Energy Availability Determines Strategy of Microbial Amino Acid Synthesis in Volatile Fatty Acid–Fed Anaerobic Methanogenic Chemostats

Abstract

In natural communities, microbes exchange a variety of metabolites (public goods) with each other, which drives the evolution of auxotroph and shapes interdependent patterns at community-level. However, factors that determine the strategy of public goods synthesis for a given community member still remains to be elucidated. In anaerobic methanogenic communities, energy availability of different community members is largely varied. We hypothesized that this uneven energy availability contributed to the heterogeneity of public goods synthesis ability among the members in these communities. We tested this hypothesis by analyzing the synthetic strategy of amino acids of the bacterial and archaeal members involved in four previously enriched anaerobic methanogenic communities residing in thermophilic chemostats. Our analyses indicate that most of the members in the communities did not possess ability to synthesize all the essential amino acids, suggesting they exchanged these essential public goods to establish interdependent patterns for survival. Importantly, we found that the amino acid synthesis ability of a functional group was largely determined by how much energy it could obtain from its metabolism in the given environmental condition. Moreover, members within a functional group also possessed different amino acid synthesis abilities, which are related to their features of energy metabolism. Our study reveals that energy availability is a key driver of microbial evolution in presence of metabolic specialization at community level and suggests the feasibility of managing anaerobic methanogenic communities for better performance through controlling the metabolic interactions involved.

High synthetic cost-amino acids reduce member interactions of acetate-degrading methanogenic microbial community

“…Compared to Methanosarcina , bacterial genera in the community (e.g., SAOB) are at a disadvantage in the competition for acetate and therefore adopt a survival strategy that reduces their ability to synthesize AAs (especially high-cost AAs). In our previous study ( Yao et al, 2021 ), we found that SAOBs generally cannot synthesize the majority of the 20 AAs, especially those with medium and high synthetic costs. This increases the AA’s dependence of SAOBs and then reduces its metabolic activity.…”

“…We summarized the daily production of biogas and the proportions of gas components in each reactor during the stabilization phase after reactor recovery and tested the differences among reactors by Tukey’s test ( Figure 1 ). When acetate is used as the carbon source, methane is produced through two pathways, one is that acetate can be converted to methane directedly by acetoclastic methanogens, and the other is that acetate is oxidized by syntrophic acetate-oxidizing bacteria (SAOB) to produce hydrogen and carbon dioxide which are later converted to methane by hydrogenotrophic methanogens ( Schink, 1997 ; Yao et al, 2021 ). Thus, the biogas production as well as the biogas composition can reflect the activity of methanogens and bacteria in the microbial community.…”

“…This variability may be related to the difference in energy accessibility among methanogens and bacteria in reactors. In methanogenic reactors where acetate is the sole carbon source, the methanogen Methanosarcina has high acetate accessibility because of both the acetate trophic pathway and the hydrogen trophic pathways ( Schink, 1997 ; Yao et al, 2021 ), leading to their absolute dominance in communities. Low energy accessibility or stress conditions promote microorganisms to interact more with each other (share more public goods, e.g., AAs, cobalamin) to cope with unfavorable conditions, which is an optimized survival strategy ( Piccardi et al, 2019 ; Zhao et al, 2023 ).…”

“…It is clear that the number of interaction relationships of the bacterial genera with lower energy accessibility in our reactors was significantly higher than that of Methanosarcina ( Supplementary Figures S3a–e ). In addition, Methanosarcina was able to synthesize most of AAs itself ( Yao et al, 2021 ) and the high energetic accessibility makes Methanosarcina not highly exogenous AA dependent. Therefore, the supplementation with different cost AAs had a lower effect on the number of interactions of Methanosarcina than other members ( Supplementary Figure S3f ).…”

“…In our study, the supplementation of different cost AAs all reduced the proportion of positive interactions among members, with the most significant effect being achieved by the supplementation of AAs with high synthesis cost. In our previous study, very few members in the acetate-degrading anaerobic microbial community were able to synthesize high-cost AAs ( Yao et al, 2021 ). This phenomenon was similarly found in the study of Mee et al (2014) and in the synthetic syntrophic community, biosynthetically costly AAs tended to promote stronger synergistic interactions.…”