Below the familiar oxygenated biosphere lay ecosystems teeming with “anaerobic” prokaryotes thriving in the absence of O2. As anaerobes exhaust compounds for favorable respiration (e.g., NO3- and SO42-), microorganisms resort to fermentation and respiration of H+ and CO2. Across Earth, microbial communities under such environmental conditions are estimated to annually mineralize 1~2 GT of organic carbon to CH4 and CO2, thereby driving a critical step in the global carbon cycle. Since the discovery that we can tame such “methanogenic” (methane-generating) microbial communities to convert society’s organic waste to CH4 as a recoverable fuel, this biotechnology has become an essential component of managing municipal and industrial waste and development of sustainable energy. Driven by the environmental and technological significance, research has found four major niches form metabolic interactions to facilitate methanogenic degradation of organic carbon: hydrolyzers, fermenters, syntrophs, and methanogens. Despite this defined general ecological structure, many organisms and metabolism in methanogenic ecosystems remain uncharacterized due to challenges in handling and cultivating anaerobes. To tackle this issue, we can employ rapidly developing sequencing technology to recover genomes for uncultivated organisms directly from the environment (“metagenomics”), obtain insight into their physiology, and ultimately uncover hitherto overlooked ecological and biochemical processes taking place in methanogenic natural ecosystems and engineered systems.In the series of studies presented in this dissertation, we use methanogenic wastewater treatment bioreactors as model ecosystems and implement cutting-edge bioinformatics with rigorous annotation of anaerobic metabolic capacities to investigate the ecological roles of uncultured syntrophs, methanogens, and organisms from other bacterial lineages. For syntrophs, we characterize novel aromatic compound degradation pathways and find that syntrophic catabolism and interactions are much more diverse and flexible than previously anticipated, opening new possibilities for ecological niches that syntrophs can exploit. In investigating methanogens, we successfully recover the first genomes for a methanogen-related Euryarchaeota class WSA2 found across various anaerobic environments and discover that they encode unique H2-oxidizing methyl-compound-reducing methanogenesis, suggesting that this may be a major process in both natural and engineered methanogenic environments. As for uncharacterized bacterial lineages, we acquire genomes for populations spanning 15 phyla, of which 5 are bacterial phyla with no cultured representatives (“candidate phyla”). We find that these organisms may contribute to novel syntrophic, fermentative, and acetogenic processes and form intricate metabolic interactions to facilitate complete mineralization of organic matter to in methanogenic ecosystems. Finally, to expand the application of the approach used throughout these studies, we compile the accumulated insight into genomics and complex metabolism and perform an unprecedentedly large-scale comparative genomics analysis on a bacterial phylum that contains both uncultivated lineages affiliated with methanogenic ecosystems and poorly understood lineages prevalent across Earth: Bacteroidetes. This reveals novel relationships between phylogeny, metabolism, and habitats and unnoticed ecological roles that Bacteroidetes can take in methanogenic environments, marine ecosystems, and even the human gastrointestinal tract. In total, we demonstrate that integration of metagenomics, comparative genomics, and strict annotation of metabolic capacity can effectively characterize the ecophysiology of uncultivated organisms and reveal novel ecological niches in methanogenic environments and beyond.
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Omics-based characterization of complex anaerobic metabolism in methanogenic wastewater treatment
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