Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics
Abstract
Linking the genomic content of uncultivated microbes to their metabolic functions remains a critical challenge in microbial ecology. Resolving this challenge has implications for improving our management of key microbial interactions in biotechnologies such as anaerobic digestion, which relies on slow-growing syntrophic and methanogenic communities to produce renewable methane from organic waste. In this study, we combined DNA stable-isotope probing (SIP) with genome-centric metagenomics to recover the genomes of populations enriched in13C after growing on [13C]butyrate. Differential abundance analysis of recovered genomic bins across the SIP metagenomes identified two metagenome-assembled genomes (MAGs) that were significantly enriched in heavy [13C]DNA. Phylogenomic analysis assigned one MAG to the genus Syntrophomonas and the other MAG to the genus Methanothrix. Metabolic reconstruction of the annotated genomes showed that the Syntrophomonas genome encoded all the enzymes for beta-oxidizing butyrate, as well as several mechanisms for interspecies electron transfer via electron transfer flavoproteins, hydrogenases, and formate dehydrogenases. The Syntrophomonas genome shared low average nucleotide identity (<95%) with any cultured representative species, indicating that it is a novel species that plays a significant role in syntrophic butyrate degradation within anaerobic digesters. The Methanothrix genome contained the complete pathway for acetoclastic methanogenesis, indicating that it was enriched in13Cmore »
- Authors:
-
[1];
- Univ. of Waterloo, ON (Canada)
- National Inst. of Advanced Industrial Science and Technology (AIST), Tsukuba (Japan)
- Wageningen Univ. (Netherlands)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Sciences and Engineering Research Council of Canada (NSERC); USEPA; Netherlands Organization for Scientific Research (NWO); Wageningen Institute for Environmental and Climate Research (WIMEK)
- OSTI Identifier:
- 1626172
- Grant/Contract Number:
- AC02-05CH11231; RD835567; 323009; 040.15.014
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mSystems
- Additional Journal Information:
- Journal Volume: 4; Journal Issue: 4; Journal ID: ISSN 2379-5077
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; microbiology; anaerobic catabolic pathways; anaerobic digestion; metagenomics; methanogenesis; stable-isotope probing; syntrophy
Citation Formats
Ziels, Ryan M., Nobu, Masaru K., and Sousa, Diana Z. Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics. United States: N. p., 2019.
Web. doi:10.1128/msystems.00159-19.
Ziels, Ryan M., Nobu, Masaru K., & Sousa, Diana Z. Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics. United States. https://doi.org/10.1128/msystems.00159-19
Ziels, Ryan M., Nobu, Masaru K., and Sousa, Diana Z. Tue .
"Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics". United States. https://doi.org/10.1128/msystems.00159-19. https://www.osti.gov/servlets/purl/1626172.
@article{osti_1626172,
title = {Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics},
author = {Ziels, Ryan M. and Nobu, Masaru K. and Sousa, Diana Z.},
abstractNote = {Linking the genomic content of uncultivated microbes to their metabolic functions remains a critical challenge in microbial ecology. Resolving this challenge has implications for improving our management of key microbial interactions in biotechnologies such as anaerobic digestion, which relies on slow-growing syntrophic and methanogenic communities to produce renewable methane from organic waste. In this study, we combined DNA stable-isotope probing (SIP) with genome-centric metagenomics to recover the genomes of populations enriched in13C after growing on [13C]butyrate. Differential abundance analysis of recovered genomic bins across the SIP metagenomes identified two metagenome-assembled genomes (MAGs) that were significantly enriched in heavy [13C]DNA. Phylogenomic analysis assigned one MAG to the genus Syntrophomonas and the other MAG to the genus Methanothrix. Metabolic reconstruction of the annotated genomes showed that the Syntrophomonas genome encoded all the enzymes for beta-oxidizing butyrate, as well as several mechanisms for interspecies electron transfer via electron transfer flavoproteins, hydrogenases, and formate dehydrogenases. The Syntrophomonas genome shared low average nucleotide identity (<95%) with any cultured representative species, indicating that it is a novel species that plays a significant role in syntrophic butyrate degradation within anaerobic digesters. The Methanothrix genome contained the complete pathway for acetoclastic methanogenesis, indicating that it was enriched in13C from syntrophic acetate transfer. This study demonstrates the potential of stable-isotope-informed genome-resolved metagenomics to identifyin situinterspecies metabolic cooperation within syntrophic consortia important to anaerobic waste treatment as well as global carbon cycling.},
doi = {10.1128/msystems.00159-19},
journal = {mSystems},
number = 4,
volume = 4,
place = {United States},
year = {Tue Aug 06 00:00:00 EDT 2019},
month = {Tue Aug 06 00:00:00 EDT 2019}
}
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Ferroferric oxide triggered possible direct interspecies electron transfer between Syntrophomonas and Methanosaeta to enhance waste activated sludge anaerobic digestion
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Microbial nanowires for bioenergy applications
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The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii : Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis
journal, August 2017
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Peat: home to novel syntrophic species that feed acetate- and hydrogen-scavenging methanogens
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