Cargando…
The encapsulin from Thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein
Bacterial nanocompartments, also known as encapsulins, are an emerging class of protein-based ‘organelles’ found in bacteria and archaea. Encapsulins are virus-like icosahedral particles comprising a ~ 25–50 nm shell surrounding a specific cargo enzyme. Compartmentalization is thought to create a un...
Autores principales: | , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8610991/ https://www.ncbi.nlm.nih.gov/pubmed/34815415 http://dx.doi.org/10.1038/s41598-021-01932-w |
_version_ | 1784603210221092864 |
---|---|
author | LaFrance, Benjamin J. Cassidy-Amstutz, Caleb Nichols, Robert J. Oltrogge, Luke M. Nogales, Eva Savage, David F. |
author_facet | LaFrance, Benjamin J. Cassidy-Amstutz, Caleb Nichols, Robert J. Oltrogge, Luke M. Nogales, Eva Savage, David F. |
author_sort | LaFrance, Benjamin J. |
collection | PubMed |
description | Bacterial nanocompartments, also known as encapsulins, are an emerging class of protein-based ‘organelles’ found in bacteria and archaea. Encapsulins are virus-like icosahedral particles comprising a ~ 25–50 nm shell surrounding a specific cargo enzyme. Compartmentalization is thought to create a unique chemical environment to facilitate catalysis and isolate toxic intermediates. Many questions regarding nanocompartment structure–function remain unanswered, including how shell symmetry dictates cargo loading and to what extent the shell facilitates enzymatic activity. Here, we explore these questions using the model Thermotoga maritima nanocompartment known to encapsulate a redox-active ferritin-like protein. Biochemical analysis revealed the encapsulin shell to possess a flavin binding site located at the interface between capsomere subunits, suggesting the shell may play a direct and active role in the function of the encapsulated cargo. Furthermore, we used cryo-EM to show that cargo proteins use a form of symmetry-matching to facilitate encapsulation and define stoichiometry. In the case of the Thermotoga maritima encapsulin, the decameric cargo protein with fivefold symmetry preferentially binds to the pentameric-axis of the icosahedral shell. Taken together, these observations suggest the shell is not simply a passive barrier—it also plays a significant role in the structure and function of the cargo enzyme. |
format | Online Article Text |
id | pubmed-8610991 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-86109912021-11-24 The encapsulin from Thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein LaFrance, Benjamin J. Cassidy-Amstutz, Caleb Nichols, Robert J. Oltrogge, Luke M. Nogales, Eva Savage, David F. Sci Rep Article Bacterial nanocompartments, also known as encapsulins, are an emerging class of protein-based ‘organelles’ found in bacteria and archaea. Encapsulins are virus-like icosahedral particles comprising a ~ 25–50 nm shell surrounding a specific cargo enzyme. Compartmentalization is thought to create a unique chemical environment to facilitate catalysis and isolate toxic intermediates. Many questions regarding nanocompartment structure–function remain unanswered, including how shell symmetry dictates cargo loading and to what extent the shell facilitates enzymatic activity. Here, we explore these questions using the model Thermotoga maritima nanocompartment known to encapsulate a redox-active ferritin-like protein. Biochemical analysis revealed the encapsulin shell to possess a flavin binding site located at the interface between capsomere subunits, suggesting the shell may play a direct and active role in the function of the encapsulated cargo. Furthermore, we used cryo-EM to show that cargo proteins use a form of symmetry-matching to facilitate encapsulation and define stoichiometry. In the case of the Thermotoga maritima encapsulin, the decameric cargo protein with fivefold symmetry preferentially binds to the pentameric-axis of the icosahedral shell. Taken together, these observations suggest the shell is not simply a passive barrier—it also plays a significant role in the structure and function of the cargo enzyme. Nature Publishing Group UK 2021-11-23 /pmc/articles/PMC8610991/ /pubmed/34815415 http://dx.doi.org/10.1038/s41598-021-01932-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article LaFrance, Benjamin J. Cassidy-Amstutz, Caleb Nichols, Robert J. Oltrogge, Luke M. Nogales, Eva Savage, David F. The encapsulin from Thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein |
title | The encapsulin from Thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein |
title_full | The encapsulin from Thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein |
title_fullStr | The encapsulin from Thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein |
title_full_unstemmed | The encapsulin from Thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein |
title_short | The encapsulin from Thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein |
title_sort | encapsulin from thermotoga maritima is a flavoprotein with a symmetry matched ferritin-like cargo protein |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8610991/ https://www.ncbi.nlm.nih.gov/pubmed/34815415 http://dx.doi.org/10.1038/s41598-021-01932-w |
work_keys_str_mv | AT lafrancebenjaminj theencapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT cassidyamstutzcaleb theencapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT nicholsrobertj theencapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT oltroggelukem theencapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT nogaleseva theencapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT savagedavidf theencapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT lafrancebenjaminj encapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT cassidyamstutzcaleb encapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT nicholsrobertj encapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT oltroggelukem encapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT nogaleseva encapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein AT savagedavidf encapsulinfromthermotogamaritimaisaflavoproteinwithasymmetrymatchedferritinlikecargoprotein |