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

• Published in: The 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
• Language: English
• 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
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-018-0297-4

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.