycobacterium marinum is a nontuberculous pathogen of poikilothermic fish and an opportunistic human pathogen. Like tuberculous mycobacteria, the M. marinum M strain requires the ESX-1 (ESAT-6 system 1) secretion system for virulence in host cells. EsxB and EsxA, two major virulence factors exported by the ESX-1 system, are encoded by the esxBA genes within the ESX-1 locus. Deletion of the esxBA genes abrogates ESX-1 export and attenuates M. marinum in ex vivo and in vivo models of infection. Interestingly, there are several duplications of the esxB and esxA genes (esxB_1, esxB_2, esxA_1, esxA_2, and esxA_3) in the M. marinum M genome located outside the ESX-1 locus. We sought to understand if this region, known as ESX-6, contributes to ESX-1-mediated virulence. We found that deletion of the esxB_1 gene alone or the entire ESX-6 locus did not impact ESX-1 export or function, supporting the idea that the esxBA genes present at the ESX-1 locus are the primary contributors to ESX-1-mediated virulence. Nevertheless, overexpression of the esxB_1 locus complemented ESX-1 function in the ΔesxBA strain, signifying that the two loci are functionally equivalent. Our findings raise questions about why duplicate versions of the esxBA genes are maintained in the M. marinum M genome and how these proteins, which are functionally equivalent to virulence factors, contribute to mycobacterial biology.IMPORTANCEMycobacterium tuberculosis is the causative agent of the human disease tuberculosis (TB). There are 10.4 million cases and 1.7 million TB-associated deaths annually, making TB a leading cause of death globally. Nontuberculous mycobacteria (NTM) cause chronic human infections that are acquired from the environment. Despite differences in disease etiology, both tuberculous and NTM pathogens use the ESX-1 secretion system to cause disease. The nontubercular mycobacterial species, Mycobacterium marinum, has additional copies of specific ESX-1 genes. Our findings demonstrate that the duplicated genes do not contribute to virulence but can substitute for virulence factors in M. marinum These findings suggest that the duplicated genes may play a specific role in NTM biology.

Dataset Information

Role of the Mycobacterium marinum ESX-1 Secretion System in Sliding Motility and Biofilm Formation.

Publications

Role of the <i>Mycobacterium marinum</i> ESX-1 Secretion System in Sliding Motility and Biofilm Formation.

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