Adapting the engine to the fuel: mutator populations can reduce the mutational load by reorganizing their genome structure
Abstract Background Mutators are common in bacterial populations, both in natural isolates and in the lab. The fate of these lineages, which mutation rate is increased up to 100 ×, has long been studied using population genetics models, showing that they can spread in a population following an envir...
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| Format: | Article |
| Language: | English |
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BMC
2019-10-01
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| Series: | BMC Evolutionary Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12862-019-1507-z |
| _version_ | 1818729120233684992 |
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| author | Jacob Pieter Rutten Paulien Hogeweg Guillaume Beslon |
| author_facet | Jacob Pieter Rutten Paulien Hogeweg Guillaume Beslon |
| author_sort | Jacob Pieter Rutten |
| collection | DOAJ |
| description | Abstract Background Mutators are common in bacterial populations, both in natural isolates and in the lab. The fate of these lineages, which mutation rate is increased up to 100 ×, has long been studied using population genetics models, showing that they can spread in a population following an environmental change. However in stable conditions, they suffer from the increased mutational load, hence being overcome by non-mutators. However, these results don’t take into account the fact that an elevated mutation rate can impact the genetic structure, hence changing the sensitivity of the population to mutations. Here we used Aevol, an in silico experimental evolution platform in which genomic structures are free to evolve, in order to study the fate of mutator populations evolving for a long time in constant conditions. Results Starting from wild-types that were pre-evolved for 300,000 generations, we let 100 mutator populations (point mutation rate ×100) evolve for 100,000 further generations in constant conditions. As expected all populations initially undergo a fitness loss. However, after that the mutator populations started to recover. Most populations ultimately recovered their ancestors fitness, and a significant fraction became even fitter than the non-mutator control clones that evolved in parallel. By analyzing the genomes of the mutators, we show that the fitness recovery is due to two mechanisms: i. an increase in robustness through compaction of the coding part of the mutator genomes, ii. an increase of the selection coefficient that decreases the mean-fitness of the population. Strikingly the latter is due to the accumulation of non-coding sequences in the mutators genomes. Conclusion Our results show that the mutational burden that is classically thought to be associated with mutator phenotype is escapable. On the long run mutators adapted their genomes and reshaped the distribution of mutation effects. Therewith the lineage is able to recover fitness even though the population still suffers the elevated mutation rate. Overall these results change our view of mutator dynamics: by being able to reduce the deleterious effect of the elevated mutation rate, mutator populations may be able to last for a very long time; A situation commonly observed in nature. |
| first_indexed | 2024-12-17T22:40:50Z |
| format | Article |
| id | doaj.art-95d484f06c1d4eb9b307dc86f8ebf21b |
| institution | Directory Open Access Journal |
| issn | 1471-2148 |
| language | English |
| last_indexed | 2024-12-17T22:40:50Z |
| publishDate | 2019-10-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Evolutionary Biology |
| spelling | doaj.art-95d484f06c1d4eb9b307dc86f8ebf21b2022-12-21T21:29:58ZengBMCBMC Evolutionary Biology1471-21482019-10-0119111710.1186/s12862-019-1507-zAdapting the engine to the fuel: mutator populations can reduce the mutational load by reorganizing their genome structureJacob Pieter Rutten0Paulien Hogeweg1Guillaume Beslon2Theoretical Biology and Bioinformatics group,Utrecht UniversityTheoretical Biology and Bioinformatics group,Utrecht UniversityUniversité de Lyon, INRIA, CNRS, INSA-Lyon, Beagle Team, LIRIS, UMR5205Abstract Background Mutators are common in bacterial populations, both in natural isolates and in the lab. The fate of these lineages, which mutation rate is increased up to 100 ×, has long been studied using population genetics models, showing that they can spread in a population following an environmental change. However in stable conditions, they suffer from the increased mutational load, hence being overcome by non-mutators. However, these results don’t take into account the fact that an elevated mutation rate can impact the genetic structure, hence changing the sensitivity of the population to mutations. Here we used Aevol, an in silico experimental evolution platform in which genomic structures are free to evolve, in order to study the fate of mutator populations evolving for a long time in constant conditions. Results Starting from wild-types that were pre-evolved for 300,000 generations, we let 100 mutator populations (point mutation rate ×100) evolve for 100,000 further generations in constant conditions. As expected all populations initially undergo a fitness loss. However, after that the mutator populations started to recover. Most populations ultimately recovered their ancestors fitness, and a significant fraction became even fitter than the non-mutator control clones that evolved in parallel. By analyzing the genomes of the mutators, we show that the fitness recovery is due to two mechanisms: i. an increase in robustness through compaction of the coding part of the mutator genomes, ii. an increase of the selection coefficient that decreases the mean-fitness of the population. Strikingly the latter is due to the accumulation of non-coding sequences in the mutators genomes. Conclusion Our results show that the mutational burden that is classically thought to be associated with mutator phenotype is escapable. On the long run mutators adapted their genomes and reshaped the distribution of mutation effects. Therewith the lineage is able to recover fitness even though the population still suffers the elevated mutation rate. Overall these results change our view of mutator dynamics: by being able to reduce the deleterious effect of the elevated mutation rate, mutator populations may be able to last for a very long time; A situation commonly observed in nature.http://link.springer.com/article/10.1186/s12862-019-1507-zBacteriaMutatorsRobustnessGenome structurein silico Experimental evolution |
| spellingShingle | Jacob Pieter Rutten Paulien Hogeweg Guillaume Beslon Adapting the engine to the fuel: mutator populations can reduce the mutational load by reorganizing their genome structure BMC Evolutionary Biology Bacteria Mutators Robustness Genome structure in silico Experimental evolution |
| title | Adapting the engine to the fuel: mutator populations can reduce the mutational load by reorganizing their genome structure |
| title_full | Adapting the engine to the fuel: mutator populations can reduce the mutational load by reorganizing their genome structure |
| title_fullStr | Adapting the engine to the fuel: mutator populations can reduce the mutational load by reorganizing their genome structure |
| title_full_unstemmed | Adapting the engine to the fuel: mutator populations can reduce the mutational load by reorganizing their genome structure |
| title_short | Adapting the engine to the fuel: mutator populations can reduce the mutational load by reorganizing their genome structure |
| title_sort | adapting the engine to the fuel mutator populations can reduce the mutational load by reorganizing their genome structure |
| topic | Bacteria Mutators Robustness Genome structure in silico Experimental evolution |
| url | http://link.springer.com/article/10.1186/s12862-019-1507-z |
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