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Evidence for Cascades of Perturbation and Adaptation in the Metabolic Genes of Higher Termite Gut Symbionts

Zhang, Xinning and Leadbetter, Jared R. (2012) Evidence for Cascades of Perturbation and Adaptation in the Metabolic Genes of Higher Termite Gut Symbionts. mBio, 3 (4). Art. No. e00223-12. ISSN 2150-7511. PMCID PMC3428693. doi:10.1128/mBio.00223-12. https://resolver.caltech.edu/CaltechAUTHORS:20190506-085640418

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Abstract

Termites and their gut microbes engage in fascinating dietary mutualisms. Less is known about how these complex symbioses have evolved after first emerging in an insect ancestor over 120 million years ago. Here we examined a bacterial gene, formate dehydrogenase (fdhF), that is key to the mutualism in 8 species of “higher” termite (members of the Termitidae, the youngest and most biomass-abundant and species-rich termite family). Patterns of fdhF diversity in the gut communities of higher termites contrasted strongly with patterns in less-derived (more-primitive) insect relatives (wood-feeding “lower” termites and roaches). We observed phylogenetic evidence for (i) the sweeping loss of several clades of fdhF that may reflect extinctions of symbiotic protozoa and, importantly, bacteria dependent on them in the last common ancestor of all higher termites and (ii) a radiation of genes from the (possibly) single allele that survived. Sweeping gene loss also resulted in (iii) the elimination of an entire clade of genes encoding selenium (Se)-independent enzymes from higher termite gut communities, perhaps reflecting behavioral or morphological innovations in higher termites that relaxed preexisting environmental limitations of Se, a dietary trace element. Curiously, several higher termite gut communities may have subsequently reencountered Se limitation, reinventing genes for Se-independent proteins via convergent evolution. Lastly, the presence of a novel fdhF lineage within litter-feeding and subterranean higher (but not other) termites may indicate recent gene “invasion” events. These results imply that cascades of perturbation and adaptation by distinct evolutionary mechanisms have impacted the evolution of complex microbial communities in a highly successful lineage of insects.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/mBio.00223-12DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3428693/PubMed CentralArticle
ORCID:
AuthorORCID
Leadbetter, Jared R.0000-0002-7033-0844
Additional Information:© 2012 Zhang and Leadbetter. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Received 10 July 2012; Accepted 16 July 2012; Published 21 August 2012. This work was supported by National Science Foundation grant EF-0523267 and Department of Energy grant DE-FG02-07ER64484 to J.R.L. and a National Science Foundation graduate research fellowship to X.Z. We thank members of the Leadbetter laboratory for their helpful discussions and comments. We are grateful for the aid of Myriam Hernández, Luis G. Acosta, Giselle Tamayo, and Catalina Murillo of the Instituto Nacional de Biodiversidad (Santo Domingo de Heredia, Costa Rica) and Brian Green, Cathy Chang, and Eric J. Mathur, formerly of Verenium, Inc., in termite collection and site access. Termites from Joshua Tree National Park were collected under permit JOTR-2008-SCI-0002. All authors participated in insect collection. X.Z. and J.R.L. conceived of the experiments. X.Z. performed the experiments and analyzed the data. X.Z. and J.R.L. wrote the manuscript. The authors have no competing interests.
Funders:
Funding AgencyGrant Number
NSFEF-0523267
Department of Energy (DOE)DE-FG02-07ER64484
NSF Graduate Research FellowshipUNSPECIFIED
Issue or Number:4
PubMed Central ID:PMC3428693
DOI:10.1128/mBio.00223-12
Record Number:CaltechAUTHORS:20190506-085640418
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190506-085640418
Official Citation:Evidence for Cascades of Perturbation and Adaptation in the Metabolic Genes of Higher Termite Gut Symbionts. Xinning Zhang, Jared R. Leadbetter. mBio Aug 2012, 3 (4) e00223-12; DOI: 10.1128/mBio.00223-12
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:95232
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:06 May 2019 16:11
Last Modified:16 Nov 2021 17:11

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