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Fiber-Associated Spirochetes Are Major Agents of Hemicellulose Degradation in the Hindgut of Wood-Feeding Higher Termites

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Fiber-Associated Spirochetes Are Major Agents of Hemicellulose Degradation in the Hindgut of Wood-Feeding Higher Termites Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites Gaku Tokudaa,b,1, Aram Mikaelyanc,d, Chiho Fukuia, Yu Matsuuraa, Hirofumi Watanabee, Masahiro Fujishimaf, and Andreas Brunec 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; 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; eBiomolecular Mimetics Research Unit, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, 305-8634 Ibaraki, Japan; and fDepartment of Sciences, Graduate School of Sciences and Technology for Innovation, Yamaguchi University, Yoshida 1677-1, 753-8512 Yamaguchi, Japan Edited by Nancy A. Moran, University of Texas at Austin, Austin, TX, and approved November 5, 2018 (received for review June 25, 2018) Symbiotic digestion of lignocellulose in wood-feeding higher digestion in the hindgut of higher termites must be attributed to termites (family Termitidae) is a two-step process that involves their entirely prokaryotic microbial community (5). endogenous host cellulases secreted in the midgut and a dense The gut microbiota of higher termites comprises more than bacterial community in the hindgut compartment. The genomes of 1,000 bacterial phylotypes, which are organized into distinc- the bacterial gut microbiota encode diverse cellulolytic and hemi- tive communities colonizing the microhabitats provided by the cellulolytic enzymes, but the contributions of host and bacterial compartmentalized intestine, including the highly differentiated symbionts to lignocellulose degradation remain ambiguous. Our hindgut (6, 7). Of particular interest are the bacteria associated previous studies of Nasutitermes spp. documented that the wood with wood particles in the dilated hindgut paunch of wood- fibers in the hindgut paunch are consistently colonized not only by feeding Nasutitermes species; these bacteria represent less than uncultured members of Fibrobacteres, which have been implicated 30% of the total microbial population but contribute more than MICROBIOLOGY in cellulose degradation, but also by unique lineages of Spiro- half of the cellulolytic activity in this compartment (8). Core chaetes. Here, we demonstrate that the degradation of xylan, members of the fiber-associated community are several so-far the major component of hemicellulose, is restricted to the hindgut uncultured lineages of Fibrobacteres and the closely related compartment, where it is preferentially hydrolyzed over cellulose. candidate phylum TG3 (now classified as Fibrobacteria and Metatranscriptomic analysis documented that the majority of gly- coside hydrolase (GH) transcripts expressed by the fiber-associated Chitinivibrionia; ref. 9) and two lineages of uncultured Spiro- bacterial community belong to family GH11, which consists exclu- chaetes (Treponema Ic and If), which represent a separate line of sively of xylanases. The substrate specificity was further confirmed descent that has been found exclusively in higher termites (8). by heterologous expression of the gene encoding the predomi- nant homolog. Although the most abundant transcripts of Significance GH11 in Nasutitermes takasagoensis were phylogenetically placed among their homologs of Firmicutes, immunofluorescence micros- Xylan, the major hemicellulosic component of lignocellulose copy, compositional binning of metagenomics contigs, and the and the second most abundant polysaccharide after cellulose, genomic context of the homologs indicated that they are encoded contributes to the structural stability of wood and its re- by Spirochaetes and were most likely obtained by horizontal gene calcitrance to enzymatic digestion. The present study identifies transfer among the intestinal microbiota. The major role of spiro- Spirochaetes as primary agents of xylan degradation in the chetes in xylan degradation is unprecedented and assigns the hindgut of wood-feeding higher termites, in contrast to the fiber-associated Treponema clades in the hindgut of wood- bovine rumen or the human colon, where Bacteroidetes are feeding higher termites a prominent part in the breakdown responsible for hydrolysis of xylan in grass or cereals. The of hemicelluloses. presence of distinctive xylanases in Spirochaetes was so far undocumented to our knowledge. Their phylogenetic origin metatranscriptome | xylanase | spirochetes | fiber-associated community | among gut bacteria of other phyla identifies horizontal gene termite hindgut transfer among the intestinal microbiota as an important driver in the evolutionary adaptation of higher termites to different ignocellulose is the most abundant biopolymer in terrestrial lignocellulosic diets. Lenvironments (1). It consists mainly of cellulose, hemi- Author contributions: G.T., A.M., Y.M., and A.B. designed research; G.T., C.F., Y.M., H.W., cellulose, and lignin, and is remarkably recalcitrant to microbial and M.F. performed research; G.T., A.M., Y.M., and A.B. analyzed data; and G.T., A.M., degradation. The ability of termites to efficiently digest ligno- Y.M., and A.B. wrote the paper. cellulose has a large impact on the global ecosystem (1). The The authors declare no conflict of interest. elucidation of the underlying mechanisms has presented a for- This article is a PNAS Direct Submission. midable challenge to research for almost a century (2). Termites Published under the PNAS license. of phylogenetically basal lineages (“lower termites”) harbor Data deposition: The data reported in this paper have been deposited in the sequence symbiotic protists in their enlarged hindgut compartment that read archive of the DNA Data Bank Japan (DDBJ) under accession nos. DRA005983 (meta- transcriptomes) and DRA005967 (metagenome). The complete sequence of the cloned phagocytize wood particles and play a crucial role in cellulose GH11 gene (NtSymX11) was deposited in GenBank/European Nucleotide Archive/DDBJ and hemicellulose degradation (3). By contrast, termites of the database under accession no. LC311413. phylogenetically most apical lineage (“higher termites”), which 1To whom correspondence should be addressed. Email: [email protected]. account for approximately two thirds of all termite species, are This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. devoid of such eukaryotic symbionts (4). As a consequence, fiber 1073/pnas.1810550115/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1810550115 PNAS Latest Articles | 1of9 Downloaded by guest on September 29, 2021 Previous metagenomic analyses (i.e., the comprehensive se- we measured hydrolytic activity against beechwood xylan in sol- quencing of the genetic material of an entire microbial com- uble (supernatant) and particulate (pellet) fractions of homog- munity) had already reported the presence of diverse genes enates of salivary glands and individual gut sections by using a encoding putative cellulases and hemicellulases in the pro- previously described protocol (21, 25). Xylanase activity was karyotic hindgut microbiota of higher termites (10–15). In the essentially confined to the hindgut proper, and the activity in the case of the wood-feeding Nasutitermes corniger, many of these particulate fraction (1.42 ± 0.19 U/g termite) exceeded that in genes were tentatively assigned to members of the Fibrobacteres the soluble fraction (0.36 ± 0.32 U/g termite) fourfold (Fig. 1), and Spirochaetes (10). Metagenomic binning revealed that the which suggests that most of the activity is associated with wood genomes of Fibrobacteres encode an abundance of cellulase particles, bacterial cells, or both. Xylanase activities in salivary genes and more hemicellulase genes than the average number in glands, foregut, and mixed segment were below the detection other cellulolytic bacteria. However, these genomes lack the limit (0.02 U/g termite), whereas midgut sections occasionally genes required to metabolize xylose (9), a major component of showed trace activities in some preparations (0.03 ± 0.06 U/g xylan and other hemicelluloses of wood (16). Moreover, none of termite; n = 5). When we compared xylanase activities with the Fibrobacteres from termite guts have been cultured, and cellulolytic activities in the hindgut, we found that xylanase ac- their hemicellulolytic ability remains to be elucidated. Spirochaetes likely play a crucial role in reductive aceto- tivities were in the same range as cellulolytic activities against carboxymethylcellulose (CMC) and more than an order of genesis, the production of acetate from H2 and CO2 by anaerobic bacteria, which is an important reaction in the hindgut of lower magnitude higher than activities against microcrystalline cellu- and higher termites (17–19). Although metagenomes of hindgut lose (Fig. 1). Moreover, activities against CMC and microcrys- contents of Nasutitermes spp. provided evidence that spirochetes talline cellulose were more evenly distributed between the carry genes encoding glycoside hydrolases (GHs) (10), a direct soluble and particulate fractions, which is in agreement with involvement of fiber-associated spirochetes in the degradation of previous reports (8, 21). These results suggest that
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