Metagenomic analysis of the microbiota in the highly compartmented hindguts of six wood- or soil-feeding higher termites
Abstract
Termites are important contributors to carbon and nitrogen cycling in tropical ecosystems. Higher termites digest lignocellulose in various stages of humification with the help of an entirely prokaryotic microbiota housed in their compartmented intestinal tract. Previous studies revealed fundamental differences in community structure between compartments, but the functional roles of individual lineages in symbiotic digestion are mostly unknown. Furthermore, we conducted a highly resolved analysis of the gut microbiota in six species of higher termites that feed on plant material at different levels of humification. Combining amplicon sequencing and metagenomics, we assessed similarities in community structure and functional potential between the major hindgut compartments (P1, P3, and P4). Cluster analysis of the relative abundances of orthologous gene clusters (COGs) revealed high similarities among woodand litter-feeding termites and strong differences to humivorous species. However, abundance estimates of bacterial phyla based on 16S rRNA genes greatly differed from those based on protein-coding genes. In conclusion, the community structure and functional potential of the microbiota in individual gut compartments are clearly driven by the digestive strategy of the host. The metagenomics libraries obtained in this study provide the basis for future studies that elucidate the fundamental differences in the symbiont-mediated breakdown of lignocellulosemore »
- Authors:
-
- Max Planck Institute for Terrestrial Microbiology, Marburg (Germany); Colorado State Univ., Fort Collins, CO (United States)
- Max Planck Institute for Terrestrial Microbiology, Marburg (Germany)
- Max Planck Institute for Terrestrial Microbiology, Marburg (Germany); Philipps-Univ. Marburg, Marburg (Germany)
- Univ. of Florida, Davie, FL (United States)
- Univ. Paris 13, Villetaneuse (France); Sorbonne Univ., Bondy (France)
- Publication Date:
- Research Org.:
- Univ. of California, Oakland, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1240993
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbiome
- Additional Journal Information:
- Journal Volume: 3; Journal Issue: 1; Journal ID: ISSN 2049-2618
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; metagenomics; termites; hindgut; functional potential; gut microbiota; community structure
Citation Formats
Rossmassler, Karen, Dietrich, Carsten, Thompson, Claire, Mikaelyan, Aram, Nonoh, James O., Scheffrahn, Rudolf H., Sillam-Dussès, David, and Brune, Andreas. Metagenomic analysis of the microbiota in the highly compartmented hindguts of six wood- or soil-feeding higher termites. United States: N. p., 2015.
Web. doi:10.1186/s40168-015-0118-1.
Rossmassler, Karen, Dietrich, Carsten, Thompson, Claire, Mikaelyan, Aram, Nonoh, James O., Scheffrahn, Rudolf H., Sillam-Dussès, David, & Brune, Andreas. Metagenomic analysis of the microbiota in the highly compartmented hindguts of six wood- or soil-feeding higher termites. United States. https://doi.org/10.1186/s40168-015-0118-1
Rossmassler, Karen, Dietrich, Carsten, Thompson, Claire, Mikaelyan, Aram, Nonoh, James O., Scheffrahn, Rudolf H., Sillam-Dussès, David, and Brune, Andreas. Thu .
"Metagenomic analysis of the microbiota in the highly compartmented hindguts of six wood- or soil-feeding higher termites". United States. https://doi.org/10.1186/s40168-015-0118-1. https://www.osti.gov/servlets/purl/1240993.
@article{osti_1240993,
title = {Metagenomic analysis of the microbiota in the highly compartmented hindguts of six wood- or soil-feeding higher termites},
author = {Rossmassler, Karen and Dietrich, Carsten and Thompson, Claire and Mikaelyan, Aram and Nonoh, James O. and Scheffrahn, Rudolf H. and Sillam-Dussès, David and Brune, Andreas},
abstractNote = {Termites are important contributors to carbon and nitrogen cycling in tropical ecosystems. Higher termites digest lignocellulose in various stages of humification with the help of an entirely prokaryotic microbiota housed in their compartmented intestinal tract. Previous studies revealed fundamental differences in community structure between compartments, but the functional roles of individual lineages in symbiotic digestion are mostly unknown. Furthermore, we conducted a highly resolved analysis of the gut microbiota in six species of higher termites that feed on plant material at different levels of humification. Combining amplicon sequencing and metagenomics, we assessed similarities in community structure and functional potential between the major hindgut compartments (P1, P3, and P4). Cluster analysis of the relative abundances of orthologous gene clusters (COGs) revealed high similarities among woodand litter-feeding termites and strong differences to humivorous species. However, abundance estimates of bacterial phyla based on 16S rRNA genes greatly differed from those based on protein-coding genes. In conclusion, the community structure and functional potential of the microbiota in individual gut compartments are clearly driven by the digestive strategy of the host. The metagenomics libraries obtained in this study provide the basis for future studies that elucidate the fundamental differences in the symbiont-mediated breakdown of lignocellulose and humus by termites of different feeding groups. Furthermore, the high proportion of uncultured bacterial lineages in all samples calls for a reference-independent approach for the correct taxonomic assignment of protein-coding genes.},
doi = {10.1186/s40168-015-0118-1},
journal = {Microbiome},
number = 1,
volume = 3,
place = {United States},
year = {Thu Nov 26 00:00:00 EST 2015},
month = {Thu Nov 26 00:00:00 EST 2015}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 36 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Phylogenetic diversity of prokaryotes associated with the mandibulate nasute termite Cornitermes cumulans and its mound
journal, October 2012
- Costa, Patrícia S.; Oliveira, Pollyanna L.; Chartone-Souza, Edmar
- Biology and Fertility of Soils, Vol. 49, Issue 5
IMG/M 4 version of the integrated metagenome comparative analysis system
journal, October 2013
- Markowitz, Victor M.; Chen, I-Min A.; Chu, Ken
- Nucleic Acids Research, Vol. 42, Issue D1, p. D568-D573
The Cockroach Origin of the Termite Gut Microbiota: Patterns in Bacterial Community Structure Reflect Major Evolutionary Events
journal, January 2014
- Dietrich, Carsten; Köhler, Tim; Brune, Andreas
- Applied and Environmental Microbiology, Vol. 80, Issue 7
The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist
journal, April 2011
- Suen, Garret; Weimer, Paul J.; Stevenson, David M.
- PLoS ONE, Vol. 6, Issue 4
The Gut Microbiota of Termites: Digesting the Diversity in the Light of Ecology and Evolution
journal, October 2015
- Brune, Andreas; Dietrich, Carsten
- Annual Review of Microbiology, Vol. 69, Issue 1
Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits
journal, March 2001
- Brauman, Alain; Doré, Joel; Eggleton, Paul
- FEMS Microbiology Ecology, Vol. 35, Issue 1
Comparison of bacterial communities in the alkaline gut segment among various species of higher termites
journal, April 2005
- Thongaram, Taksawan; Hongoh, Yuichi; Kosono, Saori
- Extremophiles, Vol. 9, Issue 3
The complete mitogenomes of six higher termite species reconstructed from metagenomic datasets ( Cornitermes sp., Cubitermes ugandensis, Microcerotermes parvus, Nasutitermes corniger, Neocapritermes taracua, and Termes hospes )
journal, December 2014
- Dietrich, Carsten; Brune, Andreas
- Mitochondrial DNA Part A, Vol. 27, Issue 6
Symbiotic digestion of lignocellulose in termite guts
journal, February 2014
- Brune, Andreas
- Nature Reviews Microbiology, Vol. 12, Issue 3
High-Resolution Analysis of Gut Environment and Bacterial Microbiota Reveals Functional Compartmentation of the Gut in Wood-Feeding Higher Termites (Nasutitermes spp.)
journal, April 2012
- Köhler, Tim; Dietrich, Carsten; Scheffrahn, Rudolf H.
- Applied and Environmental Microbiology, Vol. 78, Issue 13
Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite
journal, November 2007
- Warnecke, Falk; Luginbühl, Peter; Ivanova, Natalia
- Nature, Vol. 450, Issue 7169
Axial Dynamics, Stability, and Interspecies Similarity of Bacterial Community Structure in the Highly Compartmentalized Gut of Soil-Feeding Termites (Cubitermes spp.)
journal, October 2003
- Schmitt-Wagner, D.; Friedrich, M. W.; Wagner, B.
- Applied and Environmental Microbiology, Vol. 69, Issue 10
Illumina-based analysis of microbial community diversity
journal, June 2011
- Degnan, Patrick H.; Ochman, Howard
- The ISME Journal, Vol. 6, Issue 1
Genome analysis of Chitinivibrio alkaliphilus gen. nov., sp. nov., a novel extremely haloalkaliphilic anaerobic chitinolytic bacterium from the candidate phylum Termite Group 3 : Chitinolytic bacterium from the candidate phylum TG3
journal, October 2013
- Sorokin, Dimitry Y.; Gumerov, Vadim M.; Rakitin, Andrey L.
- Environmental Microbiology, Vol. 16, Issue 6
The fibre-associated cellulolytic bacterial community in the hindgut of wood-feeding higher termites ( N asutitermes spp.) : The fibre-associated community of higher termites
journal, March 2014
- Mikaelyan, Aram; Strassert, Jürgen F. H.; Tokuda, Gaku
- Environmental Microbiology, Vol. 16, Issue 9
Phylogenetic Diversity, Localization, and Cell Morphologies of Members of the Candidate Phylum TG3 and a Subphylum in the Phylum Fibrobacteres, Recently Discovered Bacterial Groups Dominant in Termite Guts
journal, August 2006
- Hongoh, Y.; Deevong, P.; Hattori, S.
- Applied and Environmental Microbiology, Vol. 72, Issue 10
The Termite Gut Microflora as an Oxygen Sink: Microelectrode Determination of Oxygen and pH Gradients in Guts of Lower and Higher Termites.
journal, January 1995
- Brune, A.; Emerson, D.; Breznak, J. A.
- Applied and environmental microbiology, Vol. 61, Issue 7
Hydrogen Profiles and Localization of Methanogenic Activities in the Highly Compartmentalized Hindgut of Soil-Feeding Higher Termites (Cubitermes spp.)
journal, January 1999
- Schmitt-Wagner, Dirk; Brune, Andreas
- Applied and Environmental Microbiology, Vol. 65, Issue 10
Comparative Metagenomic and Metatranscriptomic Analysis of Hindgut Paunch Microbiota in Wood- and Dung-Feeding Higher Termites
journal, April 2013
- He, Shaomei; Ivanova, Natalia; Kirton, Edward
- PLoS ONE, Vol. 8, Issue 4
Metagenomic Insights into Metabolic Capacities of the Gut Microbiota in a Fungus-Cultivating Termite (Odontotermes yunnanensis)
journal, July 2013
- Liu, Ning; Zhang, Lei; Zhou, Haokui
- PLoS ONE, Vol. 8, Issue 7
Works referencing / citing this record:
Comparison of gut bacterial communities and their associations with host diets in four fruit borers
journal, November 2019
- Liu, Yanjun; Shen, Zhongjian; Yu, Jianmei
- Pest Management Science, Vol. 76, Issue 4
Microbial Communities of the Gut and Nest of the Humus- and Litter-Feeding Termite Procornitermes araujoi (Syntermitinae)
journal, September 2018
- Moreira, Edimar A.; Alvarez, Thabata M.; Persinoti, Gabriela F.
- Current Microbiology, Vol. 75, Issue 12
Effects of diet type, developmental stage, and gut compartment in the gut bacterial communities of two Cerambycidae species (Coleoptera)
journal, December 2016
- Kim, Jeong Myeong; Choi, Min-Young; Kim, Jae-Woo
- Journal of Microbiology, Vol. 55, Issue 1
Species-wide Metabolic Interaction Network for Understanding Natural Lignocellulose Digestion in Termite Gut Microbiota
journal, November 2019
- Kundu, Pritam; Manna, Bharat; Majumder, Subham
- Scientific Reports, Vol. 9, Issue 1
The complete mitochondrial genomes of the higher termites Labiotermes labralis and Embiratermes neotenicus (Termitidae: Syntermitinae)
journal, January 2017
- Hervé, Vincent; Brune, Andreas
- Mitochondrial DNA Part B, Vol. 2, Issue 1
The origin of fungi-culture in termites was associated with a shift to a mycolytic gut bacteria community
posted_content, October 2018
- Hu, Haofu; Rodrigues da Costa, Rafael; Pilgaard, Bo
- bioRxiv
Ecological specificity of the metagenome in a set of lower termite species supports contribution of the microbiome to adaptation of the host
posted_content, May 2019
- Waidele, Lena; Korb, Judith; Voolstra, Christian R.
Efficient but occasionally imperfect vertical transmission of gut mutualistic protists in a wood‐feeding termite
journal, December 2019
- Michaud, Caroline; Hervé, Vincent; Dupont, Simon
- Molecular Ecology, Vol. 29, Issue 2
Optimization of a metatranscriptomic approach to study the lignocellulolytic potential of the higher termite gut microbiome
journal, September 2017
- Marynowska, Martyna; Goux, Xavier; Sillam-Dussès, David
- BMC Genomics, Vol. 18, Issue 1
The gut bacteria across life stages in the synanthropic fly Chrysomya megacephala
journal, October 2018
- Wang, Xiaoyun; Gao, Qiao; Wang, Wanqiang
- BMC Microbiology, Vol. 18, Issue 1
Lignocellulose degradation at the holobiont level: teamwork in a keystone soil invertebrate
journal, September 2018
- Bredon, Marius; Dittmer, Jessica; Noël, Cyril
- Microbiome, Vol. 6, Issue 1
Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
journal, June 2020
- Marynowska, Martyna; Goux, Xavier; Sillam-Dussès, David
- Microbiome, Vol. 8, Issue 1
Ecological specificity of the metagenome in a set of lower termite species supports contribution of the microbiome to adaptation of the host
journal, October 2019
- Waidele, Lena; Korb, Judith; Voolstra, Christian R.
- Animal Microbiome, Vol. 1, Issue 1
Characterization of cellulose-degrading microbiota from the eastern subterranean termite and soil
journal, January 2017
- Xie, Xianfa; Anderson, Alonzo B.; Wran, Latoya J.
- F1000Research, Vol. 6
The functional microbiome of arthropods
journal, May 2017
- Degli Esposti, Mauro; Martinez Romero, Esperanza
- PLOS ONE, Vol. 12, Issue 5
Differential Ecological Specificity of Protist and Bacterial Microbiomes across a Set of Termite Species
journal, December 2017
- Waidele, Lena; Korb, Judith; Voolstra, Christian R.
- Frontiers in Microbiology, Vol. 8
Uncovering the Potential of Termite Gut Microbiome for Lignocellulose Bioconversion in Anaerobic Batch Bioreactors
journal, December 2017
- Auer, Lucas; Lazuka, Adèle; Sillam-Dussès, David
- Frontiers in Microbiology, Vol. 8
Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
posted_content, June 2020
- Marynowska, Martyna; Goux, Xavier; Sillam-Dusses, David
- Research Square [preprints]
Characterization of Cellulose-Degrading Microbiota from The Eastern Subterranean Termite and Soil
text, January 2017
- Xie, Xianfa
- Open Science Framework
Compositional and functional characterisation of biomass-degrading microbial communities in guts of plant fibre- and soil-feeding higher termites
posted_content, June 2020
- Marynowska, Martyna; Goux, Xavier; Sillam-Dusses, David
- Research Square [preprints]