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

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 demonstrated that higher oxygen concentration in the midgut drives lignocellulose depolymerization, while a thicker gut wall in the anterior hindgut reduces oxygen diffusion and favors 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 their 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 development of specific habitats within the host to promote key microbial metabolic functions. Together, gut anatomical development and microbial functional assembly, enable lignocellulose deconstruction and colonymore » subsistence on an extremely nutrient-poor diet.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [1];  [1];  [3];  [3];  [1];  [4]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [5]; ORCiD logo [2]; ORCiD logo [2];  [6];  [1]
  1. Lawrence Berkeley National Laboratory
  2. BATTELLE (PACIFIC NW LAB)
  3. Purdue University
  4. Louisiana State University
  5. OREGON STATE UNIVERSITY
  6. Lawrence Livermore National Laboratory
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1530556
Report Number(s):
PNNL-SA-138060
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 4; Journal Issue: 5
Country of Publication:
United States
Language:
English

Citation Formats

Ceja Navarro, Javier, Karaoz, Ulas, Bill, Markus, Hao, Zhao, White, Richard A., Arellano, Abelardo, Ramanculova, Leila, Filley, Timothy R., Berry, Timothy, Conrad, Mark E., Blackwell, Meredith, Nicora, Carrie D., Kim, Young-Mo, Reardon, Patrick N., Lipton, Mary S., Adkins, Joshua N., Pett-Ridge, Jennifer, and Brodie, Eoin L. Gut anatomical properties and microbial functional assembly promote lignocellulose deconstruction and colony subsistence of a wood-feeding beetle. United States: N. p., 2019. Web. doi:10.1038/s41564-019-0384-y.
Ceja Navarro, Javier, Karaoz, Ulas, Bill, Markus, Hao, Zhao, White, Richard A., Arellano, Abelardo, Ramanculova, Leila, Filley, Timothy R., Berry, Timothy, Conrad, Mark E., Blackwell, Meredith, Nicora, Carrie D., Kim, Young-Mo, Reardon, Patrick N., Lipton, Mary S., Adkins, Joshua N., Pett-Ridge, Jennifer, & Brodie, Eoin L. Gut anatomical properties and microbial functional assembly promote lignocellulose deconstruction and colony subsistence of a wood-feeding beetle. United States. doi:10.1038/s41564-019-0384-y.
Ceja Navarro, Javier, Karaoz, Ulas, Bill, Markus, Hao, Zhao, White, Richard A., Arellano, Abelardo, Ramanculova, Leila, Filley, Timothy R., Berry, Timothy, Conrad, Mark E., Blackwell, Meredith, Nicora, Carrie D., Kim, Young-Mo, Reardon, Patrick N., Lipton, Mary S., Adkins, Joshua N., Pett-Ridge, Jennifer, and Brodie, Eoin L. Mon . "Gut anatomical properties and microbial functional assembly promote lignocellulose deconstruction and colony subsistence of a wood-feeding beetle". United States. doi:10.1038/s41564-019-0384-y.
@article{osti_1530556,
title = {Gut anatomical properties and microbial functional assembly promote lignocellulose deconstruction and colony subsistence of a wood-feeding beetle},
author = {Ceja Navarro, Javier and Karaoz, Ulas and Bill, Markus and Hao, Zhao and White, Richard A. and Arellano, Abelardo and Ramanculova, Leila and Filley, Timothy R. and Berry, Timothy and Conrad, Mark E. and Blackwell, Meredith and Nicora, Carrie D. and Kim, Young-Mo and Reardon, Patrick N. and Lipton, Mary S. and Adkins, Joshua N. and Pett-Ridge, Jennifer and Brodie, Eoin L.},
abstractNote = {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 demonstrated that higher oxygen concentration in the midgut drives lignocellulose depolymerization, while a thicker gut wall in the anterior hindgut reduces oxygen diffusion and favors 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 their 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 development of specific habitats within the host to promote key microbial metabolic functions. Together, gut anatomical development and microbial functional assembly, enable lignocellulose deconstruction and colony subsistence on an extremely nutrient-poor diet.},
doi = {10.1038/s41564-019-0384-y},
journal = {Nature Microbiology},
number = 5,
volume = 4,
place = {United States},
year = {2019},
month = {3}
}