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Nat Microbiol. 2019 May;4(5):864-875. doi: 10.1038/s41564-019-0384-y. Epub 2019 Mar 11.

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

Author information

1
Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
2
Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, USA.
3
Department of Earth, Atmospheric, and Planetary Sciences, Purdue University, West Lafayette, IN, USA.
4
Department of Soil Science, University of Wisconsin, Madison, WI, USA.
5
Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, USA.
6
University of South Carolina, Columbia, SC, USA.
7
NMR Facility, Oregon State University, Corvallis, OR, USA.
8
Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA, USA.
9
Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, USA.
10
Ecology Department, Earth and Environmental Sciences, Lawrence Berkeley National Laboratory, Berkeley, CA, USA. ELBrodie@lbl.gov.
11
Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, USA. ELBrodie@lbl.gov.

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.

PMID:
30858574
DOI:
10.1038/s41564-019-0384-y
[Indexed for MEDLINE]

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