"Compartmentalized microbial composition, oxygen gradients and nitrogen" by Javier A. Ceja-Navarro, Nhu H. Nguyen et al.

Faculty Publications

Title

Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus

Authors

Javier A. Ceja-Navarro, Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Nhu H. Nguyen, Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA.
Ulas Karaoz, Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Stephanie R. Gross, Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA.
Donald J. Herman, Department of Environmental Science Policy and Management, University of California, Berkeley, CA, USA.
Gary L. Andersen, Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Thomas D. Bruns, Ecology Department, Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Jennifer Pett-Ridge, Chemical Sciences Division, Lawrence Livermore National Laboratory, Livermore, CA, USA.

Document Type

Article

Publication Date

1-1-2014

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, 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 (15)N2 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.

Publication Source (Journal or Book title)

The ISME journal

First Page

Last Page

Recommended Citation

Ceja-Navarro, J. A., Nguyen, N. H., Karaoz, U., Gross, S. R., Herman, D. J., Andersen, G. L., Bruns, T. D., & Pett-Ridge, J. (2014). Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus. The ISME journal, 8 (1), 6-18. https://doi.org/10.1038/ismej.2013.134

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