skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: A molecular survey of Australian and North American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes

Abstract

Termites and their microbial gut symbionts are major recyclers of lignocellulosic biomass. This important symbiosis is obligate but relatively open and more complex in comparison to other well-known insect symbioses such as the strict vertical transmission of Buchnera in aphids. The relative roles of vertical inheritance and environmental factors such as diet in shaping the termite gut microbiome are not well understood.ResultsThe gut microbiomes of 66 specimens representing seven higher and nine lower termite genera collected in Australia and North America were profiled by small subunit (SSU) rRNA amplicon pyrosequencing. These represent the first reported culture-independent gut microbiome data for three higher termite genera: Tenuirostritermes, Drepanotermes, and Gnathamitermes; and two lower termite genera: Marginitermes and Porotermes. Consistent with previous studies, bacteria comprise the largest fraction of termite gut symbionts, of which 11 phylotypes (6 Treponema, 1 Desulfarculus-like, 1 Desulfovibrio, 1 Anaerovorax-like, 1 Sporobacter-like, and 1 Pirellula-like) were widespread occurring in ≥50% of collected specimens. Archaea are generally considered to comprise only a minority of the termite gut microbiota (<3%); however, archaeal relative abundance was substantially higher and variable in a number of specimens including Macrognathotermes, Coptotermes, Schedorhinotermes, Porotermes, and Mastotermes (representing up to 54% of amplicon reads). A ciliate relatedmore » to Clevelandella was detected in low abundance in Gnathamitermes indicating that protists were either reacquired after protists loss in higher termites or persisted in low numbers across this transition. Phylogenetic analyses of the bacterial communities indicate that vertical inheritance is the primary force shaping termite gut microbiota. The effect of diet is secondary and appears to influence the relative abundance, but not membership, of the gut communities.ConclusionsVertical inheritance is the primary force shaping the termite gut microbiome indicating that species are successfully and faithfully passed from one generation to the next via trophallaxis or coprophagy. Changes in relative abundance can occur on shorter time scales and appear to be an adaptive mechanism for dietary fluctuations.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [4];  [5];  [6]
  1. Univ. of Queensland, Brisbane, QLD (Australia). School of Chemistry and Molecular Biosciences. Australian Centre for Ecogenomics
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Occidental College, Los Angeles, CA (United States). Biology Dept.
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Friedrich Schiller Univ., Jena (Germany). Jena School for Microbial Communication (JSMC) and Microbial Ecology Group
  5. Univ. of Florida, Davie, FL (United States). Fort Lauderdale Research and Education Center
  6. Univ. of Queensland, Brisbane, QLD (Australia). School of Chemistry and Molecular Biosciences. Australian Centre for Ecogenomics; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1627043
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: 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:
60 APPLIED LIFE SCIENCES; Microbiology

Citation Formats

Abdul Rahman, Nurdyana, Parks, Donovan H., Willner, Dana L., Engelbrektson, Anna L., Goffredi, Shana K., Warnecke, Falk, Scheffrahn, Rudolf H., and Hugenholtz, Philip. A molecular survey of Australian and North American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes. United States: N. p., 2015. Web. doi:10.1186/s40168-015-0067-8.
Abdul Rahman, Nurdyana, Parks, Donovan H., Willner, Dana L., Engelbrektson, Anna L., Goffredi, Shana K., Warnecke, Falk, Scheffrahn, Rudolf H., & Hugenholtz, Philip. A molecular survey of Australian and North American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes. United States. https://doi.org/10.1186/s40168-015-0067-8
Abdul Rahman, Nurdyana, Parks, Donovan H., Willner, Dana L., Engelbrektson, Anna L., Goffredi, Shana K., Warnecke, Falk, Scheffrahn, Rudolf H., and Hugenholtz, Philip. Wed . "A molecular survey of Australian and North American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes". United States. https://doi.org/10.1186/s40168-015-0067-8. https://www.osti.gov/servlets/purl/1627043.
@article{osti_1627043,
title = {A molecular survey of Australian and North American termite genera indicates that vertical inheritance is the primary force shaping termite gut microbiomes},
author = {Abdul Rahman, Nurdyana and Parks, Donovan H. and Willner, Dana L. and Engelbrektson, Anna L. and Goffredi, Shana K. and Warnecke, Falk and Scheffrahn, Rudolf H. and Hugenholtz, Philip},
abstractNote = {Termites and their microbial gut symbionts are major recyclers of lignocellulosic biomass. This important symbiosis is obligate but relatively open and more complex in comparison to other well-known insect symbioses such as the strict vertical transmission of Buchnera in aphids. The relative roles of vertical inheritance and environmental factors such as diet in shaping the termite gut microbiome are not well understood.ResultsThe gut microbiomes of 66 specimens representing seven higher and nine lower termite genera collected in Australia and North America were profiled by small subunit (SSU) rRNA amplicon pyrosequencing. These represent the first reported culture-independent gut microbiome data for three higher termite genera: Tenuirostritermes, Drepanotermes, and Gnathamitermes; and two lower termite genera: Marginitermes and Porotermes. Consistent with previous studies, bacteria comprise the largest fraction of termite gut symbionts, of which 11 phylotypes (6 Treponema, 1 Desulfarculus-like, 1 Desulfovibrio, 1 Anaerovorax-like, 1 Sporobacter-like, and 1 Pirellula-like) were widespread occurring in ≥50% of collected specimens. Archaea are generally considered to comprise only a minority of the termite gut microbiota (<3%); however, archaeal relative abundance was substantially higher and variable in a number of specimens including Macrognathotermes, Coptotermes, Schedorhinotermes, Porotermes, and Mastotermes (representing up to 54% of amplicon reads). A ciliate related to Clevelandella was detected in low abundance in Gnathamitermes indicating that protists were either reacquired after protists loss in higher termites or persisted in low numbers across this transition. Phylogenetic analyses of the bacterial communities indicate that vertical inheritance is the primary force shaping termite gut microbiota. The effect of diet is secondary and appears to influence the relative abundance, but not membership, of the gut communities.ConclusionsVertical inheritance is the primary force shaping the termite gut microbiome indicating that species are successfully and faithfully passed from one generation to the next via trophallaxis or coprophagy. Changes in relative abundance can occur on shorter time scales and appear to be an adaptive mechanism for dietary fluctuations.},
doi = {10.1186/s40168-015-0067-8},
url = {https://www.osti.gov/biblio/1627043}, journal = {Microbiome},
issn = {2049-2618},
number = 1,
volume = 3,
place = {United States},
year = {2015},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 57 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Protozoa in Termites of the Genus Amitermes
journal, October 1932


UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


Host-specific assemblages typify gut microbial communities of related insect species
journal, March 2014


Novel lineages of Planctomycetes densely colonize the alkaline gut of soil-feeding termites (Cubitermes spp.)
journal, May 2008


Genome of an Endosymbiont Coupling N2 Fixation to Cellulolysis Within Protist Cells in Termite Gut
journal, November 2008


“Methanoplasmatales,” Thermoplasmatales-Related Archaea in Termite Guts and Other Environments, Are the Seventh Order of Methanogens
journal, September 2012


New termite species and newly recorded genus for Australia: Marginitermes absitus (Isoptera: Kalotermitidae): New termites from Cape York
journal, March 2013


Impaired Leaf Litter Processing in Acidified Streams: Learning from Microbial Enzyme Activities
journal, August 2012


Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut
journal, March 2011


Divergence times in the termite genus Macrotermes (Isoptera: Termitidae)
journal, October 2007


An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011


Endosymbiotic Bacteroidales Bacteria of the Flagellated Protist Pseudotrichonympha grassii in the Gut of the Termite Coptotermes formosanus
journal, December 2005


Treatise on the Isoptera of the World: VOLUME 2 BASAL FAMILIES
journal, April 2013

  • Krishna, Kumar; Grimaldi, David A.; Krishna, Valerie
  • Bulletin of the American Museum of Natural History, Vol. 377, Issue 7
  • https://doi.org/10.1206/377.2

Worlds within worlds: evolution of the vertebrate gut microbiota
journal, October 2008


Evolution of Mammals and Their Gut Microbes
journal, June 2008


Protist Communities from Four Castes and Three Species of Reticulitermes (Isoptera: Rhinotermitidae)
journal, November 2004


Characterization of the 18S rRNA Gene for Designing Universal Eukaryote Specific Primers
journal, February 2014


Who digests the lignocellulose?: Who digests the lignocellulose?
journal, April 2014


Phylogenetic and Morphological Diversity of Bacteroidales Members Associated with the Gut Wall of Termites
journal, January 2006


CD-HIT: accelerated for clustering the next-generation sequencing data
journal, October 2012


UniFrac: an effective distance metric for microbial community comparison
journal, September 2010


Building on basic metagenomics with complementary technologies
journal, January 2007


Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects
journal, March 1992


Molecular Phylogenetic Diversity of the Bacterial Community in the Gut of the Termite Coptotermes formosanus
journal, January 2005


The microbial dimension in insect nutritional ecology
journal, February 2009


Fast, accurate error-correction of amplicon pyrosequences using Acacia
journal, April 2012


Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates
journal, January 2010


The effects of fossil placement and calibration on divergence times and rates: An example from the termites (Insecta: Isoptera)
journal, March 2010


The Cockroach Origin of the Termite Gut Microbiota: Patterns in Bacterial Community Structure Reflect Major Evolutionary Events
journal, January 2014


Phylogenetic Diversity of Nitrogen Fixation Genes in the Symbiotic Microbial Community in the Gut of Diverse Termites
journal, November 1999


ARB: a software environment for sequence data
journal, February 2004


Effects of OTU Clustering and PCR Artifacts on Microbial Diversity Estimates
journal, December 2012


Putatively free-living ‘Endomicrobia’- ancestors of the intracellular symbionts of termite gut flagellates?: Putatively free-living Endomicrobia
journal, January 2010


Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis)
journal, July 2005


Molecular phylogenetic profiling of prokaryotic communities in guts of termites with different feeding habits
journal, March 2001


On the elevated intestinal pH of higher termites (Isoptera: Termitidae)
journal, March 1995


Evolutionary Relationships of Wild Hominids Recapitulated by Gut Microbial Communities
journal, November 2010


Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins
journal, April 2010


Symbiotic digestion of lignocellulose in termite guts
journal, February 2014


Novel Euryarchaeotal Lineages Detected on Rice Roots and in the Anoxic Bulk Soil of Flooded Rice Microcosms
journal, December 1998


Diversity and Genomes of Uncultured Microbial Symbionts in the Termite Gut
journal, June 2010


The Bacterial Community in the Gut of the Cockroach Shelfordella lateralis Reflects the Close Evolutionary Relatedness of Cockroaches and Termites
journal, February 2012


A Feasible Role of Sulfate-Reducing Bacteria in the Termite Gut
journal, August 1996


Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite
journal, November 2007


Localizing transcripts to single cells suggests an important role of uncultured deltaproteobacteria in the termite gut hydrogen economy
journal, September 2013


QIIME allows analysis of high-throughput community sequencing data
journal, April 2010


Basic local alignment search tool
journal, October 1990


Phylogenetic diversity of 'Endomicrobia' and their specific affiliation with termite gut flagellates
journal, October 2007


The gut microbiota of insects – diversity in structure and function
journal, September 2013


Phylogenetic evidence for a single, ancestral origin of a 'true' worker caste in termites
journal, November 2000


"Endomicrobia": Cytoplasmic Symbionts of Termite Gut Protozoa Form a Separate Phylum of Prokaryotes
journal, March 2005


A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology
journal, September 2007


Phylogeny of Wolbachia in filarial nematodes
journal, December 1998


Molecular phylogeny of Asian termites (Isoptera) of the families Termitidae and Rhinotermitidae based on mitochondrial COII sequences
journal, May 2004


Lessons from Studying Insect Symbioses
journal, October 2011


Phylogenetic relationships of symbiotic spirochetes in the gut of diverse termites
journal, December 1999


Morphology and Molecular Phylogeny of Staurojoenina mulleri sp. nov. (Trichonymphida, Parabasalia) from the Hindgut of the Kalotermitid Neotermes jouteli
journal, February 2013


FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
journal, April 2009


Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites
journal, September 2000


Dependence of the higher termite, Nasutitermes exitiosus and the lower termite, Coptotermes lacteus on their gut flora
journal, January 1978


Studies on feeding and trophallaxis in the subterranean termite Odontotermes formosanus using rubidium chloride
journal, November 2008


Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae)
journal, May 2003


Metagenomic Sequencing of an In Vitro-Simulated Microbial Community
journal, April 2010


Methanogenic Symbionts and the Locality of their Host Lower Termites
journal, January 2001


Identifying biologically relevant differences between metagenomic communities
journal, February 2010


UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005


Symbiosis in Subterranean Termites: A Review of Insights From Molecular Studies
journal, April 2010


    Works referencing / citing this record:

    Characterization of cellulose-degrading microbiota from the eastern subterranean termite and soil
    journal, January 2017


    Food Storage by the Savanna Termite Cornitermes cumulans (Syntermitinae): a Strategy to Improve Hemicellulose Digestibility?
    journal, December 2017


    Variations in the relative abundance of Wolbachia in the gut of Nasutitermes arborum across life stages and castes
    journal, February 2018


    Dissecting host-associated communities with DNA barcodes
    journal, September 2016

    • Baker, Christopher C. M.; Bittleston, Leonora S.; Sanders, Jon G.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1702
    • https://doi.org/10.1098/rstb.2015.0328

    Coral microbiome database: Integration of sequences reveals high diversity and relatedness of coral‐associated microbes
    journal, September 2018


    Gut microbial compositions mirror caste‐specific diets in a major lineage of social insects
    journal, January 2019


    Gut microbiota dynamics and functionality in Reticulitermes grassei after a 7-day dietary shift and ciprofloxacin treatment
    journal, December 2018


    A Phylogenomic Analysis of the Bacterial Phylum Fibrobacteres
    journal, January 2016


    Characterization of the Core and Caste-Specific Microbiota in the Termite, Reticulitermes flavipes
    journal, February 2016


    Differential Ecological Specificity of Protist and Bacterial Microbiomes across a Set of Termite Species
    journal, December 2017