Probe into a multi-protein prokaryotic organelle using thermal scanning assay reveals distinct properties of the core and the shell.


Journal

Biochimica et biophysica acta. General subjects
ISSN: 1872-8006
Titre abrégé: Biochim Biophys Acta Gen Subj
Pays: Netherlands
ID NLM: 101731726

Informations de publication

Date de publication:
10 2020
Historique:
received: 07 02 2020
revised: 26 06 2020
accepted: 29 06 2020
pubmed: 8 7 2020
medline: 15 12 2020
entrez: 8 7 2020
Statut: ppublish

Résumé

Bacterial microcompartments represent the only reported category of prokaryotic organelles that are capable of functioning as independent bioreactors. In this organelle, a biochemical pathway with all the enzyme machinery is encapsulated within an all protein shell. The shell proteins and the enzymes have distinct structural features. It is hypothesized that flat shell proteins align sideways to form extended sheets and, the globular enzymes fill up the central core of the organelle. Using differential scanning fluorimetry, we explored the structure and functional alteration of Pdu BMC, involving tertiary or quaternary structures. Our findings exhibit that these intact BMCs as a whole behave similar to a globular protein with a rich hydrophobic core, which is exposed upon thermal insult. The encapsulated enzymes itself have a strong hydrophobic core, which is in line with the hydrophobic-collapse model of protein folding. The shell proteins, on the other hand, do not have a strong hydrophobic core and show a significant portion of exposed hydrophobic patches. We show for the first time the thermal unfolding profile of the BMC domain proteins and the unique exposure of hydrophobic patches in them might be required for anchoring the enzymes leading to better packaging of the micro-compartments. These observations indicate that the genesis of these unique bacterial organelles is driven by the hydrophobic interactions between the shell and the enzymes. Insights from this work will aid in the genetic and biochemical engineering of thermostable efficient enzymatic biomaterials.

Sections du résumé

BACKGROUND
Bacterial microcompartments represent the only reported category of prokaryotic organelles that are capable of functioning as independent bioreactors. In this organelle, a biochemical pathway with all the enzyme machinery is encapsulated within an all protein shell. The shell proteins and the enzymes have distinct structural features. It is hypothesized that flat shell proteins align sideways to form extended sheets and, the globular enzymes fill up the central core of the organelle.
METHODS
Using differential scanning fluorimetry, we explored the structure and functional alteration of Pdu BMC, involving tertiary or quaternary structures.
RESULTS
Our findings exhibit that these intact BMCs as a whole behave similar to a globular protein with a rich hydrophobic core, which is exposed upon thermal insult. The encapsulated enzymes itself have a strong hydrophobic core, which is in line with the hydrophobic-collapse model of protein folding. The shell proteins, on the other hand, do not have a strong hydrophobic core and show a significant portion of exposed hydrophobic patches.
CONCLUSION
We show for the first time the thermal unfolding profile of the BMC domain proteins and the unique exposure of hydrophobic patches in them might be required for anchoring the enzymes leading to better packaging of the micro-compartments.
GENERAL SIGNIFICANCE
These observations indicate that the genesis of these unique bacterial organelles is driven by the hydrophobic interactions between the shell and the enzymes. Insights from this work will aid in the genetic and biochemical engineering of thermostable efficient enzymatic biomaterials.

Identifiants

pubmed: 32634534
pii: S0304-4165(20)30192-6
doi: 10.1016/j.bbagen.2020.129680
pii:
doi:

Substances chimiques

Bacterial Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

129680

Informations de copyright

Copyright © 2020 Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Auteurs

Naimat K Bari (NK)

Chemical Biology Unit, Institute of Nano Science and Technology, Habitat Centre, Sector- 64, Mohali, Punjab 160062, India.

Jagadish P Hazra (JP)

Department of Chemical Sciences, Indian Institute of Science Education and Research (IISER), Mohali, Knowledge City, Sector 81, Mohali, Punjab 140306, India.

Gaurav Kumar (G)

Chemical Biology Unit, Institute of Nano Science and Technology, Habitat Centre, Sector- 64, Mohali, Punjab 160062, India.

Simerpreet Kaur (S)

Chemical Biology Unit, Institute of Nano Science and Technology, Habitat Centre, Sector- 64, Mohali, Punjab 160062, India.

Sharmistha Sinha (S)

Chemical Biology Unit, Institute of Nano Science and Technology, Habitat Centre, Sector- 64, Mohali, Punjab 160062, India. Electronic address: sinhas@inst.ac.in.

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Classifications MeSH