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

Ceja-Navarro, Javier A.; Karaoz, Ulas; Bill, Markus; Hao, Zhao; White, Richard A.; Arellano, Abelardo; Ramanculova, Leila; Filley, Timothy R.; Berry, Timothy D.; 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.

doi:10.1038/s41564-019-0384-y

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

Journal Article · Mon Mar 11 00:00:00 EDT 2019 · Nature Microbiology

DOI:https://doi.org/10.1038/s41564-019-0384-y· OSTI ID:1526163

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^[1]; Bill, Markus ^[1];

^[1]; White, Richard A. ^[2]; Arellano, Abelardo ^[1]; Ramanculova, Leila ^[1]; Filley, Timothy R. ^[3]; Berry, Timothy D. ^[3]; Conrad, Mark E. ^[1];

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^[6]; Pett-Ridge, Jennifer ^[7];

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Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Purdue Univ., West Lafayette, IN (United States)
Louisiana State Univ., Baton Rouge, LA (United States); Univ. of South Carolina, Columbia, SC (United States)
Oregon State Univ., Corvallis, OR (United States)
Univ. of South Carolina, Columbia, SC (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

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.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC52-07NA27344; AC05-76RL01830; SCW1039; AC02-05CH11231; S10RR029668; S10RR027303

OSTI ID:: 1526163

Alternate ID(s):: OSTI ID: 1530556; OSTI ID: 1571997

Report Number(s):: LLNL-JRNL-738827; PNNL-SA-138060; 892106

Journal Information:: Nature Microbiology, Vol. 4, Issue 5; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 36 works

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

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