Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas
Wolbachiae are obligate intracellular bacteria that infect arthropods and certain nematodes. Usually maternally inherited, they may provision nutrients to (mutualism) or alter sexual biology of (reproductive parasitism) their invertebrate hosts. We report the assembly of closed genomes for two novel...
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| creator | Driscoll, Timothy P Verhoeve, Victoria I Brockway, Cassia Shrewsberry, Darin L Plumer, Mariah Sevdalis, Spiridon E Beckmann, John F Krueger, Laura M Macaluso, Kevin R Azad, Abdu F Gillespie, Joseph J |
| description | Wolbachiae are obligate intracellular bacteria that infect arthropods and certain nematodes. Usually maternally inherited, they may provision nutrients to (mutualism) or alter sexual biology of (reproductive parasitism) their invertebrate hosts. We report the assembly of closed genomes for two novel wolbachiae,
CfeT and
CfeJ, found co-infecting cat fleas (
) of the Elward Laboratory colony (Soquel, CA, USA).
CfeT is basal to nearly all described
supergroups, while
CfeJ is related to supergroups C, D and F. Both genomes contain laterally transferred genes that inform on the evolution of
host associations.
CfeT carries the Biotin synthesis Operon of Obligate intracellular Microbes (BOOM); our analyses reveal five independent acquisitions of BOOM across the
tree, indicating parallel evolution towards mutualism. Alternately,
CfeJ harbors a toxin-antidote operon analogous to the
Pip
operon recently characterized as an inducer of cytoplasmic incompatibility (CI) in flies.
CfeJ
and three adjacent genes are collectively similar to large modular toxins encoded in CI-like operons of certain
strains and
species, signifying that CI toxins streamline by fission of large modular toxins. Remarkably, the
.
genome itself contains two CI-like antidote genes, divergent from
CfeJ
, revealing episodic reproductive parasitism in cat fleas and evidencing mobility of CI loci independent of WO-phage. Additional screening revealed predominant co-infection (
CfeT/
CfeJ) amongst
.
colonies, though fleas in wild populations mostly harbor
CfeT alone. Collectively, genomes of
CfeT,
CfeJ, and their cat flea host supply instances of lateral gene transfers that could drive transitions between parasitism and mutualism. |
| doi_str_mv | 10.7717/peerj.10646 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7750005</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2470788765</sourcerecordid><originalsourceid>FETCH-LOGICAL-c372t-31fb41df1b710071a91759ca8605366b88ced81477bdbe34ac9191e175f8cec43</originalsourceid><addsrcrecordid>eNpdkctrHSEYxaU0NCHJqvsidFMIk-g4o04XhRDygkA2CV2K42iuF0enPm7pfx9vXqRx4yfnx-F8HgC-YnTMGGYni9ZxfYwR7egnsNdiyhpO-uHzu3kXHKa0RvXwliJOvoBdQghtB97ugXK-Ca5kGzwMBv4ObpRqZSWcSy7S2TRD6ScY9RLDVFS2Gw0XGWWyuWo_ofXJPqwyNDHMMP8N0IeNdjDlKKsE80pmqEJjvdGqTvVlnJbpAOwY6ZI-fLn3wf3F-d3ZVXNze3l9dnrTKMLa3BBsxg5PBo8MI8SwHDDrByU5RT2hdORc6YnjjrFxGjXppBrwgHWFTFVUR_bBr2ffpYyznpT2NZgTS7SzjP9EkFb8r3i7Eg9hIxjr63_11eDHi0EMf4pOWcw2Ke2c9DqUJNqOkQ71Axkq-v0Dug4l-rrelkKMc0a3hkfPlIohpajNWxiMxLZR8dSoeGq00t_e539jX_sjj06Lnzg</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2470788765</pqid></control><display><type>article</type><title>Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas</title><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central</source><creator>Driscoll, Timothy P ; Verhoeve, Victoria I ; Brockway, Cassia ; Shrewsberry, Darin L ; Plumer, Mariah ; Sevdalis, Spiridon E ; Beckmann, John F ; Krueger, Laura M ; Macaluso, Kevin R ; Azad, Abdu F ; Gillespie, Joseph J</creator><creatorcontrib>Driscoll, Timothy P ; Verhoeve, Victoria I ; Brockway, Cassia ; Shrewsberry, Darin L ; Plumer, Mariah ; Sevdalis, Spiridon E ; Beckmann, John F ; Krueger, Laura M ; Macaluso, Kevin R ; Azad, Abdu F ; Gillespie, Joseph J</creatorcontrib><description>Wolbachiae are obligate intracellular bacteria that infect arthropods and certain nematodes. Usually maternally inherited, they may provision nutrients to (mutualism) or alter sexual biology of (reproductive parasitism) their invertebrate hosts. We report the assembly of closed genomes for two novel wolbachiae,
CfeT and
CfeJ, found co-infecting cat fleas (
) of the Elward Laboratory colony (Soquel, CA, USA).
CfeT is basal to nearly all described
supergroups, while
CfeJ is related to supergroups C, D and F. Both genomes contain laterally transferred genes that inform on the evolution of
host associations.
CfeT carries the Biotin synthesis Operon of Obligate intracellular Microbes (BOOM); our analyses reveal five independent acquisitions of BOOM across the
tree, indicating parallel evolution towards mutualism. Alternately,
CfeJ harbors a toxin-antidote operon analogous to the
Pip
operon recently characterized as an inducer of cytoplasmic incompatibility (CI) in flies.
CfeJ
and three adjacent genes are collectively similar to large modular toxins encoded in CI-like operons of certain
strains and
species, signifying that CI toxins streamline by fission of large modular toxins. Remarkably, the
.
genome itself contains two CI-like antidote genes, divergent from
CfeJ
, revealing episodic reproductive parasitism in cat fleas and evidencing mobility of CI loci independent of WO-phage. Additional screening revealed predominant co-infection (
CfeT/
CfeJ) amongst
.
colonies, though fleas in wild populations mostly harbor
CfeT alone. Collectively, genomes of
CfeT,
CfeJ, and their cat flea host supply instances of lateral gene transfers that could drive transitions between parasitism and mutualism.</description><identifier>ISSN: 2167-8359</identifier><identifier>EISSN: 2167-8359</identifier><identifier>DOI: 10.7717/peerj.10646</identifier><identifier>PMID: 33362982</identifier><language>eng</language><publisher>United States: PeerJ, Inc</publisher><subject>Biosynthesis ; Biotin ; Colonies ; Concurrent infection ; Cytoplasmic incompatibility ; Divergence ; Entomology ; Evolution ; Evolutionary genetics ; Evolutionary Studies ; Genes ; Genomes ; Genomics ; Infections ; Intracellular ; Invertebrates ; Microbiology ; Mutualism ; Nematodes ; Nutrients ; Operons ; Parasites ; Parasitism ; Phages ; Siphonaptera ; Strains (organisms) ; Wolbachia ; Zoology</subject><ispartof>PeerJ (San Francisco, CA), 2020-12, Vol.8, p.e10646, Article e10646</ispartof><rights>2020 Driscoll et al.</rights><rights>2020 Driscoll et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020 Driscoll et al. 2020 Driscoll et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c372t-31fb41df1b710071a91759ca8605366b88ced81477bdbe34ac9191e175f8cec43</citedby><cites>FETCH-LOGICAL-c372t-31fb41df1b710071a91759ca8605366b88ced81477bdbe34ac9191e175f8cec43</cites><orcidid>0000-0002-5119-0372 ; 0000-0001-8537-6100 ; 0000-0002-5447-7264</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/PMC7750005/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7750005/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33362982$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Driscoll, Timothy P</creatorcontrib><creatorcontrib>Verhoeve, Victoria I</creatorcontrib><creatorcontrib>Brockway, Cassia</creatorcontrib><creatorcontrib>Shrewsberry, Darin L</creatorcontrib><creatorcontrib>Plumer, Mariah</creatorcontrib><creatorcontrib>Sevdalis, Spiridon E</creatorcontrib><creatorcontrib>Beckmann, John F</creatorcontrib><creatorcontrib>Krueger, Laura M</creatorcontrib><creatorcontrib>Macaluso, Kevin R</creatorcontrib><creatorcontrib>Azad, Abdu F</creatorcontrib><creatorcontrib>Gillespie, Joseph J</creatorcontrib><title>Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas</title><title>PeerJ (San Francisco, CA)</title><addtitle>PeerJ</addtitle><description>Wolbachiae are obligate intracellular bacteria that infect arthropods and certain nematodes. Usually maternally inherited, they may provision nutrients to (mutualism) or alter sexual biology of (reproductive parasitism) their invertebrate hosts. We report the assembly of closed genomes for two novel wolbachiae,
CfeT and
CfeJ, found co-infecting cat fleas (
) of the Elward Laboratory colony (Soquel, CA, USA).
CfeT is basal to nearly all described
supergroups, while
CfeJ is related to supergroups C, D and F. Both genomes contain laterally transferred genes that inform on the evolution of
host associations.
CfeT carries the Biotin synthesis Operon of Obligate intracellular Microbes (BOOM); our analyses reveal five independent acquisitions of BOOM across the
tree, indicating parallel evolution towards mutualism. Alternately,
CfeJ harbors a toxin-antidote operon analogous to the
Pip
operon recently characterized as an inducer of cytoplasmic incompatibility (CI) in flies.
CfeJ
and three adjacent genes are collectively similar to large modular toxins encoded in CI-like operons of certain
strains and
species, signifying that CI toxins streamline by fission of large modular toxins. Remarkably, the
.
genome itself contains two CI-like antidote genes, divergent from
CfeJ
, revealing episodic reproductive parasitism in cat fleas and evidencing mobility of CI loci independent of WO-phage. Additional screening revealed predominant co-infection (
CfeT/
CfeJ) amongst
.
colonies, though fleas in wild populations mostly harbor
CfeT alone. Collectively, genomes of
CfeT,
CfeJ, and their cat flea host supply instances of lateral gene transfers that could drive transitions between parasitism and mutualism.</description><subject>Biosynthesis</subject><subject>Biotin</subject><subject>Colonies</subject><subject>Concurrent infection</subject><subject>Cytoplasmic incompatibility</subject><subject>Divergence</subject><subject>Entomology</subject><subject>Evolution</subject><subject>Evolutionary genetics</subject><subject>Evolutionary Studies</subject><subject>Genes</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Infections</subject><subject>Intracellular</subject><subject>Invertebrates</subject><subject>Microbiology</subject><subject>Mutualism</subject><subject>Nematodes</subject><subject>Nutrients</subject><subject>Operons</subject><subject>Parasites</subject><subject>Parasitism</subject><subject>Phages</subject><subject>Siphonaptera</subject><subject>Strains (organisms)</subject><subject>Wolbachia</subject><subject>Zoology</subject><issn>2167-8359</issn><issn>2167-8359</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><recordid>eNpdkctrHSEYxaU0NCHJqvsidFMIk-g4o04XhRDygkA2CV2K42iuF0enPm7pfx9vXqRx4yfnx-F8HgC-YnTMGGYni9ZxfYwR7egnsNdiyhpO-uHzu3kXHKa0RvXwliJOvoBdQghtB97ugXK-Ca5kGzwMBv4ObpRqZSWcSy7S2TRD6ScY9RLDVFS2Gw0XGWWyuWo_ofXJPqwyNDHMMP8N0IeNdjDlKKsE80pmqEJjvdGqTvVlnJbpAOwY6ZI-fLn3wf3F-d3ZVXNze3l9dnrTKMLa3BBsxg5PBo8MI8SwHDDrByU5RT2hdORc6YnjjrFxGjXppBrwgHWFTFVUR_bBr2ffpYyznpT2NZgTS7SzjP9EkFb8r3i7Eg9hIxjr63_11eDHi0EMf4pOWcw2Ke2c9DqUJNqOkQ71Axkq-v0Dug4l-rrelkKMc0a3hkfPlIohpajNWxiMxLZR8dSoeGq00t_e539jX_sjj06Lnzg</recordid><startdate>20201217</startdate><enddate>20201217</enddate><creator>Driscoll, Timothy P</creator><creator>Verhoeve, Victoria I</creator><creator>Brockway, Cassia</creator><creator>Shrewsberry, Darin L</creator><creator>Plumer, Mariah</creator><creator>Sevdalis, Spiridon E</creator><creator>Beckmann, John F</creator><creator>Krueger, Laura M</creator><creator>Macaluso, Kevin R</creator><creator>Azad, Abdu F</creator><creator>Gillespie, Joseph J</creator><general>PeerJ, Inc</general><general>PeerJ Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7XB</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5119-0372</orcidid><orcidid>https://orcid.org/0000-0001-8537-6100</orcidid><orcidid>https://orcid.org/0000-0002-5447-7264</orcidid></search><sort><creationdate>20201217</creationdate><title>Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas</title><author>Driscoll, Timothy P ; Verhoeve, Victoria I ; Brockway, Cassia ; Shrewsberry, Darin L ; Plumer, Mariah ; Sevdalis, Spiridon E ; Beckmann, John F ; Krueger, Laura M ; Macaluso, Kevin R ; Azad, Abdu F ; Gillespie, Joseph J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c372t-31fb41df1b710071a91759ca8605366b88ced81477bdbe34ac9191e175f8cec43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Biosynthesis</topic><topic>Biotin</topic><topic>Colonies</topic><topic>Concurrent infection</topic><topic>Cytoplasmic incompatibility</topic><topic>Divergence</topic><topic>Entomology</topic><topic>Evolution</topic><topic>Evolutionary genetics</topic><topic>Evolutionary Studies</topic><topic>Genes</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Infections</topic><topic>Intracellular</topic><topic>Invertebrates</topic><topic>Microbiology</topic><topic>Mutualism</topic><topic>Nematodes</topic><topic>Nutrients</topic><topic>Operons</topic><topic>Parasites</topic><topic>Parasitism</topic><topic>Phages</topic><topic>Siphonaptera</topic><topic>Strains (organisms)</topic><topic>Wolbachia</topic><topic>Zoology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Driscoll, Timothy P</creatorcontrib><creatorcontrib>Verhoeve, Victoria I</creatorcontrib><creatorcontrib>Brockway, Cassia</creatorcontrib><creatorcontrib>Shrewsberry, Darin L</creatorcontrib><creatorcontrib>Plumer, Mariah</creatorcontrib><creatorcontrib>Sevdalis, Spiridon E</creatorcontrib><creatorcontrib>Beckmann, John F</creatorcontrib><creatorcontrib>Krueger, Laura M</creatorcontrib><creatorcontrib>Macaluso, Kevin R</creatorcontrib><creatorcontrib>Azad, Abdu F</creatorcontrib><creatorcontrib>Gillespie, Joseph J</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection (ProQuest)</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Science Database</collection><collection>Biological Science Database</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><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PeerJ (San Francisco, CA)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Driscoll, Timothy P</au><au>Verhoeve, Victoria I</au><au>Brockway, Cassia</au><au>Shrewsberry, Darin L</au><au>Plumer, Mariah</au><au>Sevdalis, Spiridon E</au><au>Beckmann, John F</au><au>Krueger, Laura M</au><au>Macaluso, Kevin R</au><au>Azad, Abdu F</au><au>Gillespie, Joseph J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas</atitle><jtitle>PeerJ (San Francisco, CA)</jtitle><addtitle>PeerJ</addtitle><date>2020-12-17</date><risdate>2020</risdate><volume>8</volume><spage>e10646</spage><pages>e10646-</pages><artnum>e10646</artnum><issn>2167-8359</issn><eissn>2167-8359</eissn><abstract>Wolbachiae are obligate intracellular bacteria that infect arthropods and certain nematodes. Usually maternally inherited, they may provision nutrients to (mutualism) or alter sexual biology of (reproductive parasitism) their invertebrate hosts. We report the assembly of closed genomes for two novel wolbachiae,
CfeT and
CfeJ, found co-infecting cat fleas (
) of the Elward Laboratory colony (Soquel, CA, USA).
CfeT is basal to nearly all described
supergroups, while
CfeJ is related to supergroups C, D and F. Both genomes contain laterally transferred genes that inform on the evolution of
host associations.
CfeT carries the Biotin synthesis Operon of Obligate intracellular Microbes (BOOM); our analyses reveal five independent acquisitions of BOOM across the
tree, indicating parallel evolution towards mutualism. Alternately,
CfeJ harbors a toxin-antidote operon analogous to the
Pip
operon recently characterized as an inducer of cytoplasmic incompatibility (CI) in flies.
CfeJ
and three adjacent genes are collectively similar to large modular toxins encoded in CI-like operons of certain
strains and
species, signifying that CI toxins streamline by fission of large modular toxins. Remarkably, the
.
genome itself contains two CI-like antidote genes, divergent from
CfeJ
, revealing episodic reproductive parasitism in cat fleas and evidencing mobility of CI loci independent of WO-phage. Additional screening revealed predominant co-infection (
CfeT/
CfeJ) amongst
.
colonies, though fleas in wild populations mostly harbor
CfeT alone. Collectively, genomes of
CfeT,
CfeJ, and their cat flea host supply instances of lateral gene transfers that could drive transitions between parasitism and mutualism.</abstract><cop>United States</cop><pub>PeerJ, Inc</pub><pmid>33362982</pmid><doi>10.7717/peerj.10646</doi><orcidid>https://orcid.org/0000-0002-5119-0372</orcidid><orcidid>https://orcid.org/0000-0001-8537-6100</orcidid><orcidid>https://orcid.org/0000-0002-5447-7264</orcidid><oa>free_for_read</oa></addata></record> |
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| source | DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Biosynthesis Biotin Colonies Concurrent infection Cytoplasmic incompatibility Divergence Entomology Evolution Evolutionary genetics Evolutionary Studies Genes Genomes Genomics Infections Intracellular Invertebrates Microbiology Mutualism Nematodes Nutrients Operons Parasites Parasitism Phages Siphonaptera Strains (organisms) Wolbachia Zoology |
| title | Evolution of Wolbachia mutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas |
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