Genome analyses of uncultured TG2/ZB3 bacteria in ‘Margulisbacteria’ specifically attached to ectosymbiotic spirochetes of protists in the termite gut

We investigated the phylogenetic diversity, localisation and metabolism of an uncultured bacterial clade, Termite Group 2 (TG2), or ZB3, in the termite gut, which belongs to the candidate phylum ‘Margulisbacteria’. We performed 16S rRNA amplicon sequencing analysis and detected TG2/ZB3 sequences in...

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Published inThe ISME Journal Vol. 13; no. 2; pp. 455 - 467
Main Authors Utami, Yuniar Devi, Kuwahara, Hirokazu, Igai, Katsura, Murakami, Takumi, Sugaya, Kaito, Morikawa, Takahiro, Nagura, Yuichi, Yuki, Masahiro, Deevong, Pinsurang, Inoue, Tetsushi, Kihara, Kumiko, Lo, Nathan, Yamada, Akinori, Ohkuma, Moriya, Hongoh, Yuichi
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.02.2019
Nature Publishing Group
Subjects
13/31
14/32
14/63
45/22
45/23
45/77
631/158/855
631/181/735
631/326/2565/2142
631/326/2565/547
Acetic acid
Acetogenesis
Animals
Bacteria
Bacteria - classification
Bacteria - genetics
Biomedical and Life Sciences
Candidatus Margulisbacteria
Carbon dioxide
Cellobiose
Cellulose
Cellulose acetate
Ecology
Ethanol
Evolutionary Biology
Fluorescence
Genome
Genomes
Hybridization
In Situ Hybridization, Fluorescence
Isoptera - microbiology
Life Sciences
Metabolism
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Multilayers
Phylogeny
RNA, Bacterial - genetics
RNA, Ribosomal, 16S - genetics
rRNA 16S
Spirochaetales - genetics
Spirochetes
Symbionts
Symbiosis
Termites
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Abstract We investigated the phylogenetic diversity, localisation and metabolism of an uncultured bacterial clade, Termite Group 2 (TG2), or ZB3, in the termite gut, which belongs to the candidate phylum ‘Margulisbacteria’. We performed 16S rRNA amplicon sequencing analysis and detected TG2/ZB3 sequences in 40 out of 72 termite and cockroach species, which exclusively constituted a monophyletic cluster in the TG2/ZB3 clade. Fluorescence in situ hybridisation analysis in lower termites revealed that these bacteria are specifically attached to ectosymbiotic spirochetes of oxymonad gut protists. Draft genomes of four TG2/ZB3 phylotypes from a small number of bacterial cells were reconstructed, and functional genome analysis suggested that these bacteria hydrolyse and ferment cellulose/cellobiose to H 2 , CO 2 , acetate and ethanol. We also assembled a draft genome for a partner Treponema spirochete and found that it encoded genes for reductive acetogenesis from H 2 and CO 2 . We hypothesise that the TG2/ZB3 bacteria we report here are commensal or mutualistic symbionts of the spirochetes, exploiting the spirochetes as H 2 sinks. For these bacteria, we propose a novel genus, ‘ Candidatus Termititenax’, which represents a hitherto uncharacterised class-level clade in ‘Margulisbacteria’. Our findings add another layer, i.e., cellular association between bacteria, to the multi-layered symbiotic system in the termite gut.
AbstractList Abstract We investigated the phylogenetic diversity, localisation and metabolism of an uncultured bacterial clade, Termite Group 2 (TG2), or ZB3, in the termite gut, which belongs to the candidate phylum ‘Margulisbacteria’. We performed 16S rRNA amplicon sequencing analysis and detected TG2/ZB3 sequences in 40 out of 72 termite and cockroach species, which exclusively constituted a monophyletic cluster in the TG2/ZB3 clade. Fluorescence in situ hybridisation analysis in lower termites revealed that these bacteria are specifically attached to ectosymbiotic spirochetes of oxymonad gut protists. Draft genomes of four TG2/ZB3 phylotypes from a small number of bacterial cells were reconstructed, and functional genome analysis suggested that these bacteria hydrolyse and ferment cellulose/cellobiose to H2, CO2, acetate and ethanol. We also assembled a draft genome for a partner Treponema spirochete and found that it encoded genes for reductive acetogenesis from H2 and CO2. We hypothesise that the TG2/ZB3 bacteria we report here are commensal or mutualistic symbionts of the spirochetes, exploiting the spirochetes as H2 sinks. For these bacteria, we propose a novel genus, ‘Candidatus Termititenax’, which represents a hitherto uncharacterised class-level clade in ‘Margulisbacteria’. Our findings add another layer, i.e., cellular association between bacteria, to the multi-layered symbiotic system in the termite gut.
We investigated the phylogenetic diversity, localisation and metabolism of an uncultured bacterial clade, Termite Group 2 (TG2), or ZB3, in the termite gut, which belongs to the candidate phylum 'Margulisbacteria'. We performed 16S rRNA amplicon sequencing analysis and detected TG2/ZB3 sequences in 40 out of 72 termite and cockroach species, which exclusively constituted a monophyletic cluster in the TG2/ZB3 clade. Fluorescence in situ hybridisation analysis in lower termites revealed that these bacteria are specifically attached to ectosymbiotic spirochetes of oxymonad gut protists. Draft genomes of four TG2/ZB3 phylotypes from a small number of bacterial cells were reconstructed, and functional genome analysis suggested that these bacteria hydrolyse and ferment cellulose/cellobiose to H , CO , acetate and ethanol. We also assembled a draft genome for a partner Treponema spirochete and found that it encoded genes for reductive acetogenesis from H and CO . We hypothesise that the TG2/ZB3 bacteria we report here are commensal or mutualistic symbionts of the spirochetes, exploiting the spirochetes as H sinks. For these bacteria, we propose a novel genus, 'Candidatus Termititenax', which represents a hitherto uncharacterised class-level clade in 'Margulisbacteria'. Our findings add another layer, i.e., cellular association between bacteria, to the multi-layered symbiotic system in the termite gut.
We investigated the phylogenetic diversity, localisation and metabolism of an uncultured bacterial clade, Termite Group 2 (TG2), or ZB3, in the termite gut, which belongs to the candidate phylum ‘Margulisbacteria’. We performed 16S rRNA amplicon sequencing analysis and detected TG2/ZB3 sequences in 40 out of 72 termite and cockroach species, which exclusively constituted a monophyletic cluster in the TG2/ZB3 clade. Fluorescence in situ hybridisation analysis in lower termites revealed that these bacteria are specifically attached to ectosymbiotic spirochetes of oxymonad gut protists. Draft genomes of four TG2/ZB3 phylotypes from a small number of bacterial cells were reconstructed, and functional genome analysis suggested that these bacteria hydrolyse and ferment cellulose/cellobiose to H 2 , CO 2 , acetate and ethanol. We also assembled a draft genome for a partner Treponema spirochete and found that it encoded genes for reductive acetogenesis from H 2 and CO 2 . We hypothesise that the TG2/ZB3 bacteria we report here are commensal or mutualistic symbionts of the spirochetes, exploiting the spirochetes as H 2 sinks. For these bacteria, we propose a novel genus, ‘ Candidatus Termititenax’, which represents a hitherto uncharacterised class-level clade in ‘Margulisbacteria’. Our findings add another layer, i.e., cellular association between bacteria, to the multi-layered symbiotic system in the termite gut.
We investigated the phylogenetic diversity, localisation and metabolism of an uncultured bacterial clade, Termite Group 2 (TG2), or ZB3, in the termite gut, which belongs to the candidate phylum ‘Margulisbacteria’. We performed 16S rRNA amplicon sequencing analysis and detected TG2/ZB3 sequences in 40 out of 72 termite and cockroach species, which exclusively constituted a monophyletic cluster in the TG2/ZB3 clade. Fluorescence in situ hybridisation analysis in lower termites revealed that these bacteria are specifically attached to ectosymbiotic spirochetes of oxymonad gut protists. Draft genomes of four TG2/ZB3 phylotypes from a small number of bacterial cells were reconstructed, and functional genome analysis suggested that these bacteria hydrolyse and ferment cellulose/cellobiose to H2, CO2, acetate and ethanol. We also assembled a draft genome for a partner Treponema spirochete and found that it encoded genes for reductive acetogenesis from H2 and CO2. We hypothesise that the TG2/ZB3 bacteria we report here are commensal or mutualistic symbionts of the spirochetes, exploiting the spirochetes as H2 sinks. For these bacteria, we propose a novel genus, ‘Candidatus Termititenax’, which represents a hitherto uncharacterised class-level clade in ‘Margulisbacteria’. Our findings add another layer, i.e., cellular association between bacteria, to the multi-layered symbiotic system in the termite gut.
Author Kihara, Kumiko
Kuwahara, Hirokazu
Deevong, Pinsurang
Inoue, Tetsushi
Igai, Katsura
Nagura, Yuichi
Yamada, Akinori
Hongoh, Yuichi
Utami, Yuniar Devi
Morikawa, Takahiro
Lo, Nathan
Murakami, Takumi
Ohkuma, Moriya
Yuki, Masahiro
Sugaya, Kaito
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  organization: Graduate School of Fisheries and Environmental Sciences, Nagasaki University
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30287885$$D View this record in MEDLINE/PubMed
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crossref_primary_10_1038_s41396_018_0297_4
pubmed_primary_30287885
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PublicationCentury 2000
PublicationDate 2019-02-01
PublicationDateYYYYMMDD 2019-02-01
PublicationDate_xml – month: 02
  year: 2019
  text: 2019-02-01
  day: 01
PublicationDecade 2010
PublicationPlace London
PublicationPlace_xml – name: London
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PublicationSubtitle Multidisciplinary Journal of Microbial Ecology
PublicationTitle The ISME Journal
PublicationTitleAbbrev ISME J
PublicationTitleAlternate ISME J
PublicationYear 2019
Publisher Nature Publishing Group UK
Nature Publishing Group
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
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  ident: 2024011300432106600_CR57
  article-title: Cloning and sequence analysis of a new cellulase gene encoding CelK, a major cellulosome component of Clostridium thermocellum: evidence for gene duplication and recombination
  publication-title: J Bacteriol
  doi: 10.1128/JB.181.17.5288-5295.1999
  contributor:
    fullname: Kataeva
– volume: 6
  start-page: e1469
  year: 2016
  ident: 2024011300432106600_CR73
  article-title: A phylogenomic analysis of the bacterial phylum Fibrobacteres
  publication-title: Front Microbiol
  doi: 10.3389/fmicb.2015.01469
  contributor:
    fullname: Abdul Rahman
SSID ssj0057667
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Snippet We investigated the phylogenetic diversity, localisation and metabolism of an uncultured bacterial clade, Termite Group 2 (TG2), or ZB3, in the termite gut,...
Abstract We investigated the phylogenetic diversity, localisation and metabolism of an uncultured bacterial clade, Termite Group 2 (TG2), or ZB3, in the...
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SubjectTerms 13/31
14/32
14/63
45/22
45/23
45/77
631/158/855
631/181/735
631/326/2565/2142
631/326/2565/547
Acetic acid
Acetogenesis
Animals
Bacteria
Bacteria - classification
Bacteria - genetics
Biomedical and Life Sciences
Candidatus Margulisbacteria
Carbon dioxide
Cellobiose
Cellulose
Cellulose acetate
Ecology
Ethanol
Evolutionary Biology
Fluorescence
Genome
Genomes
Hybridization
In Situ Hybridization, Fluorescence
Isoptera - microbiology
Life Sciences
Metabolism
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Multilayers
Phylogeny
RNA, Bacterial - genetics
RNA, Ribosomal, 16S - genetics
rRNA 16S
Spirochaetales - genetics
Spirochetes
Symbionts
Symbiosis
Termites
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Title Genome analyses of uncultured TG2/ZB3 bacteria in ‘Margulisbacteria’ specifically attached to ectosymbiotic spirochetes of protists in the termite gut
URI https://link.springer.com/article/10.1038/s41396-018-0297-4
https://www.ncbi.nlm.nih.gov/pubmed/30287885
https://www.proquest.com/docview/2167021533
https://search.proquest.com/docview/2116845635
https://pubmed.ncbi.nlm.nih.gov/PMC6331581
Volume 13
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