Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria

MacCready, Joshua S.; Hakim, Pusparanee; Young, Eric J.; Hu, Longhua; Liu, Jian; Osteryoung, Katherine W.; Vecchiarelli, Anthony G.; Ducat, Daniel C.

doi:10.7554/eLife.39723

Title: Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria

Journal Article · Thu Dec 06 00:00:00 EST 2018 · eLife

DOI:https://doi.org/10.7554/eLife.39723· OSTI ID:1484819

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^[3]; Hu, Longhua ^[4]; Liu, Jian ^[4];

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Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States
Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Michigan, United States
Department of Biochemistry, Michigan State University, East Lansing, United States
Biochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, United States
Department of Plant Biology, Michigan State University, East Lansing, United States
Department of Biochemistry, Michigan State University, East Lansing, United States, MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, United States

Carboxysomes are protein-based bacterial organelles encapsulating key enzymes of the Calvin-Benson-Bassham cycle. Previous work has implicated a ParA-like protein (hereafter McdA) as important for spatially organizing carboxysomes along the longitudinal axis of the model cyanobacterium Synechococcus elongatus PCC 7942. Yet, how self-organization of McdA emerges and contributes to carboxysome positioning is unknown. Here, we identify a small protein, termed McdB that localizes to carboxysomes and drives emergent oscillatory patterning of McdA on the nucleoid. Our results demonstrate that McdB directly stimulates McdA ATPase activity and its release from DNA, driving carboxysome-dependent depletion of McdA locally on the nucleoid and promoting directed motion of carboxysomes towards increased concentrations of McdA. We propose that McdA and McdB are a previously unknown class of self-organizing proteins that utilize a Brownian-ratchet mechanism to position carboxysomes in cyanobacteria, rather than a cytoskeletal system. These results have broader implications for understanding spatial organization of protein mega-complexes and organelles in bacteria.

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Research Organization:: Michigan State Univ., East Lansing (United States). MSU-DOE Plant Research Laboratory

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); University of Michigan

Grant/Contract Number:: FG02-91ER20021; 1517241; 1817478

OSTI ID:: 1484819

Alternate ID(s):: OSTI ID: 1484820; OSTI ID: 1603778

Journal Information:: eLife, Journal Name: eLife Vol. 7; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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