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Title: MamO Is a Repurposed Serine Protease that Promotes Magnetite Biomineralization through Direct Transition Metal Binding in Magnetotactic Bacteria

Abstract

Many living organisms transform inorganic atoms into highly ordered crystalline materials. An elegant example of such biomineralization processes is the production of nano-scale magnetic crystals in magnetotactic bacteria. Previous studies have implicated the involvement of two putative serine proteases, MamE and MamO, during the early stages of magnetite formation in Magnetospirillum magneticum AMB-1. Here, using genetic analysis and X-ray crystallography, we show that MamO has a degenerate active site, rendering it incapable of protease activity. Instead, MamO promotes magnetosome formation through two genetically distinct, noncatalytic activities: activation of MamE-dependent proteolysis of biomineralization factors and direct binding to transition metal ions. By solving the structure of the protease domain bound to a metal ion, we identify a surface-exposed di-histidine motif in MamO that contributes to metal binding and show that it is required to initiate biomineralization in vivo. Finally, we find that pseudoproteases are widespread in magnetotactic bacteria and that they have evolved independently in three separate taxa. In conclusion, our results highlight the versatility of protein scaffolds in accommodating new biochemical activities and provide unprecedented insight into the earliest stages of biomineralization.

Authors:
 [1];  [2];  [3];  [1];  [1];  [4];  [5];  [6];  [7]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  2. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cellular Biology; Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division
  4. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry
  5. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cellular Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division; Univ. of California, Berkeley, CA (United States). Dept. of Chemistry
  6. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cellular Biology; Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division
  7. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cellular Biology; Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences
Publication Date:
Research Org.:
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1253997
Alternate Identifier(s):
OSTI ID: 1379123; OSTI ID: 1379160
Grant/Contract Number:  
AC02-05CH11231; MR‐15‐328599; R01GM084122; N000141310421
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
PLoS biology (Online)
Additional Journal Information:
Journal Name: PLoS biology (Online); Journal Volume: 14; Journal Issue: 3; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Hershey, David M., Ren, Xuefeng, Melnyk, Ryan A., Browne, Patrick J., Ozyamak, Ertan, Jones, Stephanie R., Chang, Michelle C. Y., Hurley, James H., and Komeili, Arash. MamO Is a Repurposed Serine Protease that Promotes Magnetite Biomineralization through Direct Transition Metal Binding in Magnetotactic Bacteria. United States: N. p., 2016. Web. doi:10.1371/journal.pbio.1002402.
Hershey, David M., Ren, Xuefeng, Melnyk, Ryan A., Browne, Patrick J., Ozyamak, Ertan, Jones, Stephanie R., Chang, Michelle C. Y., Hurley, James H., & Komeili, Arash. MamO Is a Repurposed Serine Protease that Promotes Magnetite Biomineralization through Direct Transition Metal Binding in Magnetotactic Bacteria. United States. doi:10.1371/journal.pbio.1002402.
Hershey, David M., Ren, Xuefeng, Melnyk, Ryan A., Browne, Patrick J., Ozyamak, Ertan, Jones, Stephanie R., Chang, Michelle C. Y., Hurley, James H., and Komeili, Arash. Wed . "MamO Is a Repurposed Serine Protease that Promotes Magnetite Biomineralization through Direct Transition Metal Binding in Magnetotactic Bacteria". United States. doi:10.1371/journal.pbio.1002402. https://www.osti.gov/servlets/purl/1253997.
@article{osti_1253997,
title = {MamO Is a Repurposed Serine Protease that Promotes Magnetite Biomineralization through Direct Transition Metal Binding in Magnetotactic Bacteria},
author = {Hershey, David M. and Ren, Xuefeng and Melnyk, Ryan A. and Browne, Patrick J. and Ozyamak, Ertan and Jones, Stephanie R. and Chang, Michelle C. Y. and Hurley, James H. and Komeili, Arash},
abstractNote = {Many living organisms transform inorganic atoms into highly ordered crystalline materials. An elegant example of such biomineralization processes is the production of nano-scale magnetic crystals in magnetotactic bacteria. Previous studies have implicated the involvement of two putative serine proteases, MamE and MamO, during the early stages of magnetite formation in Magnetospirillum magneticum AMB-1. Here, using genetic analysis and X-ray crystallography, we show that MamO has a degenerate active site, rendering it incapable of protease activity. Instead, MamO promotes magnetosome formation through two genetically distinct, noncatalytic activities: activation of MamE-dependent proteolysis of biomineralization factors and direct binding to transition metal ions. By solving the structure of the protease domain bound to a metal ion, we identify a surface-exposed di-histidine motif in MamO that contributes to metal binding and show that it is required to initiate biomineralization in vivo. Finally, we find that pseudoproteases are widespread in magnetotactic bacteria and that they have evolved independently in three separate taxa. In conclusion, our results highlight the versatility of protein scaffolds in accommodating new biochemical activities and provide unprecedented insight into the earliest stages of biomineralization.},
doi = {10.1371/journal.pbio.1002402},
journal = {PLoS biology (Online)},
number = 3,
volume = 14,
place = {United States},
year = {Wed Mar 16 00:00:00 EDT 2016},
month = {Wed Mar 16 00:00:00 EDT 2016}
}

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Cited by: 5 works
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