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

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

doi:10.1371/journal.pbio.1002402

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

Journal Article · Wed Mar 16 00:00:00 EDT 2016 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.1002402· OSTI ID:1253997

Hershey, David M. ^[1]; Ren, Xuefeng ^[2]; Melnyk, Ryan A. ^[3]; Browne, Patrick J. ^[4]; Ozyamak, Ertan ^[4]; Jones, Stephanie R. ^[5]; Chang, Michelle C. Y. ^[6]; Hurley, James H. ^[7]; Komeili, Arash ^[8]

Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; Office of Scientific and Technical Information (OSTI)
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). Physical Biosciences Division
Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
Univ. of California, Berkeley, CA (United States). Dept. of Chemistry
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
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
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

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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1253997

Alternate ID(s):: OSTI ID: 1379123
OSTI ID: 1379160

Journal Information:: PLoS Biology (Online), Journal Name: PLoS Biology (Online) Journal Issue: 3 Vol. 14; ISSN 1545-7885

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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