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Polyketide Quinones Are Alternate Intermediate Electron Carriers during Mycobacterial Respiration in Oxygen-Deficient Niches.

ABSTRACT: Mycobacterium tuberculosis (Mtb) adaptation to hypoxia is considered crucial to its prolonged latent persistence in humans. Mtb lesions are known to contain physiologically heterogeneous microenvironments that bring about differential responses from bacteria. Here we exploit metabolic variability within biofilm cells to identify alternate respiratory polyketide quinones (PkQs) from both Mycobacterium smegmatis (Msmeg) and Mtb. PkQs are specifically expressed in biofilms and other oxygen-deficient niches to maintain cellular bioenergetics. Under such conditions, these metabolites function as mobile electron carriers in the respiratory electron transport chain. In the absence of PkQs, mycobacteria escape from the hypoxic core of biofilms and prefer oxygen-rich conditions. Unlike the ubiquitous isoprenoid pathway for the biosynthesis of respiratory quinones, PkQs are produced by type III polyketide synthases using fatty acyl-CoA precursors. The biosynthetic pathway is conserved in several other bacterial genomes, and our study reveals a redox-balancing chemicocellular process in microbial physiology.

SUBMITTER: Anand A

PROVIDER: S-EPMC6051517 | biostudies-literature | 2015 Nov

REPOSITORIES: biostudies-literature

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Polyketide Quinones Are Alternate Intermediate Electron Carriers during Mycobacterial Respiration in Oxygen-Deficient Niches.

Anand Amitesh A Verma Priyanka P Singh Anil Kumar AK Kaushik Sandeep S Pandey Rajesh R Shi Ce C Kaur Harneet H Chawla Manbeena M Elechalawar Chandra Kumar CK Kumar Dhirendra D Yang Yong Y Bhavesh Neel S NS Banerjee Rajkumar R Dash Debasis D Singh Amit A Natarajan Vivek T VT Ojha Anil K AK Aldrich Courtney C CC Gokhale Rajesh S RS

Molecular cell 20151112 4

Mycobacterium tuberculosis (Mtb) adaptation to hypoxia is considered crucial to its prolonged latent persistence in humans. Mtb lesions are known to contain physiologically heterogeneous microenvironments that bring about differential responses from bacteria. Here we exploit metabolic variability within biofilm cells to identify alternate respiratory polyketide quinones (PkQs) from both Mycobacterium smegmatis (Msmeg) and Mtb. PkQs are specifically expressed in biofilms and other oxygen-deficien ...[more]

PMID: 26585386

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Project description:Long-distance electron transfer in marine environments couples physically separated redox half-reactions, impacting biogeochemical cycles of iron, sulfur and carbon. Bacterial bio-electrochemical systems that facilitate electron transfer via conductive filaments or across man-made electrodes are well-known, but the impact of abiotic currents across naturally occurring conductive and semiconductive minerals is poorly understood. In this paper I use cyclic voltammetry to explore electron transfer between electrodes made of common iron minerals (magnetite, hematite, pyrite, pyrrhotite, mackinawite, and greigite), and hydroquinones-a class of organic molecules found in carbon-rich sediments. Of all tested minerals, only pyrite and magnetite showed an increase in electric current in the presence of organic molecules, with pyrite showing excellent electrocatalytic performance. Pyrite electrodes performed better than commercially available glassy carbon electrodes and showed higher peak currents, lower overpotential values and a smaller separation between oxidation and reduction peaks for each tested quinone. Hydroquinone oxidation on pyrite surfaces was reversible, diffusion controlled, and stable over a large number of potential cycles. Given the ubiquity of both pyrite and quinones, abiotic electron transfer between minerals and organic molecules is likely widespread in Nature and may contribute to several different phenomena, including anaerobic respiration of a wide variety of microorganisms in temporally anoxic zones or in the proximity of hydrothermal vent chimneys, as well as quinone cycling and the propagation of anoxic zones in organic rich waters. Finally, interactions between pyrite and quinones make use of electrochemical gradients that have been suggested as an important source of energy for the origins of life on Earth. Ubiquinones and iron sulfide clusters are common redox cofactors found in electron transport chains across all domains of life and interactions between quinones and pyrite might have been an early analog of these ubiquitous systems.

Dataset Information

Polyketide Quinones Are Alternate Intermediate Electron Carriers during Mycobacterial Respiration in Oxygen-Deficient Niches.

Publications

Polyketide Quinones Are Alternate Intermediate Electron Carriers during Mycobacterial Respiration in Oxygen-Deficient Niches.

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