Abstract

Methanogenesis, a biological process mediated by complex microbial communities, has attracted great attention due to its contribution to global warming and potential in biotechnological applications. The current study unveiled the core microbial methanogenic metabolisms in anaerobic vessel ecosystems by applying combined genome-centric metagenomics and metatranscriptomics. Here, we demonstrate that an enriched natural system, fueled only with acetate, could support a bacteria-dominated microbiota employing a multi-trophic methanogenic process. Moreover, significant changes, in terms of microbial structure and function, were recorded after the system was supplemented with additional H2. Methanosarcina thermophila, the predominant methanogen prior to H2 addition, simultaneously performed acetoclastic, hydrogenotrophic, and methylotrophic methanogenesis. The methanogenic pattern changed after the addition of H2, which immediately stimulated Methanomicrobia-activity and was followed by a slow enrichment of Methanobacteria members. Interestingly, the essential genes involved in the Wood-Ljungdahl pathway were not expressed in bacterial members. The high expression of a glycine cleavage system indicated the activation of alternative metabolic pathways for acetate metabolism, which were reconstructed in the most abundant bacterial genomes. Moreover, as evidenced by predicted auxotrophies, we propose that specific microbes of the community were forming symbiotic relationships, thus reducing the biosynthetic burden of individual members. These results provide new information that will facilitate future microbial ecology studies of interspecies competition and symbiosis in methanogenic niches.6mWxSszdRnKL2KDYxsStzzVideo abstract.

Highlights

  • Microbial methanogenic metabolism is considered as one of the oldest bio-activities on earth and draws great attention because of its global warming potential [1], which is 28 times higher than carbon dioxide (CO2) on a 100-year horizon [2]

  • The majority of studies regarding methanogenic process were focused on specific microbes contributing to the degradation of recalcitrant substrates [9] or the involvement of rare taxon in the methanogenic process [10, 11], while few attempts have been made to underlie the basic mechanisms of microbial community assembly and function [7, 12, 13]

  • A significant discrepancy among triplicate reactors was observed during the transition before and after H2 addition (Sample Point 2), which was mainly attributed to the instability of the microbial community adaptation process

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Summary

Introduction

Microbial methanogenic metabolism is considered as one of the oldest bio-activities on earth and draws great attention because of its global warming potential [1] , which is 28 times higher than carbon dioxide (CO2) on a 100-year horizon [2]. Genome-centric metagenomics was extensively used to describe complex syntrophic microbial communities, and successfully revealed essential knowledge regarding the microbial functions of the keystone species mainly based on their gene profiles [7, 8]. The in-situ activity of the individual members in microbial communities and the ecological relationships existing among microbes were extremely difficult to elucidate during the digestion of complexed substrates. A previous study dissected the complex methanogenic consortium into tractable model sections by substrates specification in continuous reactor operation and successfully assigned putative functional roles to the de-novo reconstructed genomes [12]. Other –omics approaches and advanced molecular tools, such as transcriptomics, proteomics, metabolomics, and stable isotope labelling were gradually introduced to analyze the microbial activity during the methanogenic process [14,15,16,17]

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