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Synergistic epistasis enhances the co-operativity of mutualistic interspecies interactions.

ABSTRACT: Early evolution of mutualism is characterized by big and predictable adaptive changes, including the specialization of interacting partners, such as through deleterious mutations in genes not required for metabolic cross-feeding. We sought to investigate whether these early mutations improve cooperativity by manifesting in synergistic epistasis between genomes of the mutually interacting species. Specifically, we have characterized evolutionary trajectories of syntrophic interactions of Desulfovibrio vulgaris (Dv) with Methanococcus maripaludis (Mm) by longitudinally monitoring mutations accumulated over 1000 generations of nine independently evolved communities with analysis of the genotypic structure of one community down to the single-cell level. We discovered extensive parallelism across communities despite considerable variance in their evolutionary trajectories and the perseverance within many evolution lines of a rare lineage of Dv that retained sulfate-respiration (SR+) capability, which is not required for metabolic cross-feeding. An in-depth investigation revealed that synergistic epistasis across pairings of Dv and Mm genotypes had enhanced cooperativity within SR- and SR+ assemblages, enabling their coexistence within the same community. Thus, our findings demonstrate that cooperativity of a mutualism can improve through synergistic epistasis between genomes of the interacting species, enabling the coexistence of mutualistic assemblages of generalists and their specialized variants.

SUBMITTER: Turkarslan S

PROVIDER: S-EPMC8319347 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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Synergistic epistasis enhances the co-operativity of mutualistic interspecies interactions.

Turkarslan Serdar S Stopnisek Nejc N Thompson Anne W AW Arens Christina E CE Valenzuela Jacob J JJ Wilson James J Hunt Kristopher A KA Hardwicke Jessica J de Lomana Adrián López García ALG Lim Sujung S Seah Yee Mey YM Fu Ying Y Wu Liyou L Zhou Jizhong J Hillesland Kristina L KL Stahl David A DA Baliga Nitin S NS

The ISME journal 20210221 8

Early evolution of mutualism is characterized by big and predictable adaptive changes, including the specialization of interacting partners, such as through deleterious mutations in genes not required for metabolic cross-feeding. We sought to investigate whether these early mutations improve cooperativity by manifesting in synergistic epistasis between genomes of the mutually interacting species. Specifically, we have characterized evolutionary trajectories of syntrophic interactions of Desulfov ...[more]

PMID: 33612833

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Project description:Metabolic exchange plays a crucial role in shaping microbial community interactions and functions, including the exchange of small molecules such as cofactors. Cofactors are fundamental to enzyme catalytic activities; however, the role of cofactors in microbial stress tolerance is unclear. Here, we constructed a synergistic consortium containing two strains that could efficiently mineralize di-(2-ethylhexyl) phthalate under hyperosmotic stress. Integration of transcriptomic analysis, metabolic profiling, and a genome-scale metabolic model (GEM) facilitated the discovery of the potential mechanism of microbial interactions. Multi-omics analysis revealed that the vitamin B12-dependent methionine-folate cycle could be a key pathway for enhancing the hyperosmotic stress tolerance of synergistic consortium. Further GEM simulations revealed interspecies exchange of S-adenosyl-L-methionine and riboflavin, cofactors needed for vitamin B12 biosynthesis, which was confirmed by in vitro experiments. Overall, we proposed a new mechanism of bacterial hyperosmotic stress tolerance: bacteria might promote the production of vitamin B12 to enhance biofilm formation, and the species collaborate with each other by exchanging cofactors to improve consortium hyperosmotic stress tolerance. These findings offer new insights into the role of cofactors in microbial interactions and stress tolerance and are potentially exploitable for environmental remediation.ImportanceMetabolic interactions (also known as cross-feeding) are thought to be ubiquitous in microbial communities. Cross-feeding is the basis for many positive interactions (e.g., mutualism) and is a primary driver of microbial community assembly. In this study, a combination of multi-omics analysis and metabolic modeling simulation was used to reveal the metabolic interactions of a synthetic consortium under hyperosmotic stress. Interspecies cofactor exchange was found to promote biofilm formation under hyperosmotic stress. This provides a new perspective for understanding the role of metabolic interactions in microbial communities to enhance environmental adaptation, which is significant for improving the efficiency of production activities and environmental bioremediation.

Project description:Biotic interactions are crucial for determining the structure and dynamics of communities; however, direct measurement of these interactions can be challenging in terms of time and resources, especially when numerous species are involved. Inferring species interactions from species co-occurrence patterns is increasingly being used; however, recent studies have highlighted some limitations. To our knowledge, no attempt has been made to test the accuracy of the existing methods for detecting mutualistic interactions in terrestrial ecosystems. In this study, we compiled two literature-based, long-term datasets of interactions between butterflies and herbaceous plant species in two regions of Germany and compared them with observational abundance and presence/absence data collected within a year in the same regions. We tested how well the species associations generated by three different co-occurrence analysis methods matched those of empirically measured mutualistic associations using sensitivity and specificity analyses and compared the strength of associations. We also checked whether flower abundance data (instead of plant abundance data) increased the accuracy of the co-occurrence models and validated our results using empirical flower visitation data. The results revealed that, although all methods exhibited low sensitivity, our implementation of the Relative Interaction Intensity index with pairwise null models performed the best, followed by the probabilistic method and Spearman's rank correlation method. However, empirical data showed a significant number of interactions that were not detected using co-occurrence methods. Incorporating flower abundance data did not improve sensitivity but enhanced specificity in one region. Further analysis demonstrated incongruence between the predicted co-occurrence associations and actual interaction strengths, with many pairs exhibiting high interaction strength but low co-occurrence or vice versa. These findings underscore the complexity of ecological dynamics and highlight the limitations of current co-occurrence methods for accurately capturing species interactions.

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Synergistic epistasis enhances the co-operativity of mutualistic interspecies interactions.

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Synergistic epistasis enhances the co-operativity of mutualistic interspecies interactions.

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