The effects of elevated CO2 concentration on competitive interaction between aceticlastic and syntrophic methanogenesis in a model microbial consortium.

Souichiro Kato,Takashi Yamaguchi,Rina Yoshida,Tomoyuki Sato,Isao Yumoto,Yoichi Kamagata

doi:10.3389/fmicb.2014.00575

Abstract

Investigation of microbial interspecies interactions is essential for elucidating the function and stability of microbial ecosystems. However, community-based analyses including molecular-fingerprinting methods have limitations for precise understanding of interspecies interactions. Construction of model microbial consortia consisting of defined mixed cultures of isolated microorganisms is an excellent method for research on interspecies interactions. In this study, a model microbial consortium consisting of microorganisms that convert acetate into methane directly (Methanosaeta thermophila) and syntrophically (Thermacetogenium phaeum and Methanothermobacter thermautotrophicus) was constructed and the effects of elevated CO2 concentrations on intermicrobial competition were investigated. Analyses on the community dynamics by quantitative RT-PCR and fluorescent in situ hybridization targeting their 16S rRNAs revealed that high concentrations of CO2 have suppressive effects on the syntrophic microorganisms, but not on the aceticlastic methanogen. The pathways were further characterized by determining the Gibbs free energy changes (ΔG) of the metabolic reactions conducted by each microorganism under different CO2 concentrations. The ΔG value of the acetate oxidation reaction (T. phaeum) under high CO2 conditions became significantly higher than -20 kJ per mol of acetate, which is the borderline level for sustaining microbial growth. These results suggest that high concentrations of CO2 undermine energy acquisition of T. phaeum, resulting in dominance of the aceticlastic methanogen. This study demonstrates that investigation on model microbial consortia is useful for untangling microbial interspecies interactions, including competition among microorganisms occupying the same trophic niche in complex microbial ecosystems.

Highlights

In natural and engineered environments, many species of microorganisms coexist by interacting with each other
As the model consortium performing methanogenic acetate degradation, we utilized a defined mixed culture of an aceticlastic methanogen (Methanosaeta thermophila), a hydrogenotrophic methanogen (Methanothermobacter thermautotrophicus), and a syntrophic acetate-oxidizing bacteria (SAOB) (T. phaeum; Table 3). These microbial species were originally isolated from a thermophilic methanogenic digester (Kamagata and Mikami, 1991; Hattori et al, 2000) and are regarded as representative species for the methanogenic acetate degradation reactions that occur in various natural environments such as high-temperature petroleum reservoirs (Pham et al, 2009; Mayumi et al, 2011, 2013) and thermophilic methanogenic digesters (Sekiguchi et al, 1998; McHugh et al, 2003; Hori et al, 2011)
CO2 ]initial, consortium were composed of Methanosaeta thermophila, Methanothermobacter thermautotrophicus, and T. phaeum was cultivated under the three different [ CO2]initial conditions to evaluate their methanogenic acetate degradation abilities (Figure 1)

Summary

Introduction

In natural and engineered environments, many species of microorganisms coexist by interacting with each other. Comprehension of interspecies interactions is essential for describing the features of complex microbial ecosystems, and competition among microorganisms occupying similar trophic niches is a conventional and significant aspect of such interspecies interaction. Coexistence of multiple microorganisms with similar trophic niches is regarded as one of the major factors to confer functional stability and resiliency on microbial ecosystems (Loreau et al, 2001; Deng, 2012). Most microbial ecological research has assessed the effects of specific environmental factors on competitive interactions among multiple microbial species by observing the transition of abundances of each microorganism responding to environmental disturbances. This approach has produced many excellent outcomes, existence of non-target microorganisms and uncontrollable environmental factors in the systems often hamper precise understanding of the effects of specific environmental factors on the competitive interactions among target microorganisms

Methods

Results

Conclusion