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

Abdul Rahman, Nurdyana; Parks, Donovan H.; Willner, Dana L.; Engelbrektson, Anna L.; Goffredi, Shana K.; Warnecke, Falk; Scheffrahn, Rudolf H.; Hugenholtz, Philip

doi:10.1186/s40168-015-0067-8

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

Journal Article · Wed Feb 25 00:00:00 EST 2015 · Microbiome

DOI:https://doi.org/10.1186/s40168-015-0067-8· OSTI ID:1627043

Abdul Rahman, Nurdyana ^[1]; Parks, Donovan H. ^[1]; Willner, Dana L. ^[1]; Engelbrektson, Anna L. ^[2]; Goffredi, Shana K. ^[3]; Warnecke, Falk ^[4]; Scheffrahn, Rudolf H. ^[5]; Hugenholtz, Philip ^[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)
Occidental College, Los Angeles, CA (United States). Biology Dept.
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
Univ. of Florida, Davie, FL (United States). Fort Lauderdale Research and Education Center
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)

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.

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Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627043

Journal Information:: Microbiome, Vol. 3, Issue 1; ISSN 2049-2618

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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"Endomicrobia": Cytoplasmic Symbionts of Termite Gut Protozoa Form a Separate Phylum of Prokaryotes Stingl, U.; Radek, R.; Yang, H. Applied and Environmental Microbiology, Vol. 71, Issue 3 https://doi.org/10.1128/aem.71.3.1473-1479.2005	journal	March 2005
Protist Communities from Four Castes and Three Species of Reticulitermes (Isoptera: Rhinotermitidae) Lewis, J. L.; Forschler, B. T. Annals of the Entomological Society of America, Vol. 97, Issue 6 https://doi.org/10.1603/0013-8746(2004)097[1242:pcffca]2.0.co;2	journal	November 2004
Symbiosis in Subterranean Termites: A Review of Insights From Molecular Studies Husseneder, Claudia Environmental Entomology, Vol. 39, Issue 2 https://doi.org/10.1603/en09006	journal	April 2010
Data from: The hindgut-lumen prokaryotic microbiota of the lignocellulose-degrading termite Reticulitermes flavipes and its responses to dietary lignocellulose composition Boucias, Drion G.; Cai, Yunpeng; Sun, Yijun Dryad https://doi.org/10.5061/dryad.b922k	dataset	January 2013

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Generating amplicon reads for microbial community assessment with next‐generation sequencing Gołębiewski, M.; Tretyn, A. Journal of Applied Microbiology, Vol. 128, Issue 2 https://doi.org/10.1111/jam.14380	journal	August 2019
Gut microbial compositions mirror caste-specific diets in a major lineage of eusocial insects Otani, Saria; Zhukova, Mariya; Koné, N’golo Abdoulaye https://doi.org/10.1101/418954	posted_content	September 2018
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Cophylogenetic analysis suggests cospeciation between the Scorpion Mycoplasma Clade symbionts and their hosts Bolaños, Luis M.; Rosenblueth, Mónica; Manrique de Lara, Amaranta PLOS ONE, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pone.0209588	journal	January 2019
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