A virus capsid-like nanocompartment that stores iron and protects bacteria from oxidative stress

Colleen A. McHugh, Juan Fontana, Daniel Nemecek, Naiqian Cheng, Anastasia A. Aksyuk, J. Bernard Heymann, Dennis C. Winkler, Alan S. Lam, Joseph S. Wall, Alasdair C. Steven, Egbert Hoiczyk

Research output: Contribution to journalArticle

Abstract

Living cells compartmentalize materials and enzymatic reactions to increase metabolic efficiency. While eukaryotes use membrane-bound organelles, bacteria and archaea rely primarily on protein-bound nanocompartments. Encapsulins constitute a class of nanocompartments widespread in bacteria and archaea whose functions have hitherto been unclear. Here, we characterize the encapsulin nanocompartment from Myxococcus xanthus, which consists of a shell protein (EncA, 32.5 kDa) and three internal proteins (EncB, 17 kDa; EncC, 13 kDa; EncD, 11 kDa). Using cryo-electron microscopy, we determined that EncA self-assembles into an icosahedral shell 32 nm in diameter (26 nm internal diameter), built from 180 subunits with the fold first observed in bacteriophage HK97 capsid. The internal proteins, of which EncB and EncC have ferritin-like domains, attach to its inner surface. Native nanocompartments have dense iron-rich cores. Functionally, they resemble ferritins, cage-like iron storage proteins, but with a massively greater capacity (∼30,000 iron atoms versus ∼3,000 in ferritin). Physiological data reveal that few nanocompartments are assembled during vegetative growth, but they increase fivefold upon starvation, protecting cells from oxidative stress through iron sequestration. Synopsis Bacteria compartmentalize by sequestering components into protein shells. Here, such a nanocompartment is shown to structurally resemble virus capsids and to store large amounts of iron for protection under starvation conditions. Iron homeostasis in Myxococcus xanthus involves iron sequestration into large protein shells (encapsulin nanocompartments). The shell is lined with adaptor proteins with ferritin-like folds that nucleate iron-rich granules. The encapsulin system appears to complement a ferritin system. The encapsulin shell closely resembles capsids of bacteriophages and herpesvirus. Thus, phages may have arisen from cellular genes, or M. xanthus may have acquired the encapsulin shell gene from a bacteriophage. Bacteria compartmentalize by sequestering components into protein shells. Here, such a nanocompartment is shown to structurally resemble virus capsids and to store large amounts of iron for protection under starvation conditions.

Original languageEnglish (US)
Pages (from-to)1896-1911
Number of pages16
JournalThe EMBO journal
Volume33
Issue number17
DOIs
StatePublished - Sep 1 2014

Fingerprint

Oxidative stress
Capsid
Viruses
Bacteria
Oxidative Stress
Iron
Ferritins
Bacteriophages
Myxococcus xanthus
Proteins
Starvation
Archaea
Genes
Cryoelectron Microscopy
Herpesviridae
Eukaryota
Organelles
Electron microscopy
Homeostasis
Cells

Keywords

  • cryo-electron microscopy
  • encapsulin
  • ferritin
  • HK97 fold
  • oxidative stress

ASJC Scopus subject areas

  • Molecular Biology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Neuroscience(all)

Cite this

McHugh, C. A., Fontana, J., Nemecek, D., Cheng, N., Aksyuk, A. A., Heymann, J. B., ... Hoiczyk, E. (2014). A virus capsid-like nanocompartment that stores iron and protects bacteria from oxidative stress. The EMBO journal, 33(17), 1896-1911. https://doi.org/10.15252/embj.201488566

A virus capsid-like nanocompartment that stores iron and protects bacteria from oxidative stress. / McHugh, Colleen A.; Fontana, Juan; Nemecek, Daniel; Cheng, Naiqian; Aksyuk, Anastasia A.; Heymann, J. Bernard; Winkler, Dennis C.; Lam, Alan S.; Wall, Joseph S.; Steven, Alasdair C.; Hoiczyk, Egbert.

In: The EMBO journal, Vol. 33, No. 17, 01.09.2014, p. 1896-1911.

Research output: Contribution to journalArticle

McHugh, CA, Fontana, J, Nemecek, D, Cheng, N, Aksyuk, AA, Heymann, JB, Winkler, DC, Lam, AS, Wall, JS, Steven, AC & Hoiczyk, E 2014, 'A virus capsid-like nanocompartment that stores iron and protects bacteria from oxidative stress', The EMBO journal, vol. 33, no. 17, pp. 1896-1911. https://doi.org/10.15252/embj.201488566
McHugh CA, Fontana J, Nemecek D, Cheng N, Aksyuk AA, Heymann JB et al. A virus capsid-like nanocompartment that stores iron and protects bacteria from oxidative stress. The EMBO journal. 2014 Sep 1;33(17):1896-1911. https://doi.org/10.15252/embj.201488566
McHugh, Colleen A. ; Fontana, Juan ; Nemecek, Daniel ; Cheng, Naiqian ; Aksyuk, Anastasia A. ; Heymann, J. Bernard ; Winkler, Dennis C. ; Lam, Alan S. ; Wall, Joseph S. ; Steven, Alasdair C. ; Hoiczyk, Egbert. / A virus capsid-like nanocompartment that stores iron and protects bacteria from oxidative stress. In: The EMBO journal. 2014 ; Vol. 33, No. 17. pp. 1896-1911.
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