LESS IS MORE: SELECTIVE ADVANTAGES CAN EXPLAIN THE PREVALENT LOSS OF BIOSYNTHETIC GENES IN BACTERIA

Bacteria that have adapted to nutrient-rich, stable environments are typically characterized by reduced genomes. The loss of biosynthetic genes frequently renders these lineages auxotroph, hinging their survival on an environmental uptake of certain metabolites. The evolutionary forces that drive th...

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Bibliographic Details
Published in:Evolution 2014-09, Vol.68 (9), p.2559-2570
Main Authors: D'Souza, Glen, Waschina, Silvio, Pande, Samay, Bohl, Katrin, Kaleta, Christoph, Kost, Christian
Format: Article
Language:English
Subjects:
Acinetobacter
Acinetobacter - genetics
Acinetobacter - metabolism
Adaptive gene loss
Amino acid metabolism
Amino acids
auxotrophy
Bacteria
Bacteria - genetics
Bacteria - metabolism
Biochemical pathways
Biosynthesis
Biosynthetic Pathways - genetics
black queen hypothesis
cross-feeding
Ecological competition
Escherichia coli
Escherichia coli - genetics
Escherichia coli - metabolism
Evolution
Genes
Genes, Bacterial - genetics
Genes, Essential
Genomes
Metabolic Networks and Pathways - genetics
Metabolites
Mutation
prototrophy
symbiosis
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Summary:Bacteria that have adapted to nutrient-rich, stable environments are typically characterized by reduced genomes. The loss of biosynthetic genes frequently renders these lineages auxotroph, hinging their survival on an environmental uptake of certain metabolites. The evolutionary forces that drive this genome degradation, however, remain elusive. Our analysis of 949 metabolic networks revealed auxotrophies are likely highly prevalent in both symbiotic and free-living bacteria. To unravel whether selective advantages can account for the rampant loss of anabolic genes, we systematically determined the fitness consequences that result from deleting conditionally essential biosynthetic genes from the genomes of Escherichia coli and Acinetobacter baylyi in the presence of the focal nutrient. Pairwise competition experiments with each of 20 mutants auxotrophic for different amino acids, vitamins, and nucleobases against the prototrophic wild type unveiled a pronounced, concentration-dependent growth advantage of around 13% for virtually all mutants tested. Individually deleting different genes from the same biosynthesis pathway entailed gene-specific fitness consequences and loss of the same biosynthetic genes from the genomes of E. coli and A. baylyi differentially affected the fitness of the resulting auxotrophic mutants. Taken together, our findings suggest adaptive benefits could drive the loss of conditionally essential biosynthetic genes.
ISSN:0014-3820
1558-5646
DOI:10.1111/evo.12468