Abstract

Methane-producing microbial communities are of ecological and biotechnological interest. Syntrophic interactions among sulfate reducers and aceto/hydrogenotrophic and obligate hydrogenotrophic methanogens form a key component of these communities, yet, the impact of these different syntrophic routes on methane production and their stability against sulfate availability are not well understood. Here, we construct model synthetic communities using a sulfate reducer and two types of methanogens representing different methanogenesis routes. We find that tri-cultures with both routes increase methane production by almost twofold compared to co-cultures and are stable in the absence of sulfate. With increasing sulfate, system stability and productivity decreases and does so faster in communities with aceto/hydrogenotrophic methanogens despite the continued presence of acetate. We show that this is due to a shift in the metabolism of these methanogens towards co-utilization of hydrogen with acetate. These findings indicate the important role of hydrogen dynamics in the stability and productivity of syntrophic communities.

Highlights

  • All studied habitats, ranging from human and animal guts to the soil and ocean, are found to be inhabited by microbial communities composed of hundreds of different species [1]

  • We used three key species to represent the roles of sulfate-reducing bacteria (SRB) (Desulfovibrio vulgaris Hildenborough; Dv), and hydrogenotrophic/acetotrophic (Methanosarcina barkeri; Mb) and hydrogenotrophic methanogens (Methanococcus maripaludis; Mm)

  • The Dv–Mm pair has emerged in recent years as a model system to study syntrophic interactions [44] and was recently shown to be enabled by polymorphisms found in Dv [45]

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Summary

Introduction

All studied habitats, ranging from human and animal guts to the soil and ocean, are found to be inhabited by microbial communities composed of hundreds of different species [1]. Interactions among these species give rise to community-level functions, including metabolic conversions that enable animal and plant nutrition [2,3], and geo-biochemical cycles [4,5]. Towards deciphering ecological and evolutionary drivers of function and functional stability in microbial communities, methanogenic anaerobic digestion (AD) offers an ideal model system, where the production of methane from complex organic substrates can be taken as a proxy for a community function. It is well known that high substrate levels and limited availability of electron acceptors in the AD system can create thermodynamic limitations that can dominate functional stability and community dynamics [15], underpin the emergence and maintenance of diversity in the community [16] and drive evolution of

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