Termites and subsocial roaches inherited many bacterial-borne carbohydrate-active enzymes (CAZymes) from their common ancestor
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
PubMed
39506101
PubMed Central
PMC11541852
DOI
10.1038/s42003-024-07146-w
PII: 10.1038/s42003-024-07146-w
Knihovny.cz E-zdroje
- MeSH
- Bacteria * enzymologie genetika MeSH
- bakteriální proteiny metabolismus genetika MeSH
- fylogeneze * MeSH
- Isoptera * mikrobiologie enzymologie MeSH
- metabolismus sacharidů MeSH
- metagenom MeSH
- molekulární evoluce MeSH
- střevní mikroflóra MeSH
- švábi mikrobiologie enzymologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- bakteriální proteiny MeSH
Termites digest wood using Carbohydrate-Active Enzymes (CAZymes) produced by gut bacteria with whom they have cospeciated at geological timescales. Whether CAZymes were encoded in the genomes of their ancestor's gut bacteria and transmitted to modern termites or acquired more recently from bacteria not associated with termites is unclear. We used gut metagenomes from 195 termites and one Cryptocercus, the sister group of termites, to investigate the evolution of termite gut bacterial CAZymes. We found 420 termite-specific clusters in 81 bacterial CAZyme gene trees, including 404 clusters showing strong cophylogenetic patterns with termites. Of the 420 clusters, 131 included at least one bacterial CAZyme sequence associated with Cryptocercus or Mastotermes, the sister group of all other termites. Our results suggest many bacterial CAZymes have been encoded in the genomes of termite gut bacteria since termite origin, indicating termites rely upon many bacterial CAZymes endemic to their guts to digest wood.
Faculty of Tropical AgriSciences Czech University of Life Sciences Prague Czech Republic
Innovative Genomics Institute University of California Berkeley Berkeley CA 94720 USA
Tropical Biosphere Research Center University of the Ryukyus Okinawa Japan
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Engel, M. S., Barden, P., Riccio, M. L. & Grimaldi, D. A. Morphologically specialized termite castes and advanced sociality in the Early Cretaceous. Curr. Biol.26, 522–530 (2016). PubMed
Lo, N. et al. Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr. Biol.10, 801–804 (2000). PubMed
Inward, D. J. G., Vogler, A. P. & Eggleton, P. A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol. Phylogenet. Evol.44, 953–967 (2007). PubMed
Donovan, S. E., Eggleton, P. & Bignell, D. E. Gut content analysis and a new feeding group classification of termites. Ecol. Entomol.26, 356–366 (2001).
Bourguignon, T. et al. Feeding ecology and phylogenetic structure of a complex neotropical termite assemblage, revealed by nitrogen stable isotope ratios. Ecol. Entomol.36, 261–269 (2011).
Watanabe, H., Noda, H., Tokuda, G. & Lo, N. A cellulase gene of termite origin. Nature394, 330–331 (1998). PubMed
Tokuda, G. et al. Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Mol. Ecol.13, 3219–3228 (2004). PubMed
Brune, A. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol.12, 168–180 (2014). PubMed
Chouvenc, T., Šobotník, J., Engel, M. S. & Bourguignon, T. Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae. Cell. Mol. Life Sci.78, 2749–2769 (2021). PubMed PMC
Rouland-Lefèvre, C. Symbiosis with Fungi. in Termites: Evolution, Sociality, Symbioses, Ecology (eds. Abe, T., Bignell, D.E., Higashi, M.) 289–306 (Springer Netherlands, Dordrecht, 2000). 10.1007/978-94-017-3223-9_14.
Lynd, L. R., Weimer, P. J., van Zyl, W. H. & Pretorius, I. S. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol. Mol. Biol. Rev.66, 506–77 (2002). PubMed PMC
Béguin, P. & Aubert, J.-P. The biological degradation of cellulose. FEMS Microbiol. Rev.13, 25–58 (1994). PubMed
Cantarel, B. L. et al. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res.37, D233–D238 (2009). PubMed PMC
Drula, E. et al. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res.50, D571–D577 (2022). PubMed PMC
Coutinho, P. M., Deleury, E., Davies, G. J. & Henrissat, B. An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol.328, 307–317 (2003). PubMed
Henrissat, B. & Davies, G. Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol.7, 637–644 (1997). PubMed
Lombard, V. et al. A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem. J.432, 437–444 (2010). PubMed
Levasseur, A., Drula, E., Lombard, V., Coutinho, P. M. & Henrissat, B. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol. Biofuels6, 41 (2013). PubMed PMC
Boraston, A. B., Bolam, D. N., Gilbert, H. J. & Davies, G. J. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J.382, 769–781 (2004). PubMed PMC
Arora, J. et al. The functional evolution of termite gut microbiota. Microbiome10, 78 (2022). PubMed PMC
Marynowska, M. et al. Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites. Microbiome8, 96 (2020). PubMed PMC
Warnecke, F. et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature450, 560–565 (2007). PubMed
Watanabe, H. & Tokuda, G. Cellulolytic systems in insects. Annu. Rev. Entomol.55, 609–632 (2010). PubMed
Albersheim, P., Darvill, A., Roberts, K., Sederoff, R. & Staehelin, A. Plant Cell Walls (Garland Science, 2010). 10.1201/9780203833476.
Brune, A. & Ohkuma, M. Role of the termite gut microbiota in symbiotic digestion. In Biology of Termites: a Modern Synthesis (eds. Bignell, D. E., Roisin, Y., Lo, N.) 439–475 (Springer Netherlands, 2010). 10.1007/978-90-481-3977-4_16.
Katsumata, K. S., Jin, Z., Hori, K. & Iiyama, K. Structural changes in lignin of tropical woods during digestion by termite, Cryptotermes brevis. J. Wood Sci.53, 419–426 (2007).
Ebert, D. The epidemiology and evolution of symbionts with mixed-mode transmission. Annu. Rev. Ecol. Evol. Syst.44, 623–643 (2013).
Arora, J. et al. Evidence of cospeciation between termites and their gut bacteria on a geological time scale. Proc. Biol. Sci.290, 20230619 (2023). PubMed PMC
Bourguignon, T. et al. Rampant host switching shaped the termite gut microbiome. Curr. Biol.28, 649–654 (2018). PubMed
Noda, S. et al. Endosymbiotic Bacteroidales bacteria of the flagellated protist Pseudotrichonympha grassii in the gut of the termite Coptotermes formosanus. Appl. Environ. Microbiol.71, 8811–8817 (2005). PubMed PMC
Ohkuma, M., Noda, S. & Kudo, T. Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl. Environ. Microbiol.65, 4926–4934 (1999). PubMed PMC
Ohkuma, M. & Brune, A. Diversity, structure, and evolution of the termite gut microbial community. in Biology of Termites: a Modern Synthesis (eds. Bignell, D.E. Roisin, Y., Lo, N.) 413–438 (Springer Netherlands, 2010). 10.1007/978-90-481-3977-4_15.
Michaud, C. et al. Efficient but occasionally imperfect vertical transmission of gut mutualistic protists in a wood-feeding termite. Mol. Ecol.29, 308–324 (2020). PubMed
Nalepa, C. A., Bignell, D. E. & Bandi, C. Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera. Insectes Soc.48, 194–201 (2001).
Sinotte, V. M., Renelies-Hamilton, J., Andreu-Sánchez, S., Vasseur-Cognet, M. & Poulsen, M. Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite. Proc. Biol. Sci.290, 20231559 (2023). PubMed PMC
Dietrich, C., Köhler, T. & Brune, A. The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl. Environ. Microbiol.80, 2261–2269 (2014). PubMed PMC
Chouvenc, T., Elliott, M. L., Šobotník, J., Efstathion, C. A. & Su, N.-Y. The Termite Fecal Nest: A Framework for the Opportunistic Acquisition of Beneficial Soil Streptomyces (Actinomycetales: Streptomycetaceae). Environ. Entomol.47, 1431–1439 (2018). PubMed
Visser, A. A., Nobre, T., Currie, C. R., Aanen, D. K. & Poulsen, M. Exploring the potential for actinobacteria as defensive symbionts in fungus-growing termites. Microb. Ecol.63, 975–985 (2012). PubMed
Hellemans, S. et al. Genomic data provide insights into the classification of extant termites. Nat. Commun.15, 6724 (2024). PubMed PMC
Bucek, A. et al. Evolution of termite symbiosis informed by transcriptome-based phylogenies. Curr. Biol.29, 3728–3734.e4 (2019). PubMed
Hellemans, S. et al. Using ultraconserved elements to reconstruct the termite tree of life. Mol. Phylogenet. Evol.173, 107520 (2022). PubMed
Balbuena, J. A., Míguez-Lozano, R. & Blasco-Costa, I. PACo: A novel Procrustes Application to Cophylogenetic analysis. PLoS One8, e61048 (2013). PubMed PMC
Smith, M. R. Information theoretic generalized Robinson-Foulds metrics for comparing phylogenetic trees. Bioinformatics36, 5007–5013 (2020). PubMed
Nye, T. M. W., Liò, P. & Gilks, W. R. A novel algorithm and web-based tool for comparing two alternative phylogenetic trees. Bioinformatics22, 117–119 (2006). PubMed
Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods12, 59–60 (2015). PubMed
Parks, D. H. et al. GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res.50, D785–D794 (2022). PubMed PMC
Tokuda, G. et al. Fiber-associated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites. Proc. Natl Acad. Sci. USA115, E11996–E12004 (2018). PubMed PMC
Hongoh, Y. et al. Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science322, 1108–1109 (2008). PubMed
Kitade, O. & Matsumoto, T. Characteristics of the symbiotic flagellate composition within the termite family Rhinotermitidae (Isoptera). Symbiosis25, 271–278 (1998).
Parks, D. H. et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat. Biotechnol.38, 1079–1086 (2020). PubMed
Zhang, H. et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res.46, W95–W101 (2018). PubMed PMC
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol.215, 403–410 (1990). PubMed
Shen, W., Le, S., Li, Y. & Hu, F. SeqKit: A Cross-pPlatform and Ultrafast Toolkit for FASTA/Q File Manipulation. PLoS One11, e0163962 (2016). PubMed PMC
Katoh, K., Misawa, K., Kuma, K.-I. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res.30, 3059–3066 (2002). PubMed PMC
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol.30, 772–780 (2013). PubMed PMC
Suyama, M., Torrents, D. & Bork, P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res.34, W609–W612 (2006). PubMed PMC
Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol.26, 1641–1650 (2009). PubMed PMC
Terrapon, N. et al. Molecular traces of alternative social organization in a termite genome. Nat. Commun.5, 3636 (2014). PubMed
Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: Improving the ultrafast bootstrap approximation. Mol. Biol. Evol.35, 518–522 (2018). PubMed PMC
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol.32, 268–274 (2015). PubMed PMC
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics25, 1754–1760 (2009). PubMed PMC
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics25, 2078–2079 (2009). PubMed PMC
Oksanen, J., Blanchet, F. G., Kindt, R. & Legendre, R. vegan: Community Ecology Package. R package version 2.0-10, edn. (2014). https://CRAN.R-project.org/package=vegan.
Hutchinson, M. C., Fernando Cagua, E., Balbuena, J. A., Stouffer, D. B. & Poisot, T. paco: implementing Procrustean Approach to Cophylogeny in R. Methods Ecol. Evol.8, 932–940 (2017).
Perez-Lamarque, B. & Morlon, H. Characterizing symbiont inheritance during host-microbiota evolution: Application to the great apes gut microbiota. Mol. Ecol. Resour.19, 1659–1671 (2019). PubMed
Satler, J. D. et al. Inferring processes of coevolutionary diversification in a community of Panamanian strangler figs and associated pollinating wasps. Evolution73, 2295–2311 (2019). PubMed