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A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior
The evolution of eukaryotic organisms is often strongly influenced by microbial symbionts that confer novel traits to their hosts. Here we describe the intracellular Enterobacteriaceae symbiont of the invasive ant Cardiocondyla obscurior , ‘ Candidatus Westeberhardia cardiocondylae’. Upon metamorpho...
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Published in: | The ISME Journal 2016-02, Vol.10 (2), p.376-388 |
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creator | Klein, Antonia Schrader, Lukas Gil, Rosario Manzano-Marín, Alejandro Flórez, Laura Wheeler, David Werren, John H Latorre, Amparo Heinze, Jürgen Kaltenpoth, Martin Moya, Andrés Oettler, Jan |
description | The evolution of eukaryotic organisms is often strongly influenced by microbial symbionts that confer novel traits to their hosts. Here we describe the intracellular Enterobacteriaceae symbiont of the invasive ant
Cardiocondyla obscurior
, ‘
Candidatus
Westeberhardia cardiocondylae’. Upon metamorphosis,
Westeberhardia
is found in gut-associated bacteriomes that deteriorate following eclosion. Only queens maintain
Westeberhardia
in the ovarian nurse cells from where the symbionts are transmitted to late-stage oocytes during nurse cell depletion. Functional analyses of the streamlined genome of
Westeberhardia
(533 kb, 23.41% GC content) indicate that neither vitamins nor essential amino acids are provided for the host. However, the genome encodes for an almost complete shikimate pathway leading to 4-hydroxyphenylpyruvate, which could be converted into tyrosine by the host. Taken together with increasing titers of
Westeberhardia
during pupal stage, this suggests a contribution of
Westeberhardia
to cuticle formation. Despite a widespread occurrence of
Westeberhardia
across host populations, one ant lineage was found to be naturally symbiont-free, pointing to the loss of an otherwise prevalent endosymbiont. This study yields insights into a novel intracellular mutualist that could play a role in the invasive success of
C. obscurior. |
doi_str_mv | 10.1038/ismej.2015.119 |
format | article |
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Cardiocondyla obscurior
, ‘
Candidatus
Westeberhardia cardiocondylae’. Upon metamorphosis,
Westeberhardia
is found in gut-associated bacteriomes that deteriorate following eclosion. Only queens maintain
Westeberhardia
in the ovarian nurse cells from where the symbionts are transmitted to late-stage oocytes during nurse cell depletion. Functional analyses of the streamlined genome of
Westeberhardia
(533 kb, 23.41% GC content) indicate that neither vitamins nor essential amino acids are provided for the host. However, the genome encodes for an almost complete shikimate pathway leading to 4-hydroxyphenylpyruvate, which could be converted into tyrosine by the host. Taken together with increasing titers of
Westeberhardia
during pupal stage, this suggests a contribution of
Westeberhardia
to cuticle formation. Despite a widespread occurrence of
Westeberhardia
across host populations, one ant lineage was found to be naturally symbiont-free, pointing to the loss of an otherwise prevalent endosymbiont. This study yields insights into a novel intracellular mutualist that could play a role in the invasive success of
C. obscurior.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/ismej.2015.119</identifier><identifier>PMID: 26172209</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>14/32 ; 45 ; 45/77 ; 45/91 ; 631/326/41/547 ; Amino acids ; Animals ; Ants - metabolism ; Ants - microbiology ; Bacteria ; Bacteria - classification ; Bacteria - genetics ; Bacteria - isolation & purification ; Bacteria - metabolism ; Biomedical and Life Sciences ; Cardiocondyla obscurior ; Ecology ; Enterobacteriaceae ; Evolutionary Biology ; Female ; Formicidae ; Invasive insects ; Life Sciences ; Male ; Metamorphosis ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Original ; original-article ; Phenylpyruvic Acids - metabolism ; Phylogeny ; Symbiosis ; Vitamins</subject><ispartof>The ISME Journal, 2016-02, Vol.10 (2), p.376-388</ispartof><rights>International Society for Microbial Ecology 2016</rights><rights>Copyright Nature Publishing Group Feb 2016</rights><rights>Copyright © 2016 International Society for Microbial Ecology 2016 International Society for Microbial Ecology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-15d16a2bc6e3ed2168a3742949ca103d52f7e5c8ecf18b08ad34ce680f8f0e8e3</citedby><cites>FETCH-LOGICAL-c451t-15d16a2bc6e3ed2168a3742949ca103d52f7e5c8ecf18b08ad34ce680f8f0e8e3</cites><orcidid>0000-0002-9397-1003</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4737929/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4737929/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,315,730,783,787,888,27936,27937,53804,53806</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26172209$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Klein, Antonia</creatorcontrib><creatorcontrib>Schrader, Lukas</creatorcontrib><creatorcontrib>Gil, Rosario</creatorcontrib><creatorcontrib>Manzano-Marín, Alejandro</creatorcontrib><creatorcontrib>Flórez, Laura</creatorcontrib><creatorcontrib>Wheeler, David</creatorcontrib><creatorcontrib>Werren, John H</creatorcontrib><creatorcontrib>Latorre, Amparo</creatorcontrib><creatorcontrib>Heinze, Jürgen</creatorcontrib><creatorcontrib>Kaltenpoth, Martin</creatorcontrib><creatorcontrib>Moya, Andrés</creatorcontrib><creatorcontrib>Oettler, Jan</creatorcontrib><title>A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>The evolution of eukaryotic organisms is often strongly influenced by microbial symbionts that confer novel traits to their hosts. Here we describe the intracellular Enterobacteriaceae symbiont of the invasive ant
Cardiocondyla obscurior
, ‘
Candidatus
Westeberhardia cardiocondylae’. Upon metamorphosis,
Westeberhardia
is found in gut-associated bacteriomes that deteriorate following eclosion. Only queens maintain
Westeberhardia
in the ovarian nurse cells from where the symbionts are transmitted to late-stage oocytes during nurse cell depletion. Functional analyses of the streamlined genome of
Westeberhardia
(533 kb, 23.41% GC content) indicate that neither vitamins nor essential amino acids are provided for the host. However, the genome encodes for an almost complete shikimate pathway leading to 4-hydroxyphenylpyruvate, which could be converted into tyrosine by the host. Taken together with increasing titers of
Westeberhardia
during pupal stage, this suggests a contribution of
Westeberhardia
to cuticle formation. Despite a widespread occurrence of
Westeberhardia
across host populations, one ant lineage was found to be naturally symbiont-free, pointing to the loss of an otherwise prevalent endosymbiont. This study yields insights into a novel intracellular mutualist that could play a role in the invasive success of
C. obscurior.</description><subject>14/32</subject><subject>45</subject><subject>45/77</subject><subject>45/91</subject><subject>631/326/41/547</subject><subject>Amino acids</subject><subject>Animals</subject><subject>Ants - metabolism</subject><subject>Ants - microbiology</subject><subject>Bacteria</subject><subject>Bacteria - classification</subject><subject>Bacteria - genetics</subject><subject>Bacteria - isolation & purification</subject><subject>Bacteria - metabolism</subject><subject>Biomedical and Life Sciences</subject><subject>Cardiocondyla obscurior</subject><subject>Ecology</subject><subject>Enterobacteriaceae</subject><subject>Evolutionary Biology</subject><subject>Female</subject><subject>Formicidae</subject><subject>Invasive insects</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Metamorphosis</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Original</subject><subject>original-article</subject><subject>Phenylpyruvic Acids - 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Academic</collection><collection>Entomology Abstracts (Full archive)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Klein, Antonia</au><au>Schrader, Lukas</au><au>Gil, Rosario</au><au>Manzano-Marín, Alejandro</au><au>Flórez, Laura</au><au>Wheeler, David</au><au>Werren, John H</au><au>Latorre, Amparo</au><au>Heinze, Jürgen</au><au>Kaltenpoth, Martin</au><au>Moya, Andrés</au><au>Oettler, Jan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2016-02-01</date><risdate>2016</risdate><volume>10</volume><issue>2</issue><spage>376</spage><epage>388</epage><pages>376-388</pages><issn>1751-7362</issn><eissn>1751-7370</eissn><abstract>The evolution of eukaryotic organisms is often strongly influenced by microbial symbionts that confer novel traits to their hosts. Here we describe the intracellular Enterobacteriaceae symbiont of the invasive ant
Cardiocondyla obscurior
, ‘
Candidatus
Westeberhardia cardiocondylae’. Upon metamorphosis,
Westeberhardia
is found in gut-associated bacteriomes that deteriorate following eclosion. Only queens maintain
Westeberhardia
in the ovarian nurse cells from where the symbionts are transmitted to late-stage oocytes during nurse cell depletion. Functional analyses of the streamlined genome of
Westeberhardia
(533 kb, 23.41% GC content) indicate that neither vitamins nor essential amino acids are provided for the host. However, the genome encodes for an almost complete shikimate pathway leading to 4-hydroxyphenylpyruvate, which could be converted into tyrosine by the host. Taken together with increasing titers of
Westeberhardia
during pupal stage, this suggests a contribution of
Westeberhardia
to cuticle formation. Despite a widespread occurrence of
Westeberhardia
across host populations, one ant lineage was found to be naturally symbiont-free, pointing to the loss of an otherwise prevalent endosymbiont. This study yields insights into a novel intracellular mutualist that could play a role in the invasive success of
C. obscurior.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>26172209</pmid><doi>10.1038/ismej.2015.119</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-9397-1003</orcidid><oa>free_for_read</oa></addata></record> |
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source | PubMed Central |
subjects | 14/32 45 45/77 45/91 631/326/41/547 Amino acids Animals Ants - metabolism Ants - microbiology Bacteria Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Bacteria - metabolism Biomedical and Life Sciences Cardiocondyla obscurior Ecology Enterobacteriaceae Evolutionary Biology Female Formicidae Invasive insects Life Sciences Male Metamorphosis Microbial Ecology Microbial Genetics and Genomics Microbiology Original original-article Phenylpyruvic Acids - metabolism Phylogeny Symbiosis Vitamins |
title | A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior |
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