Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria
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...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2018-12-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/39723 |
| _version_ | 1811200769822556160 |
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| author | Joshua S MacCready Pusparanee Hakim Eric J Young Longhua Hu Jian Liu Katherine W Osteryoung Anthony G Vecchiarelli Daniel C Ducat |
| author_facet | Joshua S MacCready Pusparanee Hakim Eric J Young Longhua Hu Jian Liu Katherine W Osteryoung Anthony G Vecchiarelli Daniel C Ducat |
| author_sort | Joshua S MacCready |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-12T02:09:14Z |
| format | Article |
| id | doaj.art-8d45d2f2db4f4af1ae9a1222619da298 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:09:14Z |
| publishDate | 2018-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-8d45d2f2db4f4af1ae9a1222619da2982022-12-22T03:52:27ZengeLife Sciences Publications LtdeLife2050-084X2018-12-01710.7554/eLife.39723Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteriaJoshua S MacCready0https://orcid.org/0000-0001-6438-8110Pusparanee Hakim1https://orcid.org/0000-0002-9018-8179Eric J Young2https://orcid.org/0000-0002-6770-6310Longhua Hu3Jian Liu4Katherine W Osteryoung5https://orcid.org/0000-0002-0028-2509Anthony G Vecchiarelli6https://orcid.org/0000-0002-6198-3245Daniel C Ducat7https://orcid.org/0000-0002-1520-0588Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, United StatesDepartment of Molecular, Cellular, and Developmental Biology, University of Michigan, Michigan, United StatesDepartment of Biochemistry, Michigan State University, East Lansing, United StatesBiochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, United StatesBiochemistry and Biophysics Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, United StatesDepartment of Plant Biology, Michigan State University, East Lansing, United StatesDepartment of Molecular, Cellular, and Developmental Biology, University of Michigan, Michigan, United StatesDepartment of Biochemistry, Michigan State University, East Lansing, United States; MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, United StatesCarboxysomes 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.https://elifesciences.org/articles/39723Synechococcus elongatus PCC 7942cyanobacteriacarboxysomesprotein self-organization |
| spellingShingle | Joshua S MacCready Pusparanee Hakim Eric J Young Longhua Hu Jian Liu Katherine W Osteryoung Anthony G Vecchiarelli Daniel C Ducat Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria eLife Synechococcus elongatus PCC 7942 cyanobacteria carboxysomes protein self-organization |
| title | Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria |
| title_full | Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria |
| title_fullStr | Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria |
| title_full_unstemmed | Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria |
| title_short | Protein gradients on the nucleoid position the carbon-fixing organelles of cyanobacteria |
| title_sort | protein gradients on the nucleoid position the carbon fixing organelles of cyanobacteria |
| topic | Synechococcus elongatus PCC 7942 cyanobacteria carboxysomes protein self-organization |
| url | https://elifesciences.org/articles/39723 |
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