Abstract
Bacteria frequently lose biosynthetic genes, thus making them dependent on an environmental uptake of the corresponding metabolite. Despite the ubiquity of this ‘genome streamlining’, it is generally unclear whether the concomitant loss of biosynthetic functions is favored by natural selection or rather caused by random genetic drift. Here we demonstrate experimentally that a loss of metabolic functions is strongly selected for when the corresponding metabolites can be derived from the environment. Serially propagating replicate populations of the bacterium Escherichia coli in amino acid-containing environments revealed that auxotrophic genotypes rapidly evolved in less than 2,000 generations in almost all replicate populations. Moreover, auxotrophs also evolved in environments lacking amino acids–yet to a much lesser extent. Loss of these biosynthetic functions was due to mutations in both structural and regulatory genes. In competition experiments performed in the presence of amino acids, auxotrophic mutants gained a significant fitness advantage over the evolutionary ancestor, suggesting their emergence was selectively favored. Interestingly, auxotrophic mutants derived amino acids not only via an environmental uptake, but also by cross-feeding from coexisting strains. Our results show that adaptive fitness benefits can favor biosynthetic loss-of-function mutants and drive the establishment of intricate metabolic interactions within microbial communities.
Highlights
Bacterial genomes are highly dynamic in terms of both size and composition [1]
We discovered that populations of Escherichia coli that evolved in amino acid-replete environments rapidly lost the ability to autonomously produce several amino acids, which was beneficial when amino acids were present in the environment
Our findings show that nutrient-containing environments drive the loss of biosynthetic genes from bacterial genomes and facilitate the establishment of metabolic cross-feeding interactions among bacteria
Summary
Bacterial genomes are highly dynamic in terms of both size and composition [1]. The extensive variation in gene repertoires that characterizes prokaryotic genomes can be caused by genome expansion via horizontal gene transfer and gene duplication or, alternatively, contraction due to gene loss. Comparative analyses have provided evidence that gene loss may be quantitatively more important for determining the size of prokaryotic genomes than the gain of new genetic information [1,2,3]. Analyzing the genetic content of these reduced genomes revealed—besides a lack of dispensable elements [6]— the elimination of seemingly essential biosynthetic functions. Reconstructing metabolic networks from sequence data to predict the phenotype of the focal organism unraveled that the majority of bacterial genomes analyzed lacked the biosynthetic capability to produce several essential building block metabolites such as amino acids, vitamins, or even nucleobases [7,8,9,10]. The ubiquity of biosynthetic loss-of-function mutations in bacteria that inhabit ecologically disparate environments begs an explanation: Which evolutionary mechanisms have favored a loss of biosynthetic genes over metabolic autonomy in these bacteria?
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