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

Abstract

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.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3];  [4];  [4]; ORCiD logo [5]; ORCiD logo [2]; ORCiD logo [6]
  1. Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United States
  2. Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Michigan, United States
  3. Department of Biochemistry, Michigan State University, East Lansing, United States
  4. Biochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, United States
  5. Department of Plant Biology, Michigan State University, East Lansing, United States
  6. Department of Biochemistry, Michigan State University, East Lansing, United States, MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, United States
Publication Date:
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1484819
Alternate Identifier(s):
OSTI ID: 1484820
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Journal Article: Published Article
Journal Name:
eLife
Additional Journal Information:
Journal Name: eLife Journal Volume: 7; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
English

Citation Formats

MacCready, Joshua S., Hakim, Pusparanee, Young, Eric J., Hu, Longhua, Liu, Jian, Osteryoung, Katherine W., Vecchiarelli, Anthony G., and Ducat, Daniel C. Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria. United States: N. p., 2018. Web. doi:10.7554/eLife.39723.
MacCready, Joshua S., Hakim, Pusparanee, Young, Eric J., Hu, Longhua, Liu, Jian, Osteryoung, Katherine W., Vecchiarelli, Anthony G., & Ducat, Daniel C. Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria. United States. doi:10.7554/eLife.39723.
MacCready, Joshua S., Hakim, Pusparanee, Young, Eric J., Hu, Longhua, Liu, Jian, Osteryoung, Katherine W., Vecchiarelli, Anthony G., and Ducat, Daniel C. Thu . "Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria". United States. doi:10.7554/eLife.39723.
@article{osti_1484819,
title = {Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria},
author = {MacCready, Joshua S. and Hakim, Pusparanee and Young, Eric J. and Hu, Longhua and Liu, Jian and Osteryoung, Katherine W. and Vecchiarelli, Anthony G. and Ducat, Daniel C.},
abstractNote = {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.},
doi = {10.7554/eLife.39723},
journal = {eLife},
issn = {2050-084X},
number = ,
volume = 7,
place = {United States},
year = {2018},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.7554/eLife.39723

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Works referenced in this record:

Enzymatic assembly of DNA molecules up to several hundred kilobases
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