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Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism

Prokaryotic nanocompartments, also known as encapsulins, are a recently discovered proteinaceous organelle-like compartment in prokaryotes that compartmentalize cargo enzymes. While initial studies have begun to elucidate the structure and physiological roles of encapsulins, bioinformatic evidence s...

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Autores principales: Nichols, Robert J, LaFrance, Benjamin, Phillips, Naiya R, Radford, Devon R, Oltrogge, Luke M, Valentin-Alvarado, Luis E, Bischoff, Amanda J, Nogales, Eva, Savage, David F
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8049743/
https://www.ncbi.nlm.nih.gov/pubmed/33821786
http://dx.doi.org/10.7554/eLife.59288
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author Nichols, Robert J
LaFrance, Benjamin
Phillips, Naiya R
Radford, Devon R
Oltrogge, Luke M
Valentin-Alvarado, Luis E
Bischoff, Amanda J
Nogales, Eva
Savage, David F
author_facet Nichols, Robert J
LaFrance, Benjamin
Phillips, Naiya R
Radford, Devon R
Oltrogge, Luke M
Valentin-Alvarado, Luis E
Bischoff, Amanda J
Nogales, Eva
Savage, David F
author_sort Nichols, Robert J
collection PubMed
description Prokaryotic nanocompartments, also known as encapsulins, are a recently discovered proteinaceous organelle-like compartment in prokaryotes that compartmentalize cargo enzymes. While initial studies have begun to elucidate the structure and physiological roles of encapsulins, bioinformatic evidence suggests that a great diversity of encapsulin nanocompartments remains unexplored. Here, we describe a novel encapsulin in the freshwater cyanobacterium Synechococcus elongatus PCC 7942. This nanocompartment is upregulated upon sulfate starvation and encapsulates a cysteine desulfurase enzyme via an N-terminal targeting sequence. Using cryo-electron microscopy, we have determined the structure of the nanocompartment complex to 2.2 Å resolution. Lastly, biochemical characterization of the complex demonstrated that the activity of the cysteine desulfurase is enhanced upon encapsulation. Taken together, our discovery, structural analysis, and enzymatic characterization of this prokaryotic nanocompartment provide a foundation for future studies seeking to understand the physiological role of this encapsulin in various bacteria.
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spelling pubmed-80497432021-04-21 Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism Nichols, Robert J LaFrance, Benjamin Phillips, Naiya R Radford, Devon R Oltrogge, Luke M Valentin-Alvarado, Luis E Bischoff, Amanda J Nogales, Eva Savage, David F eLife Microbiology and Infectious Disease Prokaryotic nanocompartments, also known as encapsulins, are a recently discovered proteinaceous organelle-like compartment in prokaryotes that compartmentalize cargo enzymes. While initial studies have begun to elucidate the structure and physiological roles of encapsulins, bioinformatic evidence suggests that a great diversity of encapsulin nanocompartments remains unexplored. Here, we describe a novel encapsulin in the freshwater cyanobacterium Synechococcus elongatus PCC 7942. This nanocompartment is upregulated upon sulfate starvation and encapsulates a cysteine desulfurase enzyme via an N-terminal targeting sequence. Using cryo-electron microscopy, we have determined the structure of the nanocompartment complex to 2.2 Å resolution. Lastly, biochemical characterization of the complex demonstrated that the activity of the cysteine desulfurase is enhanced upon encapsulation. Taken together, our discovery, structural analysis, and enzymatic characterization of this prokaryotic nanocompartment provide a foundation for future studies seeking to understand the physiological role of this encapsulin in various bacteria. eLife Sciences Publications, Ltd 2021-04-06 /pmc/articles/PMC8049743/ /pubmed/33821786 http://dx.doi.org/10.7554/eLife.59288 Text en © 2021, Nichols et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Microbiology and Infectious Disease
Nichols, Robert J
LaFrance, Benjamin
Phillips, Naiya R
Radford, Devon R
Oltrogge, Luke M
Valentin-Alvarado, Luis E
Bischoff, Amanda J
Nogales, Eva
Savage, David F
Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism
title Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism
title_full Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism
title_fullStr Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism
title_full_unstemmed Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism
title_short Discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism
title_sort discovery and characterization of a novel family of prokaryotic nanocompartments involved in sulfur metabolism
topic Microbiology and Infectious Disease
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8049743/
https://www.ncbi.nlm.nih.gov/pubmed/33821786
http://dx.doi.org/10.7554/eLife.59288
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