"Gut anatomical properties and microbial functional assembly promote li" by Javier A. Ceja-Navarro, Ulas Karaoz et al.

Faculty Publications

Title

Gut anatomical properties and microbial functional assembly promote lignocellulose deconstruction and colony subsistence of a wood-feeding beetle

Authors

Javier A. Ceja-Navarro, Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Ulas Karaoz, Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Markus Bill, Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Zhao Hao, Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Richard A. White, Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, USA.
Abelardo Arellano, Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Leila Ramanculova, Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
Timothy R. Filley, Department of Earth, Atmospheric, and Planetary Sciences, Purdue University, West Lafayette, IN, USA.

Document Type

Article

Publication Date

5-1-2019

Abstract

Beneficial microbial associations enhance the fitness of most living organisms, and wood-feeding insects offer some of the most striking examples of this. Odontotaenius disjunctus is a wood-feeding beetle that possesses a digestive tract with four main compartments, each of which contains well-differentiated microbial populations, suggesting that anatomical properties and separation of these compartments may enhance energy extraction from woody biomass. Here, using integrated chemical analyses, we demonstrate that lignocellulose deconstruction and fermentation occur sequentially across compartments, and that selection for microbial groups and their metabolic pathways is facilitated by gut anatomical features. Metaproteogenomics showed that higher oxygen concentration in the midgut drives lignocellulose depolymerization, while a thicker gut wall in the anterior hindgut reduces oxygen diffusion and favours hydrogen accumulation, facilitating fermentation, homoacetogenesis and nitrogen fixation. We demonstrate that depolymerization continues in the posterior hindgut, and that the beetle excretes an energy- and nutrient-rich product on which its offspring subsist and develop. Our results show that the establishment of beneficial microbial partners within a host requires both the acquisition of the microorganisms and the formation of specific habitats within the host to promote key microbial metabolic functions. Together, gut anatomical properties and microbial functional assembly enable lignocellulose deconstruction and colony subsistence on an extremely nutrient-poor diet.

Publication Source (Journal or Book title)

Nature microbiology

First Page

864

Last Page

875

Recommended Citation

Ceja-Navarro, J. A., Karaoz, U., Bill, M., Hao, Z., White, R. A., Arellano, A., Ramanculova, L., & Filley, T. R. (2019). Gut anatomical properties and microbial functional assembly promote lignocellulose deconstruction and colony subsistence of a wood-feeding beetle. Nature microbiology, 4 (5), 864-875. https://doi.org/10.1038/s41564-019-0384-y

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