Long-term phenotypic evolution of bacteria

Abstract

For many decades comparative analyses of protein sequences and structures have been used to investigate fundamental principles of molecular evolution. In contrast, relatively little is known about the long-term evolution of species' phenotypic and genetic properties. This represents an important gap in our understanding of evolution, as exactly these proprieties play key roles in natural selection and adaptation to diverse environments. Here we perform a comparative analysis of bacterial growth and gene deletion phenotypes using hundreds of genome-scale metabolic models. Overall, bacterial phenotypic evolution can be described by a two-stage process with a rapid initial phenotypic diversification followed by a slow long-term exponential divergence. The observed average divergence trend, with approximately similar fractions of phenotypic properties changing per unit time, continues for billions of years. We experimentally confirm the predicted divergence trend using the phenotypic profiles of 40 diverse bacterial species across more than 60 growth conditions. Our analysis suggests that, at long evolutionary distances, gene essentiality is significantly more conserved than the ability to utilize different nutrients, while synthetic lethality is significantly less conserved. We also find that although a rapid phenotypic evolution is sometimes observed within the same species, a transition from high to low phenotypic similarity occurs primarily at the genus level.

The adaptive acquisition of single DNA segments drives metabolic evolution acrossE. colilineages

“…http://dx.doi.org/10.1101/148460 doi: bioRxiv preprint first posted online Jun. 10, 2017; increase with evolutionary distance 2 . The lack of phenotypic divergence within E. coli may be linked to our observation that even for the most diverged genomes, there is still a 99% chance that a given phenotype of one strain can be transferred to the other with a single DNA segment.…”

“…The answer likely lies in frequent recombination between bacterial strains belonging to the same species, a process that facilitates the transfer of genes (horizontal gene transfer, HGT) 8 . This process effectively decouples phenotypic divergence, dominated by HGT of metabolic pathways 2 , from genome sequence divergence, dominated by mutations accumulating along lines of vertical inheritance. Thus, the E. coli pan-genome acts like a repository from which individual strains can add metabolic tools to their existing toolboxes 9,10 , a process independent from vertical inheritance.…”

“…Experimental growth data indicates that genetic distance, based on multilocus sequence typing data, is a weak indicator of how similar two E. coli strains are in terms of the carbon sources they can metabolize 1 . Similarly, a computational analysis of automatically generated metabolic models for hundreds of species suggested that withinspecies phenotypic divergence is almost instantaneous, while divergence between genera is gradual or "clock-like" 2 . How can within-species divergence be so much faster than betweenspecies divergence?…”

“…However, it is the phenotype that natural selection acts upon; to fully appreciate the patterns and driving forces of adaptation, we need to link genotypes to phenotypes both on the genomic scale and on an evolutionary timescale. Bacterial metabolism is arguably the most promising model system for such an endeavour: the ability to metabolize different nutrient sources always remains an essential determinant of bacterial fitness 2 , and flux balance analysis (FBA) has been established as a robust and reliable modeling framework for the prediction of this ability 7 . Experimental growth data indicates that genetic distance, based on multilocus sequence typing data, is a weak indicator of how similar two E. coli strains are in terms of the carbon sources they can metabolize 1 .…”

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AbstractEven closely related prokaryotes show an astounding diversity in their ability to grow in different nutritional environments 1,2 ; more fundamentally, it is unknown what fraction of metabolic adaptations are indeed complex. Here, we use metabolic network simulations to show that all 3,363 phenotypic innovations observed in the evolutionary history of 53 E. coli strains arose through the acquisition of a single DNA segment; while we found no evidence for the contribution of selectively neutral processes, 10.6% of adaptations to previously unviable environments relied on the support of DNA acquisitions on earlier phylogenetic branches.

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