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Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites

Gaku Tokuda, Aram Mikaelyan, Chiho Fukui, Yu Matsuura, Hirofumi Watanabe, Masahiro Fujishima, and Andreas Brune
PNAS December 18, 2018 115 (51) E11996-E12004; published ahead of print November 30, 2018 https://doi.org/10.1073/pnas.1810550115
Gaku Tokuda
aTropical Biosphere Research Center, Center of Molecular Biosciences, University of the Ryukyus, Nishihara, 903-0213 Okinawa, Japan;bGraduate School of Engineering and Science, University of the Ryukyus, Nishihara, 903-0213 Okinawa, Japan;
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  • ORCID record for Gaku Tokuda
  • For correspondence: tokuda@comb.u-ryukyu.ac.jp
Aram Mikaelyan
cResearch Group Insect Gut Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany;dDepartment of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27607;
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Chiho Fukui
aTropical Biosphere Research Center, Center of Molecular Biosciences, University of the Ryukyus, Nishihara, 903-0213 Okinawa, Japan;
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Yu Matsuura
aTropical Biosphere Research Center, Center of Molecular Biosciences, University of the Ryukyus, Nishihara, 903-0213 Okinawa, Japan;
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Hirofumi Watanabe
eBiomolecular Mimetics Research Unit, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, 305-8634 Ibaraki, Japan;
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Masahiro Fujishima
fDepartment of Sciences, Graduate School of Sciences and Technology for Innovation, Yamaguchi University, Yoshida 1677-1, 753-8512 Yamaguchi, Japan
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Andreas Brune
cResearch Group Insect Gut Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany;
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  • ORCID record for Andreas Brune
  1. Edited by Nancy A. Moran, University of Texas at Austin, Austin, TX, and approved November 5, 2018 (received for review June 25, 2018)

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Significance

Xylan, the major hemicellulosic component of lignocellulose and the second most abundant polysaccharide after cellulose, contributes to the structural stability of wood and its recalcitrance to enzymatic digestion. The present study identifies Spirochaetes as primary agents of xylan degradation in the hindgut of wood-feeding higher termites, in contrast to the bovine rumen or the human colon, where Bacteroidetes are responsible for hydrolysis of xylan in grass or cereals. The presence of distinctive xylanases in Spirochaetes was so far undocumented to our knowledge. Their phylogenetic origin among gut bacteria of other phyla identifies horizontal gene transfer among the intestinal microbiota as an important driver in the evolutionary adaptation of higher termites to different lignocellulosic diets.

Abstract

Symbiotic digestion of lignocellulose in wood-feeding higher termites (family Termitidae) is a two-step process that involves endogenous host cellulases secreted in the midgut and a dense bacterial community in the hindgut compartment. The genomes of the bacterial gut microbiota encode diverse cellulolytic and hemicellulolytic enzymes, but the contributions of host and bacterial symbionts to lignocellulose degradation remain ambiguous. Our previous studies of Nasutitermes spp. documented that the wood fibers in the hindgut paunch are consistently colonized not only by uncultured members of Fibrobacteres, which have been implicated in cellulose degradation, but also by unique lineages of Spirochaetes. Here, we demonstrate that the degradation of xylan, the major component of hemicellulose, is restricted to the hindgut compartment, where it is preferentially hydrolyzed over cellulose. Metatranscriptomic analysis documented that the majority of glycoside hydrolase (GH) transcripts expressed by the fiber-associated bacterial community belong to family GH11, which consists exclusively of xylanases. The substrate specificity was further confirmed by heterologous expression of the gene encoding the predominant homolog. Although the most abundant transcripts of GH11 in Nasutitermes takasagoensis were phylogenetically placed among their homologs of Firmicutes, immunofluorescence microscopy, compositional binning of metagenomics contigs, and the genomic context of the homologs indicated that they are encoded by Spirochaetes and were most likely obtained by horizontal gene transfer among the intestinal microbiota. The major role of spirochetes in xylan degradation is unprecedented and assigns the fiber-associated Treponema clades in the hindgut of wood-feeding higher termites a prominent part in the breakdown of hemicelluloses.

  • metatranscriptome
  • xylanase
  • spirochetes
  • fiber-associated community
  • termite hindgut

Footnotes

  • ↵1To whom correspondence should be addressed. Email: tokuda{at}comb.u-ryukyu.ac.jp.
  • Author contributions: G.T., A.M., Y.M., and A.B. designed research; G.T., C.F., Y.M., H.W., and M.F. performed research; G.T., A.M., Y.M., and A.B. analyzed data; and G.T., A.M., Y.M., and A.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The data reported in this paper have been deposited in the sequence read archive of the DNA Data Bank Japan (DDBJ) under accession nos. DRA005983 (metatranscriptomes) and DRA005967 (metagenome). The complete sequence of the cloned GH11 gene (NtSymX11) was deposited in GenBank/European Nucleotide Archive/DDBJ database under accession no. LC311413.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1810550115/-/DCSupplemental.

Published under the PNAS license.

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Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites
Gaku Tokuda, Aram Mikaelyan, Chiho Fukui, Yu Matsuura, Hirofumi Watanabe, Masahiro Fujishima, Andreas Brune
Proceedings of the National Academy of Sciences Dec 2018, 115 (51) E11996-E12004; DOI: 10.1073/pnas.1810550115

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Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites
Gaku Tokuda, Aram Mikaelyan, Chiho Fukui, Yu Matsuura, Hirofumi Watanabe, Masahiro Fujishima, Andreas Brune
Proceedings of the National Academy of Sciences Dec 2018, 115 (51) E11996-E12004; DOI: 10.1073/pnas.1810550115
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