4.5 Article

Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes

Journal

NATURE MICROBIOLOGY
Volume 6, Issue 4, Pages 499-+

Publisher

NATURE PORTFOLIO
DOI: 10.1038/s41564-020-00861-0

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Funding

  1. National Science Foundation (NSF) [MCB-1553721]
  2. Office of Science (BER) of the US Department of Energy (DOE) [DE-SC0010352]
  3. Institute for Collaborative Biotechnologies from the US Army Research Office [W911NF-09-D-0001, W911NF-19-2-0026]
  4. Camille Dreyfus Teacher-Scholar Awards Program
  5. University of California, Santa Barbara (UCSB)
  6. University of California, Office of the President
  7. Office of Biological and Environmental Research of the DOE Office of Science [DE-AC02-05CH11231]
  8. Dow Discovery Fellowship
  9. NSF Graduate Research Fellowship Program
  10. Office of Science of the US DOE [DE-AC02-05CH11231]
  11. NSF [ACI-1548562, CNS-0960316]
  12. NSF at the Pittsburgh Supercomputing Center [ACI-1445606]
  13. California NanoSystems Institute
  14. Materials Research Science and Engineering Center (MRSEC) at UCSB [NSF DMR 1720256]

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The study found that microbial consortia dominated by anaerobic fungi outperformed bacterially dominated consortia in methane production and cellulose degradation. Cross-domain partnerships between fungi and methanogens enabled the production of acetate, formate, and methane, while bacterially dominated consortia mainly produced short-chain fatty acids. The division of labor among herbivore anaerobes for plant biomass degradation could be utilized for industrial bioprocessing.
The herbivore digestive tract is home to a complex community of anaerobic microbes that work together to break down lignocellulose. These microbiota are an untapped resource of strains, pathways and enzymes that could be applied to convert plant waste into sugar substrates for green biotechnology. We carried out more than 400 parallel enrichment experiments from goat faeces to determine how substrate and antibiotic selection influence membership, activity, stability and chemical productivity of herbivore gut communities. We assembled 719 high-quality metagenome-assembled genomes (MAGs) that are unique at the species level. More than 90% of these MAGs are from previously unidentified herbivore gut microorganisms. Microbial consortia dominated by anaerobic fungi outperformed bacterially dominated consortia in terms of both methane production and extent of cellulose degradation, which indicates that fungi have an important role in methane release. Metabolic pathway reconstructions from MAGs of 737 bacteria, archaea and fungi suggest that cross-domain partnerships between fungi and methanogens enabled production of acetate, formate and methane, whereas bacterially dominated consortia mainly produced short-chain fatty acids, including propionate and butyrate. Analyses of carbohydrate-active enzyme domains present in each anaerobic consortium suggest that anaerobic bacteria and fungi employ mostly complementary hydrolytic strategies. The division of labour among herbivore anaerobes to degrade plant biomass could be harnessed for industrial bioprocessing.

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