Magnetosome chains are recruited to cellular division sites and split by asymmetric septation
Summary Magnetotactic bacteria navigate along magnetic field lines using well‐ordered chains of membrane‐enclosed magnetic crystals, referred to as magnetosomes, which have emerged as model to investigate organelle biogenesis in prokaryotic systems. To become divided and segregated faithfully during...
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Veröffentlicht in: | Molecular microbiology 2011-12, Vol.82 (6), p.1316-1329 |
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creator | Katzmann, Emanuel Müller, Frank D. Lang, Claus Messerer, Maxim Winklhofer, Michael Plitzko, Jürgen M. Schüler, Dirk |
description | Summary
Magnetotactic bacteria navigate along magnetic field lines using well‐ordered chains of membrane‐enclosed magnetic crystals, referred to as magnetosomes, which have emerged as model to investigate organelle biogenesis in prokaryotic systems. To become divided and segregated faithfully during cytokinesis, the magnetosome chain has to be properly positioned, cleaved and separated against intrachain magnetostatic forces. Here we demonstrate that magnetotactic bacteria use dedicated mechanisms to control the position and division of the magnetosome chain, thus maintaining magnetic orientation throughout divisional cycle. Using electron and time‐lapse microscopy of synchronized cells of Magnetospirillum gryphiswaldense, we confirm that magnetosome chains undergo a dynamic pole‐to‐midcell translocation during cytokinesis. Nascent chains were recruited to division sites also in division‐inhibited cells, but not in a mamK mutant, indicating an active mechanism depending upon the actin‐like cytoskeletal magnetosome filament. Cryo‐electron tomography revealed that both the magnetosome chain and the magnetosome filament are spilt into halves by asymmetric septation and unidirectional indentation, which we interpret in terms of a specific adaptation required to overcome the magnetostatic interactions between separating daughter chains. Our study demonstrates that magnetosome division and segregation is co‐ordinated with cytokinesis and resembles partitioning mechanisms of other organelles and macromolecular complexes in bacteria. |
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Magnetotactic bacteria navigate along magnetic field lines using well‐ordered chains of membrane‐enclosed magnetic crystals, referred to as magnetosomes, which have emerged as model to investigate organelle biogenesis in prokaryotic systems. To become divided and segregated faithfully during cytokinesis, the magnetosome chain has to be properly positioned, cleaved and separated against intrachain magnetostatic forces. Here we demonstrate that magnetotactic bacteria use dedicated mechanisms to control the position and division of the magnetosome chain, thus maintaining magnetic orientation throughout divisional cycle. Using electron and time‐lapse microscopy of synchronized cells of Magnetospirillum gryphiswaldense, we confirm that magnetosome chains undergo a dynamic pole‐to‐midcell translocation during cytokinesis. Nascent chains were recruited to division sites also in division‐inhibited cells, but not in a mamK mutant, indicating an active mechanism depending upon the actin‐like cytoskeletal magnetosome filament. Cryo‐electron tomography revealed that both the magnetosome chain and the magnetosome filament are spilt into halves by asymmetric septation and unidirectional indentation, which we interpret in terms of a specific adaptation required to overcome the magnetostatic interactions between separating daughter chains. Our study demonstrates that magnetosome division and segregation is co‐ordinated with cytokinesis and resembles partitioning mechanisms of other organelles and macromolecular complexes in bacteria.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/j.1365-2958.2011.07874.x</identifier><identifier>PMID: 22026731</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Asymmetric Cell Division ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biological and medical sciences ; Cell division ; Crystals ; Cytokines ; Cytokinesis ; Fundamental and applied biological sciences. Psychology ; Magnetic fields ; Magnetosomes - genetics ; Magnetosomes - metabolism ; Magnetospirillum - cytology ; Magnetospirillum - genetics ; Magnetospirillum - metabolism ; Microbiology</subject><ispartof>Molecular microbiology, 2011-12, Vol.82 (6), p.1316-1329</ispartof><rights>2011 Blackwell Publishing Ltd</rights><rights>2015 INIST-CNRS</rights><rights>2011 Blackwell Publishing Ltd.</rights><rights>Copyright Blackwell Publishing Ltd. Dec 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5414-3bc9e629d83d39d3a0bcfd41b5ab2df4fe5c162c4aa4e81d1bd4cb2343dfa7e63</citedby><cites>FETCH-LOGICAL-c5414-3bc9e629d83d39d3a0bcfd41b5ab2df4fe5c162c4aa4e81d1bd4cb2343dfa7e63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1365-2958.2011.07874.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1365-2958.2011.07874.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25273877$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22026731$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Katzmann, Emanuel</creatorcontrib><creatorcontrib>Müller, Frank D.</creatorcontrib><creatorcontrib>Lang, Claus</creatorcontrib><creatorcontrib>Messerer, Maxim</creatorcontrib><creatorcontrib>Winklhofer, Michael</creatorcontrib><creatorcontrib>Plitzko, Jürgen M.</creatorcontrib><creatorcontrib>Schüler, Dirk</creatorcontrib><title>Magnetosome chains are recruited to cellular division sites and split by asymmetric septation</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
Magnetotactic bacteria navigate along magnetic field lines using well‐ordered chains of membrane‐enclosed magnetic crystals, referred to as magnetosomes, which have emerged as model to investigate organelle biogenesis in prokaryotic systems. To become divided and segregated faithfully during cytokinesis, the magnetosome chain has to be properly positioned, cleaved and separated against intrachain magnetostatic forces. Here we demonstrate that magnetotactic bacteria use dedicated mechanisms to control the position and division of the magnetosome chain, thus maintaining magnetic orientation throughout divisional cycle. Using electron and time‐lapse microscopy of synchronized cells of Magnetospirillum gryphiswaldense, we confirm that magnetosome chains undergo a dynamic pole‐to‐midcell translocation during cytokinesis. Nascent chains were recruited to division sites also in division‐inhibited cells, but not in a mamK mutant, indicating an active mechanism depending upon the actin‐like cytoskeletal magnetosome filament. Cryo‐electron tomography revealed that both the magnetosome chain and the magnetosome filament are spilt into halves by asymmetric septation and unidirectional indentation, which we interpret in terms of a specific adaptation required to overcome the magnetostatic interactions between separating daughter chains. Our study demonstrates that magnetosome division and segregation is co‐ordinated with cytokinesis and resembles partitioning mechanisms of other organelles and macromolecular complexes in bacteria.</description><subject>Asymmetric Cell Division</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biological and medical sciences</subject><subject>Cell division</subject><subject>Crystals</subject><subject>Cytokines</subject><subject>Cytokinesis</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Magnetic fields</subject><subject>Magnetosomes - genetics</subject><subject>Magnetosomes - metabolism</subject><subject>Magnetospirillum - cytology</subject><subject>Magnetospirillum - genetics</subject><subject>Magnetospirillum - metabolism</subject><subject>Microbiology</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU1r3DAQhkVpabZp_0IRgdKTHX3Zlg85lNA2gSy9JNBLEbI0brT4Y6Ox2-y_r5zdJJBT5zID88zw8r6EUM5ynup0k3NZFpmoC50LxnnOKl2p_P4VWT0tXpMVqwuWSS1-HpF3iBvGuGSlfEuOhGCirCRfkV9r-3uAacSxB-pubRiQ2gg0gotzmMDTaaQOum7ubKQ-_AkYxoFiWiVw8BS3XZhos6MWd30PUwyOImwnOyXuPXnT2g7hw6Efk5tvX6_PL7KrH98vz79cZa5QXGWycTWUovZaell7aVnjWq94U9hG-Fa1UDheCqesVaC5541XrhFSSd_aCkp5TD7v_27jeDcDTqYPuKi2A4wzmprzWmqleCJPXpCbcY5DEpcgphRjukqQ3kMujogRWrONobdxZzgzSwBmYxafzeKzWQIwDwGY-3T68fB_bnrwT4ePjifg0wGw6GzXRju4gM9cISqpq0XD2Z77GzrY_bcAs15fLpP8B7gToug</recordid><startdate>201112</startdate><enddate>201112</enddate><creator>Katzmann, Emanuel</creator><creator>Müller, Frank D.</creator><creator>Lang, Claus</creator><creator>Messerer, Maxim</creator><creator>Winklhofer, Michael</creator><creator>Plitzko, Jürgen M.</creator><creator>Schüler, Dirk</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201112</creationdate><title>Magnetosome chains are recruited to cellular division sites and split by asymmetric septation</title><author>Katzmann, Emanuel ; Müller, Frank D. ; Lang, Claus ; Messerer, Maxim ; Winklhofer, Michael ; Plitzko, Jürgen M. ; Schüler, Dirk</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5414-3bc9e629d83d39d3a0bcfd41b5ab2df4fe5c162c4aa4e81d1bd4cb2343dfa7e63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Asymmetric Cell Division</topic><topic>Bacteria</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Biological and medical sciences</topic><topic>Cell division</topic><topic>Crystals</topic><topic>Cytokines</topic><topic>Cytokinesis</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Magnetic fields</topic><topic>Magnetosomes - genetics</topic><topic>Magnetosomes - metabolism</topic><topic>Magnetospirillum - cytology</topic><topic>Magnetospirillum - genetics</topic><topic>Magnetospirillum - metabolism</topic><topic>Microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Katzmann, Emanuel</creatorcontrib><creatorcontrib>Müller, Frank D.</creatorcontrib><creatorcontrib>Lang, Claus</creatorcontrib><creatorcontrib>Messerer, Maxim</creatorcontrib><creatorcontrib>Winklhofer, Michael</creatorcontrib><creatorcontrib>Plitzko, Jürgen M.</creatorcontrib><creatorcontrib>Schüler, Dirk</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Katzmann, Emanuel</au><au>Müller, Frank D.</au><au>Lang, Claus</au><au>Messerer, Maxim</au><au>Winklhofer, Michael</au><au>Plitzko, Jürgen M.</au><au>Schüler, Dirk</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Magnetosome chains are recruited to cellular division sites and split by asymmetric septation</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2011-12</date><risdate>2011</risdate><volume>82</volume><issue>6</issue><spage>1316</spage><epage>1329</epage><pages>1316-1329</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
Magnetotactic bacteria navigate along magnetic field lines using well‐ordered chains of membrane‐enclosed magnetic crystals, referred to as magnetosomes, which have emerged as model to investigate organelle biogenesis in prokaryotic systems. To become divided and segregated faithfully during cytokinesis, the magnetosome chain has to be properly positioned, cleaved and separated against intrachain magnetostatic forces. Here we demonstrate that magnetotactic bacteria use dedicated mechanisms to control the position and division of the magnetosome chain, thus maintaining magnetic orientation throughout divisional cycle. Using electron and time‐lapse microscopy of synchronized cells of Magnetospirillum gryphiswaldense, we confirm that magnetosome chains undergo a dynamic pole‐to‐midcell translocation during cytokinesis. Nascent chains were recruited to division sites also in division‐inhibited cells, but not in a mamK mutant, indicating an active mechanism depending upon the actin‐like cytoskeletal magnetosome filament. Cryo‐electron tomography revealed that both the magnetosome chain and the magnetosome filament are spilt into halves by asymmetric septation and unidirectional indentation, which we interpret in terms of a specific adaptation required to overcome the magnetostatic interactions between separating daughter chains. Our study demonstrates that magnetosome division and segregation is co‐ordinated with cytokinesis and resembles partitioning mechanisms of other organelles and macromolecular complexes in bacteria.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>22026731</pmid><doi>10.1111/j.1365-2958.2011.07874.x</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Asymmetric Cell Division Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Biological and medical sciences Cell division Crystals Cytokines Cytokinesis Fundamental and applied biological sciences. Psychology Magnetic fields Magnetosomes - genetics Magnetosomes - metabolism Magnetospirillum - cytology Magnetospirillum - genetics Magnetospirillum - metabolism Microbiology |
title | Magnetosome chains are recruited to cellular division sites and split by asymmetric septation |
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