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

Author:

Nichols Robert J1ORCID,LaFrance Benjamin1,Phillips Naiya R1ORCID,Radford Devon R2,Oltrogge Luke M1ORCID,Valentin-Alvarado Luis E3,Bischoff Amanda J4,Nogales Eva15678ORCID,Savage David F1ORCID

Affiliation:

1. Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

2. Department of Molecular Genetics, University of Toronto, Toronto, Canada

3. Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, United States

4. Department of Chemistry, University of California Berkeley, Berkeley, United States

5. Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States

6. Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, United States

7. California Institute for Quantitative Biosciences (QB3), University of California, Berkeley, Berkeley, United States

8. Molecular Biophysics and Integrated Bio-Imaging Division, Lawrence Berkeley National Laboratory, Berkeley, United States

Abstract

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.

Funder

U.S. Department of Energy

National Science Foundation

Howard Hughes Medical Institute

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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