Host-Symbiont Cospeciation of Termite-Gut Cellulolytic Protists of the Genera Teranympha and Eucomonympha and their Treponema Endosymbionts
Cellulolytic flagellated protists inhabit the hindgut of termites. They are unique and essential to termites and related wood-feeding cockroaches, enabling host feeding on cellulosic matter. Protists of two genera in the family Teranymphidae (phylum Parabasalia), Eucomonympha and Teranympha, are phy...
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| Veröffentlicht in: | Microbes and Environments 2018, Vol.33(1), pp.26-33 |
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| creator | Noda, Satoko Shimizu, Daichi Yuki, Masahiro Kitade, Osamu Ohkuma, Moriya |
| description | Cellulolytic flagellated protists inhabit the hindgut of termites. They are unique and essential to termites and related wood-feeding cockroaches, enabling host feeding on cellulosic matter. Protists of two genera in the family Teranymphidae (phylum Parabasalia), Eucomonympha and Teranympha, are phylogenetically closely related and harbor intracellular endosymbiotic bacteria from the genus Treponema. In order to obtain a clearer understanding of the evolutionary history of this triplex symbiotic relationship, the molecular phylogenies of the three symbiotic partners, the Teranymphidae protists, their Treponema endosymbionts, and their host termites, were inferred and compared. Strong congruence was observed in the tree topologies of all interacting partners, implying their cospeciating relationships. In contrast, the coevolutionary relationship between the Eucomonympha protists and their endosymbionts was more complex, and evidence of incongruence against cospeciating relationships suggested frequent host switches of the endosymbionts, possibly because multiple Eucomonympha species are present in the same gut community. Similarities in the 16S rRNA and gyrB gene sequences of the endosymbionts were higher among Teranympha spp. (>99.25% and >97.2%, respectively), whereas those between Teranympha and Eucomonympha were lower ( |
| doi_str_mv | 10.1264/jsme2.ME17096 |
| format | Article |
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They are unique and essential to termites and related wood-feeding cockroaches, enabling host feeding on cellulosic matter. Protists of two genera in the family Teranymphidae (phylum Parabasalia), Eucomonympha and Teranympha, are phylogenetically closely related and harbor intracellular endosymbiotic bacteria from the genus Treponema. In order to obtain a clearer understanding of the evolutionary history of this triplex symbiotic relationship, the molecular phylogenies of the three symbiotic partners, the Teranymphidae protists, their Treponema endosymbionts, and their host termites, were inferred and compared. Strong congruence was observed in the tree topologies of all interacting partners, implying their cospeciating relationships. In contrast, the coevolutionary relationship between the Eucomonympha protists and their endosymbionts was more complex, and evidence of incongruence against cospeciating relationships suggested frequent host switches of the endosymbionts, possibly because multiple Eucomonympha species are present in the same gut community. Similarities in the 16S rRNA and gyrB gene sequences of the endosymbionts were higher among Teranympha spp. (>99.25% and >97.2%, respectively), whereas those between Teranympha and Eucomonympha were lower (<97.1% and <91.9%, respectively). In addition, the endosymbionts of Teranympha spp. formed a phylogenetic clade distinct from those of Eucomonympha spp. Therefore, the endosymbiont species of Teranympha spp., designated here as “Candidatus Treponema teratonymphae”, needs to be classified as a species distinct from the endosymbiont species of Eucomonympha spp.</description><identifier>ISSN: 1342-6311</identifier><identifier>EISSN: 1347-4405</identifier><identifier>DOI: 10.1264/jsme2.ME17096</identifier><identifier>PMID: 29367472</identifier><language>eng</language><publisher>Japan: Japanese Society of Microbial Ecology / Japanese Society of Soil Microbiology / Taiwan Society of Microbial Ecology / Japanese Society of Plant Microbe Interactions / Japanese Society for Extremophiles</publisher><subject>Animals ; Bacteria ; Cockroaches ; cospeciation ; DNA topoisomerase ; DNA, Bacterial - genetics ; Endosymbionts ; endosymbiotic bacteria ; Evolution, Molecular ; Feeding ; Gastrointestinal Microbiome ; Gene sequencing ; Genera ; Hindgut ; Host alternation ; Isoptera ; Isoptera - genetics ; Isoptera - microbiology ; Parabasalidea - genetics ; Parabasalidea - physiology ; Phylogeny ; Protists ; RNA, Ribosomal, 16S ; rRNA 16S ; Sequence Analysis, DNA ; Species ; Species classification ; Switches ; Symbionts ; Symbiosis ; Teranymphidae protist ; termite ; Treponema ; Treponema - genetics ; Treponema - physiology ; Wood</subject><ispartof>Microbes and Environments, 2018, Vol.33(1), pp.26-33</ispartof><rights>2018 by Japanese Society of Microbial Ecology / Japanese Society of Soil Microbiology / Taiwan Society of Microbial Ecology / Japanese Society of Plant Microbe Interactions.</rights><rights>Copyright Japan Science and Technology Agency 2018</rights><rights>Copyright © 2018 by Japanese Society of Microbial Ecology / Japanese Society of Soil Microbiology / Taiwan Society of Microbial Ecology / Japanese Society of Plant Microbe Interactions. 2018</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5006-1e3a6248f76120745182d5dd8c6a0b3bd15d25cdaed9eadee1b35c8e5c1686583</citedby><cites>FETCH-LOGICAL-c5006-1e3a6248f76120745182d5dd8c6a0b3bd15d25cdaed9eadee1b35c8e5c1686583</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5877339/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5877339/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,1877,4010,27900,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29367472$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Noda, Satoko</creatorcontrib><creatorcontrib>Shimizu, Daichi</creatorcontrib><creatorcontrib>Yuki, Masahiro</creatorcontrib><creatorcontrib>Kitade, Osamu</creatorcontrib><creatorcontrib>Ohkuma, Moriya</creatorcontrib><title>Host-Symbiont Cospeciation of Termite-Gut Cellulolytic Protists of the Genera Teranympha and Eucomonympha and their Treponema Endosymbionts</title><title>Microbes and Environments</title><addtitle>Microbes Environ.</addtitle><description>Cellulolytic flagellated protists inhabit the hindgut of termites. They are unique and essential to termites and related wood-feeding cockroaches, enabling host feeding on cellulosic matter. Protists of two genera in the family Teranymphidae (phylum Parabasalia), Eucomonympha and Teranympha, are phylogenetically closely related and harbor intracellular endosymbiotic bacteria from the genus Treponema. In order to obtain a clearer understanding of the evolutionary history of this triplex symbiotic relationship, the molecular phylogenies of the three symbiotic partners, the Teranymphidae protists, their Treponema endosymbionts, and their host termites, were inferred and compared. Strong congruence was observed in the tree topologies of all interacting partners, implying their cospeciating relationships. In contrast, the coevolutionary relationship between the Eucomonympha protists and their endosymbionts was more complex, and evidence of incongruence against cospeciating relationships suggested frequent host switches of the endosymbionts, possibly because multiple Eucomonympha species are present in the same gut community. Similarities in the 16S rRNA and gyrB gene sequences of the endosymbionts were higher among Teranympha spp. (>99.25% and >97.2%, respectively), whereas those between Teranympha and Eucomonympha were lower (<97.1% and <91.9%, respectively). In addition, the endosymbionts of Teranympha spp. formed a phylogenetic clade distinct from those of Eucomonympha spp. Therefore, the endosymbiont species of Teranympha spp., designated here as “Candidatus Treponema teratonymphae”, needs to be classified as a species distinct from the endosymbiont species of Eucomonympha spp.</description><subject>Animals</subject><subject>Bacteria</subject><subject>Cockroaches</subject><subject>cospeciation</subject><subject>DNA topoisomerase</subject><subject>DNA, Bacterial - genetics</subject><subject>Endosymbionts</subject><subject>endosymbiotic bacteria</subject><subject>Evolution, Molecular</subject><subject>Feeding</subject><subject>Gastrointestinal Microbiome</subject><subject>Gene sequencing</subject><subject>Genera</subject><subject>Hindgut</subject><subject>Host alternation</subject><subject>Isoptera</subject><subject>Isoptera - genetics</subject><subject>Isoptera - microbiology</subject><subject>Parabasalidea - genetics</subject><subject>Parabasalidea - physiology</subject><subject>Phylogeny</subject><subject>Protists</subject><subject>RNA, Ribosomal, 16S</subject><subject>rRNA 16S</subject><subject>Sequence Analysis, DNA</subject><subject>Species</subject><subject>Species classification</subject><subject>Switches</subject><subject>Symbionts</subject><subject>Symbiosis</subject><subject>Teranymphidae protist</subject><subject>termite</subject><subject>Treponema</subject><subject>Treponema - genetics</subject><subject>Treponema - physiology</subject><subject>Wood</subject><issn>1342-6311</issn><issn>1347-4405</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkU9rGzEQxUVpadK0x16LoOdN9WelXV8KxThOIaGFumehlcaxzK60lbQFf4Z-6cjx1iSX0YzejzcDD6GPlFxTJusv-zQAu75f0YYs5Ct0SXndVHVNxOunnlWSU3qB3qW0J4Rz0bC36IItuGzqhl2if7ch5erXYehc8BkvQxrBOJ3LhMMWbyAOLkO1nooGfT_1oT9kZ_DPGLJLOR2hvAO8Bg9RH3ntD8O401h7i1eTCUN49lFQF_Emwhg8DBqvvA1pXp7eozdb3Sf4ML9X6PfNarO8re5-rL8vv91VRhAiKwpcS1a320ZSRppa0JZZYW1rpCYd7ywVlgljNdgFaAtAOy5MC8JQ2UrR8iv09eQ7Tt0A1oDPUfdqjG7Q8aCCduql4t1OPYS_SrRNw_miGHyeDWL4M0HKah-m6MvNihHGKOWEyUJVJ8rEkFKE7XkDJeqYnXrKTs3ZFf7T87PO9P-wCrA8AfuU9QOcAR1LIj3Mdpwreiyz7Vk1Ox0VeP4I0MGx3g</recordid><startdate>2018</startdate><enddate>2018</enddate><creator>Noda, Satoko</creator><creator>Shimizu, Daichi</creator><creator>Yuki, Masahiro</creator><creator>Kitade, Osamu</creator><creator>Ohkuma, Moriya</creator><general>Japanese Society of Microbial Ecology / Japanese Society of Soil Microbiology / Taiwan Society of Microbial Ecology / Japanese Society of Plant Microbe Interactions / Japanese Society for Extremophiles</general><general>Japan Science and Technology Agency</general><general>the Japanese Society of Microbial Ecology (JSME)/the Japanese Society of Soil Microbiology (JSSM)/the Taiwan Society of Microbial Ecology (TSME)/the Japanese Society of Plant Microbe Interactions (JSPMI)</general><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>C1K</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>5PM</scope></search><sort><creationdate>2018</creationdate><title>Host-Symbiont Cospeciation of Termite-Gut Cellulolytic Protists of the Genera Teranympha and Eucomonympha and their Treponema Endosymbionts</title><author>Noda, Satoko ; Shimizu, Daichi ; Yuki, Masahiro ; Kitade, Osamu ; Ohkuma, Moriya</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5006-1e3a6248f76120745182d5dd8c6a0b3bd15d25cdaed9eadee1b35c8e5c1686583</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Animals</topic><topic>Bacteria</topic><topic>Cockroaches</topic><topic>cospeciation</topic><topic>DNA topoisomerase</topic><topic>DNA, Bacterial - genetics</topic><topic>Endosymbionts</topic><topic>endosymbiotic bacteria</topic><topic>Evolution, Molecular</topic><topic>Feeding</topic><topic>Gastrointestinal Microbiome</topic><topic>Gene sequencing</topic><topic>Genera</topic><topic>Hindgut</topic><topic>Host alternation</topic><topic>Isoptera</topic><topic>Isoptera - genetics</topic><topic>Isoptera - microbiology</topic><topic>Parabasalidea - genetics</topic><topic>Parabasalidea - physiology</topic><topic>Phylogeny</topic><topic>Protists</topic><topic>RNA, Ribosomal, 16S</topic><topic>rRNA 16S</topic><topic>Sequence Analysis, DNA</topic><topic>Species</topic><topic>Species classification</topic><topic>Switches</topic><topic>Symbionts</topic><topic>Symbiosis</topic><topic>Teranymphidae protist</topic><topic>termite</topic><topic>Treponema</topic><topic>Treponema - genetics</topic><topic>Treponema - physiology</topic><topic>Wood</topic><toplevel>online_resources</toplevel><creatorcontrib>Noda, Satoko</creatorcontrib><creatorcontrib>Shimizu, Daichi</creatorcontrib><creatorcontrib>Yuki, Masahiro</creatorcontrib><creatorcontrib>Kitade, Osamu</creatorcontrib><creatorcontrib>Ohkuma, Moriya</creatorcontrib><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>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Microbes and Environments</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Noda, Satoko</au><au>Shimizu, Daichi</au><au>Yuki, Masahiro</au><au>Kitade, Osamu</au><au>Ohkuma, Moriya</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Host-Symbiont Cospeciation of Termite-Gut Cellulolytic Protists of the Genera Teranympha and Eucomonympha and their Treponema Endosymbionts</atitle><jtitle>Microbes and Environments</jtitle><addtitle>Microbes Environ.</addtitle><date>2018</date><risdate>2018</risdate><volume>33</volume><issue>1</issue><spage>26</spage><epage>33</epage><pages>26-33</pages><issn>1342-6311</issn><eissn>1347-4405</eissn><abstract>Cellulolytic flagellated protists inhabit the hindgut of termites. They are unique and essential to termites and related wood-feeding cockroaches, enabling host feeding on cellulosic matter. Protists of two genera in the family Teranymphidae (phylum Parabasalia), Eucomonympha and Teranympha, are phylogenetically closely related and harbor intracellular endosymbiotic bacteria from the genus Treponema. In order to obtain a clearer understanding of the evolutionary history of this triplex symbiotic relationship, the molecular phylogenies of the three symbiotic partners, the Teranymphidae protists, their Treponema endosymbionts, and their host termites, were inferred and compared. Strong congruence was observed in the tree topologies of all interacting partners, implying their cospeciating relationships. In contrast, the coevolutionary relationship between the Eucomonympha protists and their endosymbionts was more complex, and evidence of incongruence against cospeciating relationships suggested frequent host switches of the endosymbionts, possibly because multiple Eucomonympha species are present in the same gut community. Similarities in the 16S rRNA and gyrB gene sequences of the endosymbionts were higher among Teranympha spp. (>99.25% and >97.2%, respectively), whereas those between Teranympha and Eucomonympha were lower (<97.1% and <91.9%, respectively). In addition, the endosymbionts of Teranympha spp. formed a phylogenetic clade distinct from those of Eucomonympha spp. Therefore, the endosymbiont species of Teranympha spp., designated here as “Candidatus Treponema teratonymphae”, needs to be classified as a species distinct from the endosymbiont species of Eucomonympha spp.</abstract><cop>Japan</cop><pub>Japanese Society of Microbial Ecology / Japanese Society of Soil Microbiology / Taiwan Society of Microbial Ecology / Japanese Society of Plant Microbe Interactions / Japanese Society for Extremophiles</pub><pmid>29367472</pmid><doi>10.1264/jsme2.ME17096</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Bacteria Cockroaches cospeciation DNA topoisomerase DNA, Bacterial - genetics Endosymbionts endosymbiotic bacteria Evolution, Molecular Feeding Gastrointestinal Microbiome Gene sequencing Genera Hindgut Host alternation Isoptera Isoptera - genetics Isoptera - microbiology Parabasalidea - genetics Parabasalidea - physiology Phylogeny Protists RNA, Ribosomal, 16S rRNA 16S Sequence Analysis, DNA Species Species classification Switches Symbionts Symbiosis Teranymphidae protist termite Treponema Treponema - genetics Treponema - physiology Wood |
| title | Host-Symbiont Cospeciation of Termite-Gut Cellulolytic Protists of the Genera Teranympha and Eucomonympha and their Treponema Endosymbionts |
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