A protease-mediated switch regulates the growth of magnetosome organelles in Magnetospirillum magneticum

Journal Article · 02 February 2022 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.2111745119 · OSTI ID:2470952

Wan, Juan  ^[1]; Browne, Patrick J. ^[1]; Hershey, David M.  ^[2]; Montabana, Elizabeth ^[3]; Iavarone, Anthony T. ^[1]; Downing, Kenneth H.  ^[4]; Komeili, Arash  ^[1]

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1. University of California, Berkeley, CA (United States)
2. University of Wisconsin, Madison, WI (United States)
3. Stanford University, CA (United States). School of Medicine
4. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Magnetosomes are lipid-bound organelles that direct the biomineralization of magnetic nanoparticles in magnetotactic bacteria. Magnetosome membranes are not uniform in size and can grow in a biomineralization-dependent manner. However, the underlying mechanisms of magnetosome membrane growth regulation remain unclear. Using cryoelectron tomography, we systematically examined mutants with defects at various stages of magnetosome formation to identify factors involved in controlling membrane growth. We found that a conserved serine protease, MamE, plays a key role in magnetosome membrane growth regulation. When the protease activity of MamE is disrupted, magnetosome membrane growth is restricted, which, in turn, limits the size of the magnetite particles. Consistent with this finding, the upstream regulators of MamE protease activity, MamO and MamM, are also required for magnetosome membrane growth. We then used a combination of candidate and comparative proteomics approaches to identify Mms6 and MamD as two MamE substrates. Mms6 does not appear to participate in magnetosome membrane growth. However, in the absence of MamD, magnetosome membranes grow to a larger size than the wild type. Furthermore, when the cleavage of MamD by MamE protease is blocked, magnetosome membrane growth and biomineralization are severely inhibited, phenocopying the MamE protease-inactive mutant. We therefore propose that the growth of magnetosome membranes is controlled by a protease-mediated switch through processing of MamD. Overall, our work shows that, like many eukaryotic systems, bacteria control the growth and size of biominerals by manipulating the physical properties of intracellular organelles.

• Research Organization: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
• Sponsoring Organization: National Institutes of Health (NIH); USDOE
• Grant/Contract Number: AC02-05CH11231
• OSTI ID: 2470952
• Journal Information: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 6 Vol. 119; ISSN 0027-8424
• Publisher: National Academy of SciencesCopyright Statement
• Country of Publication: United States
• Language: English