Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus
Abstract
Coarse woody debris is an important biomass pool in forest ecosystems that numerous groups of insects have evolved to take advantage of. These insects are ecologically important and represent useful natural analogs for biomass to biofuel conversion. Using a range of molecular approaches combined with microelectrode measurements of oxygen, here we have characterized the gut microbiome and physiology of Odontotaenius disjunctus, a wood-feeding beetle native to the eastern United States. We hypothesized that morphological and physiological differences among gut regions would correspond to distinct microbial populations and activities. In fact, significantly different communities were found in the foregut (FG), midgut (MG)/posterior hindgut (PHG) and anterior hindgut (AHG), with Actinobacteria and Rhizobiales being more abundant toward the FG and PHG. Conversely, fermentative bacteria such as Bacteroidetes and Clostridia were more abundant in the AHG, and also the sole region where methanogenic Archaea were detected. Although each gut region possessed an anaerobic core, micron-scale profiling identified radial gradients in oxygen concentration in all regions. Nitrogen fixation was confirmed by 15N2 incorporation, and nitrogenase gene (nifH) expression was greatest in the AHG. Phylogenetic analysis of nifH identified the most abundant transcript as related to Ni–Fe nitrogenase of a Bacteroidetes species, Paludibacter propionicigenes. Overall,more »
- Authors:
-
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division, Ecology Dept.
- Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
- Louisiana State Univ., Baton Rouge, LA (United States). Dept. of Biological Sciences
- Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science Policy and Management
- Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Chemical Sciences Division
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division, Ecology Dept.; Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science Policy and Management
- Publication Date:
- Research Org.:
- Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER); Conacyt, Mexico City (Mexico); National Science Foundation (NSF)
- OSTI Identifier:
- 1647142
- Report Number(s):
- LLNL-JRNL-582992
Journal ID: ISSN 1751-7362; 659332
- Grant/Contract Number:
- AC52-07NA27344; SCW1039; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; environmental sciences; energy - hydrogen; biological and medical sciences; chemistry - inorganic; organic; physical and analytical chemistry; chemistry - isotopes and radiation sources; symbiosis; microbial diversity; gut microbiome; insect; passalidae; cellulose; entomology; microbial ecology
Citation Formats
Ceja-Navarro, Javier A., Nguyen, Nhu H., Karaoz, Ulas, Gross, Stephanie R., Herman, Donald J., Andersen, Gary L., Bruns, Thomas D., Pett-Ridge, Jennifer, Blackwell, Meredith, and Brodie, Eoin L. Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus. United States: N. p., 2013.
Web. doi:10.1038/ismej.2013.134.
Ceja-Navarro, Javier A., Nguyen, Nhu H., Karaoz, Ulas, Gross, Stephanie R., Herman, Donald J., Andersen, Gary L., Bruns, Thomas D., Pett-Ridge, Jennifer, Blackwell, Meredith, & Brodie, Eoin L. Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus. United States. https://doi.org/10.1038/ismej.2013.134
Ceja-Navarro, Javier A., Nguyen, Nhu H., Karaoz, Ulas, Gross, Stephanie R., Herman, Donald J., Andersen, Gary L., Bruns, Thomas D., Pett-Ridge, Jennifer, Blackwell, Meredith, and Brodie, Eoin L. Thu .
"Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus". United States. https://doi.org/10.1038/ismej.2013.134. https://www.osti.gov/servlets/purl/1647142.
@article{osti_1647142,
title = {Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus},
author = {Ceja-Navarro, Javier A. and Nguyen, Nhu H. and Karaoz, Ulas and Gross, Stephanie R. and Herman, Donald J. and Andersen, Gary L. and Bruns, Thomas D. and Pett-Ridge, Jennifer and Blackwell, Meredith and Brodie, Eoin L.},
abstractNote = {Coarse woody debris is an important biomass pool in forest ecosystems that numerous groups of insects have evolved to take advantage of. These insects are ecologically important and represent useful natural analogs for biomass to biofuel conversion. Using a range of molecular approaches combined with microelectrode measurements of oxygen, here we have characterized the gut microbiome and physiology of Odontotaenius disjunctus, a wood-feeding beetle native to the eastern United States. We hypothesized that morphological and physiological differences among gut regions would correspond to distinct microbial populations and activities. In fact, significantly different communities were found in the foregut (FG), midgut (MG)/posterior hindgut (PHG) and anterior hindgut (AHG), with Actinobacteria and Rhizobiales being more abundant toward the FG and PHG. Conversely, fermentative bacteria such as Bacteroidetes and Clostridia were more abundant in the AHG, and also the sole region where methanogenic Archaea were detected. Although each gut region possessed an anaerobic core, micron-scale profiling identified radial gradients in oxygen concentration in all regions. Nitrogen fixation was confirmed by 15N2 incorporation, and nitrogenase gene (nifH) expression was greatest in the AHG. Phylogenetic analysis of nifH identified the most abundant transcript as related to Ni–Fe nitrogenase of a Bacteroidetes species, Paludibacter propionicigenes. Overall, we demonstrate not only a compartmentalized microbiome in this beetle digestive tract but also sharp oxygen gradients that may permit aerobic and anaerobic metabolism to occur within the same regions in close proximity. We provide evidence for the microbial fixation of N2 that is important for this beetle to subsist on woody biomass.},
doi = {10.1038/ismej.2013.134},
journal = {The ISME Journal},
number = 1,
volume = 8,
place = {United States},
year = {Thu Aug 29 00:00:00 EDT 2013},
month = {Thu Aug 29 00:00:00 EDT 2013}
}
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