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

• Published in: Nature microbiology Vol. 6; no. 4; pp. 499 - 511
• Main Authors: Peng, Xuefeng, Wilken, St. Elmo, Lankiewicz, Thomas S., Gilmore, Sean P., Brown, Jennifer L., Henske, John K., Swift, Candice L., Salamov, Asaf, Barry, Kerrie, Grigoriev, Igor V., Theodorou, Michael K., Valentine, David L., O’Malley, Michelle A.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.04.2021; Nature Publishing Group
• Subjects: 38/22; 45; 45/23; 631/326/2522; 631/326/2565; 631/61/252; Acetic acid; Anaerobic bacteria; Anaerobic microorganisms; Anaerobiosis; Animals; Anti-Bacterial Agents - pharmacology; Antibiotics; Archaea - classification; Archaea - drug effects; Archaea - genetics; Archaea - metabolism; Bacteria, Anaerobic - classification; Bacteria, Anaerobic - drug effects; Bacteria, Anaerobic - genetics; Bacteria, Anaerobic - metabolism; BASIC BIOLOGICAL SCIENCES; Biodegradation; Biomass; Biomedical and Life Sciences; Biotechnology; Cellulose; Cellulose - metabolism; Consortia; Digestive system; Division of labor; Fatty acids; Feces; Feces - microbiology; Fungi; Fungi - classification; Fungi - genetics; Fungi - metabolism; Gastrointestinal Microbiome - drug effects; Gastrointestinal Microbiome - genetics; Gastrointestinal tract; Goats; Herbivores; Infectious Diseases; Intestinal microflora; Life Sciences; Lignin - metabolism; Lignocellulose; Medical Microbiology; Metabolic pathways; Metabolome; Metagenome; Metagenomics; Methane; Methane - metabolism; Methanogenic bacteria; Microbial Consortia - drug effects; Microbial Consortia - genetics; Microbiology; Microbiomes; Microbiota; Parasitology; Phylogeny; Propionic acid; Virology
• ISSN: 2058-5276; 2058-5276
• DOI: 10.1038/s41564-020-00861-0

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. More than 400 parallel enrichment experiments from goat faeces are analysed using metagenomics to evaluate how substrate and antibiotic selection affect membership, activity, stability and chemical productivity of herbivore gut microbiomes.