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Genetic determinants of swimming motility in the squid light‐organ symbiont V ibrio fischeri
Bacterial flagellar motility is a complex cellular behavior required for the colonization of the light‐emitting organ of the Hawaiian bobtail squid, E uprymna scolopes , by the beneficial bioluminescent symbiont V ibrio fischeri . We characterized the basis of this behavior by performing (i) a forwa...
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| Published in: | MicrobiologyOpen (Weinheim) 2013-08, Vol.2 (4), p.576-594 |
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| creator | Brennan, Caitlin A. Mandel, Mark J. Gyllborg, Mattias C. Thomasgard, Krista A. Ruby, Edward G. |
| description | Bacterial flagellar motility is a complex cellular behavior required for the colonization of the light‐emitting organ of the Hawaiian bobtail squid,
E
uprymna scolopes
, by the beneficial bioluminescent symbiont
V
ibrio fischeri
. We characterized the basis of this behavior by performing (i) a forward genetic screen to identify mutants defective in soft‐agar motility, as well as (ii) a transcriptional analysis to determine the genes that are expressed downstream of the flagellar master regulator FlrA. Mutants with severe defects in soft‐agar motility were identified due to insertions in genes with putative roles in flagellar motility and in genes that were unexpected, including those predicted to encode hypothetical proteins and cell division–related proteins. Analysis of mutants for their ability to enter into a productive symbiosis indicated that flagellar motility mutants are deficient, while chemotaxis mutants are able to colonize a subset of juvenile squid to light‐producing levels. Thirty‐three genes required for normal motility in soft agar were also downregulated in the absence of FlrA, suggesting they belong to the flagellar regulon of
V
. fischeri
. Mutagenesis of putative paralogs of the flagellar motility genes
motA
,
motB,
and
fliL
revealed that
motA1
,
motB1
, and both
fliL1
and
fliL2
, but not
motA2
and
motB2
, likely contribute to soft‐agar motility. Using these complementary approaches, we have characterized the genetic basis of flagellar motility in
V
. fischeri
and furthered our understanding of the roles of flagellar motility and chemotaxis in colonization of the juvenile squid, including identifying 11 novel mutants unable to enter into a productive light‐organ symbiosis. |
| doi_str_mv | 10.1002/mbo3.96 |
| format | article |
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E
uprymna scolopes
, by the beneficial bioluminescent symbiont
V
ibrio fischeri
. We characterized the basis of this behavior by performing (i) a forward genetic screen to identify mutants defective in soft‐agar motility, as well as (ii) a transcriptional analysis to determine the genes that are expressed downstream of the flagellar master regulator FlrA. Mutants with severe defects in soft‐agar motility were identified due to insertions in genes with putative roles in flagellar motility and in genes that were unexpected, including those predicted to encode hypothetical proteins and cell division–related proteins. Analysis of mutants for their ability to enter into a productive symbiosis indicated that flagellar motility mutants are deficient, while chemotaxis mutants are able to colonize a subset of juvenile squid to light‐producing levels. Thirty‐three genes required for normal motility in soft agar were also downregulated in the absence of FlrA, suggesting they belong to the flagellar regulon of
V
. fischeri
. Mutagenesis of putative paralogs of the flagellar motility genes
motA
,
motB,
and
fliL
revealed that
motA1
,
motB1
, and both
fliL1
and
fliL2
, but not
motA2
and
motB2
, likely contribute to soft‐agar motility. Using these complementary approaches, we have characterized the genetic basis of flagellar motility in
V
. fischeri
and furthered our understanding of the roles of flagellar motility and chemotaxis in colonization of the juvenile squid, including identifying 11 novel mutants unable to enter into a productive light‐organ symbiosis.</description><identifier>ISSN: 2045-8827</identifier><identifier>EISSN: 2045-8827</identifier><identifier>DOI: 10.1002/mbo3.96</identifier><language>eng</language><publisher>Bognor Regis: John Wiley & Sons, Inc</publisher><subject>Bacteria ; Biosynthesis ; Cell division ; Chemotaxis ; Colonization ; E coli ; Flagella ; Genes ; Genetic engineering ; Genetic screening ; Grants ; Light levels ; Motility ; Mutagenesis ; Mutants ; Mutualism ; Proteins ; Roles ; Squid ; Studies ; Swimming ; Symbiosis ; Transcription ; Waterborne diseases</subject><ispartof>MicrobiologyOpen (Weinheim), 2013-08, Vol.2 (4), p.576-594</ispartof><rights>2013. This work is published under http://creativecommons.org/licenses/by/3.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c985-c23d1c64b7d02939b977d92ad12297da9b051c219cb4c66555a2742ba0293fe43</citedby><cites>FETCH-LOGICAL-c985-c23d1c64b7d02939b977d92ad12297da9b051c219cb4c66555a2742ba0293fe43</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2290773145/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2290773145?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,25753,27924,27925,37012,44590,75126</link.rule.ids></links><search><creatorcontrib>Brennan, Caitlin A.</creatorcontrib><creatorcontrib>Mandel, Mark J.</creatorcontrib><creatorcontrib>Gyllborg, Mattias C.</creatorcontrib><creatorcontrib>Thomasgard, Krista A.</creatorcontrib><creatorcontrib>Ruby, Edward G.</creatorcontrib><title>Genetic determinants of swimming motility in the squid light‐organ symbiont V ibrio fischeri</title><title>MicrobiologyOpen (Weinheim)</title><description>Bacterial flagellar motility is a complex cellular behavior required for the colonization of the light‐emitting organ of the Hawaiian bobtail squid,
E
uprymna scolopes
, by the beneficial bioluminescent symbiont
V
ibrio fischeri
. We characterized the basis of this behavior by performing (i) a forward genetic screen to identify mutants defective in soft‐agar motility, as well as (ii) a transcriptional analysis to determine the genes that are expressed downstream of the flagellar master regulator FlrA. Mutants with severe defects in soft‐agar motility were identified due to insertions in genes with putative roles in flagellar motility and in genes that were unexpected, including those predicted to encode hypothetical proteins and cell division–related proteins. Analysis of mutants for their ability to enter into a productive symbiosis indicated that flagellar motility mutants are deficient, while chemotaxis mutants are able to colonize a subset of juvenile squid to light‐producing levels. Thirty‐three genes required for normal motility in soft agar were also downregulated in the absence of FlrA, suggesting they belong to the flagellar regulon of
V
. fischeri
. Mutagenesis of putative paralogs of the flagellar motility genes
motA
,
motB,
and
fliL
revealed that
motA1
,
motB1
, and both
fliL1
and
fliL2
, but not
motA2
and
motB2
, likely contribute to soft‐agar motility. Using these complementary approaches, we have characterized the genetic basis of flagellar motility in
V
. fischeri
and furthered our understanding of the roles of flagellar motility and chemotaxis in colonization of the juvenile squid, including identifying 11 novel mutants unable to enter into a productive light‐organ symbiosis.</description><subject>Bacteria</subject><subject>Biosynthesis</subject><subject>Cell division</subject><subject>Chemotaxis</subject><subject>Colonization</subject><subject>E coli</subject><subject>Flagella</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Genetic screening</subject><subject>Grants</subject><subject>Light levels</subject><subject>Motility</subject><subject>Mutagenesis</subject><subject>Mutants</subject><subject>Mutualism</subject><subject>Proteins</subject><subject>Roles</subject><subject>Squid</subject><subject>Studies</subject><subject>Swimming</subject><subject>Symbiosis</subject><subject>Transcription</subject><subject>Waterborne diseases</subject><issn>2045-8827</issn><issn>2045-8827</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNpNkM9KAzEYxIMoWGrxFQIePG1NssmmOUrRKhS8FI-G_NttSjdpkxTpzUfwGX0St9SDc_lm4Md8MADcYjTFCJGHXsd6KpoLMCKIsmo2I_zyn78Gk5w3aBBHpKF4BD4WLrjiDbSuuNT7oELJMLYwf_p-iB3sY_FbX47QB1jWDub9wVu49d26_Hx9x9SpAPOx1z6GAt-h18lH2Pps1i75G3DVqm12k787Bqvnp9X8pVq-LV7nj8vKiBmrDKktNg3V3CIiaqEF51YQZTEhglslNGLYECyMpqZpGGOKcEq0OtGto_UY3J1rdynuDy4XuYmHFIaPcmhAnNeYsoG6P1MmxZyTa-Uu-V6lo8RInuaTp_mkaOpf19BjTg</recordid><startdate>201308</startdate><enddate>201308</enddate><creator>Brennan, Caitlin A.</creator><creator>Mandel, Mark J.</creator><creator>Gyllborg, Mattias C.</creator><creator>Thomasgard, Krista A.</creator><creator>Ruby, Edward G.</creator><general>John Wiley & Sons, Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7T7</scope><scope>7X7</scope><scope>7XB</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope></search><sort><creationdate>201308</creationdate><title>Genetic determinants of swimming motility in the squid light‐organ symbiont V ibrio fischeri</title><author>Brennan, Caitlin A. ; Mandel, Mark J. ; Gyllborg, Mattias C. ; Thomasgard, Krista A. ; Ruby, Edward G.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c985-c23d1c64b7d02939b977d92ad12297da9b051c219cb4c66555a2742ba0293fe43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Bacteria</topic><topic>Biosynthesis</topic><topic>Cell division</topic><topic>Chemotaxis</topic><topic>Colonization</topic><topic>E coli</topic><topic>Flagella</topic><topic>Genes</topic><topic>Genetic engineering</topic><topic>Genetic screening</topic><topic>Grants</topic><topic>Light levels</topic><topic>Motility</topic><topic>Mutagenesis</topic><topic>Mutants</topic><topic>Mutualism</topic><topic>Proteins</topic><topic>Roles</topic><topic>Squid</topic><topic>Studies</topic><topic>Swimming</topic><topic>Symbiosis</topic><topic>Transcription</topic><topic>Waterborne diseases</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brennan, Caitlin A.</creatorcontrib><creatorcontrib>Mandel, Mark J.</creatorcontrib><creatorcontrib>Gyllborg, Mattias C.</creatorcontrib><creatorcontrib>Thomasgard, Krista A.</creatorcontrib><creatorcontrib>Ruby, Edward G.</creatorcontrib><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><jtitle>MicrobiologyOpen (Weinheim)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brennan, Caitlin A.</au><au>Mandel, Mark J.</au><au>Gyllborg, Mattias C.</au><au>Thomasgard, Krista A.</au><au>Ruby, Edward G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genetic determinants of swimming motility in the squid light‐organ symbiont V ibrio fischeri</atitle><jtitle>MicrobiologyOpen (Weinheim)</jtitle><date>2013-08</date><risdate>2013</risdate><volume>2</volume><issue>4</issue><spage>576</spage><epage>594</epage><pages>576-594</pages><issn>2045-8827</issn><eissn>2045-8827</eissn><abstract>Bacterial flagellar motility is a complex cellular behavior required for the colonization of the light‐emitting organ of the Hawaiian bobtail squid,
E
uprymna scolopes
, by the beneficial bioluminescent symbiont
V
ibrio fischeri
. We characterized the basis of this behavior by performing (i) a forward genetic screen to identify mutants defective in soft‐agar motility, as well as (ii) a transcriptional analysis to determine the genes that are expressed downstream of the flagellar master regulator FlrA. Mutants with severe defects in soft‐agar motility were identified due to insertions in genes with putative roles in flagellar motility and in genes that were unexpected, including those predicted to encode hypothetical proteins and cell division–related proteins. Analysis of mutants for their ability to enter into a productive symbiosis indicated that flagellar motility mutants are deficient, while chemotaxis mutants are able to colonize a subset of juvenile squid to light‐producing levels. Thirty‐three genes required for normal motility in soft agar were also downregulated in the absence of FlrA, suggesting they belong to the flagellar regulon of
V
. fischeri
. Mutagenesis of putative paralogs of the flagellar motility genes
motA
,
motB,
and
fliL
revealed that
motA1
,
motB1
, and both
fliL1
and
fliL2
, but not
motA2
and
motB2
, likely contribute to soft‐agar motility. Using these complementary approaches, we have characterized the genetic basis of flagellar motility in
V
. fischeri
and furthered our understanding of the roles of flagellar motility and chemotaxis in colonization of the juvenile squid, including identifying 11 novel mutants unable to enter into a productive light‐organ symbiosis.</abstract><cop>Bognor Regis</cop><pub>John Wiley & Sons, Inc</pub><doi>10.1002/mbo3.96</doi><tpages>19</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 2045-8827 |
| ispartof | MicrobiologyOpen (Weinheim), 2013-08, Vol.2 (4), p.576-594 |
| issn | 2045-8827 2045-8827 |
| language | eng |
| recordid | cdi_proquest_journals_2290773145 |
| source | Publicly Available Content Database; Wiley Open Access; PubMed Central |
| subjects | Bacteria Biosynthesis Cell division Chemotaxis Colonization E coli Flagella Genes Genetic engineering Genetic screening Grants Light levels Motility Mutagenesis Mutants Mutualism Proteins Roles Squid Studies Swimming Symbiosis Transcription Waterborne diseases |
| title | Genetic determinants of swimming motility in the squid light‐organ symbiont V ibrio fischeri |
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