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.

Highlights

  • In most natural environments, microbial individuals rarely live alone but co-colonize with other species to form complex communities

  • We found that many MAGs were highly abundant in the four anaerobic methanogenic communities (AMCs), but did not contain the genes involved in the above core methanogenic pathways, which we defined as “noncore functional bacteria,” including 45 MAGs in ATL, 55 MAGs in PTL, 40 MAGs in BTL, and 42 MAGs in VTL

  • The prevalent lack of amino acids (AAs) synthesis capacity among MAGs suggested that metabolic interdependency relying on public goods (PGs) sharing is essential for the survival of these MAGs in our four AMCs

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Summary

Introduction

Microbial individuals rarely live alone but co-colonize with other species to form complex communities. Associated with PG sharing, several genomic investigations indicate that many microorganisms in diverse environments [such as methanogenic chemostats (Hubalek et al, 2017), oil reservoir (Liu et al, 2018), and human gut (Soto-Martin et al, 2020)] contain only a small set of genes that encode these public functions, so they must survive by exchanging PGs with other members This phenomenon reflects that PG sharing is a main force to drive the microbial genomic evolution (Morris et al, 2011) and play important roles in governing the assembly of the community (Zengler and Zaramela, 2018). Uncovering these factors is crucial for understanding microbial evolution at community scale, as well as uncovering the assembly rule of microbial community with complex interaction networks

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