Macarena Toll Riera

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Toll Riera

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Macarena

ORCID

0000-0003-0978-3139

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Publications 1 - 10 of 10

The Genomic Basis of Evolutionary Innovation in Pseudomonas aeruginosa
Toll Riera, Macarena; San Millan, Alvaro; Wagner, Andreas; et al. (2016)
PLoS Genetics
Novel traits play a key role in evolution, but their origins remain poorly understood. Here we address this problem by using experimental evolution to study bacterial innovation in real time. We allowed 380 populations of Pseudomonas aeruginosa to adapt to 95 different carbon sources that challenged bacteria with either evolving novel metabolic traits or optimizing existing traits. Whole genome sequencing of more than 80 clones revealed profound differences in the genetic basis of innovation and optimization. Innovation was associated with the rapid acquisition of mutations in genes involved in transcription and metabolism. Mutations in pre-existing duplicate genes in the P. aeruginosa genome were common during innovation, but not optimization. These duplicate genes may have been acquired by P. aeruginosa due to either spontaneous gene amplification or horizontal gene transfer. High throughput phenotype assays revealed that novelty was associated with increased pleiotropic costs that are likely to constrain innovation. However, mutations in duplicate genes with close homologs in the P. aeruginosa genome were associated with low pleiotropic costs compared to mutations in duplicate genes with distant homologs in the P. aeruginosa genome, suggesting that functional redundancy between duplicates facilitates innovation by buffering pleiotropic costs.
Hypermutation and Fluctuating Stress Levels Can Enable Evolutionary Rescue
Ebert, Gleb G.; Toll Riera, Macarena (2025)
ESEB 2025 Abstract Book
When an environmental change leads to a decline in population size, selection on standing or de novo genetic variation can lead to recovery of the population. This process is called evolutionary rescue and is an important mechanism preventing populations from going extinct due to abiotic stressors such as temperature. In an earlier evolution we explored the evolvability of the upper thermal limit in Pseudoalteromonas haloplanktis TAC125, a cold-adapted strain of a globally distributed marine bacterium, by slowly increasing the cultivation temperature over the course of 900 generations. While we succeeded in extending the upper thermal limit by one degree to 30°C, the experiment revealed a constrained evolutionary potential of the upper thermal limit. We hypothesised that increasing the mutational supply might lead to this hard limit being surpassed. In this follow up evolution experiment we picked evolved clones from the previous experiment with and without a hypermutator phenotype and subjected them to regularly fluctuating levels of heat stress (2.5°C apart). By gradually increasing the temperatures over 840 additional generations, we were able to reach 32°C, at which point further adaptation stalled. Every time the temperatures were increased, the evolving populations declined in optical density but slowly recovered with time, indicating repeating waves of evolutionary rescue. Furthermore, populations descending from hypermutator clones showed higher optical densities throughout the course of adaptation to increasing temperatures compared to populations descending from nonmutator clones. While over half of the hypermutator populations acquired additional mutations in genes affecting the mutation rate, only one nonmutator population evolved a hypermutator phenotype. Hypermutator populations on average accumulated 8x more mutations than nonmutator populations. Interestingly, hypermutator populations experienced 14x more mutations rising to fixation than nonmutator populations. Furthermore, we observe parallel genome evolution with genes encoding for membrane-associated proteins in particular showing the exact same mutations in up to a third of all populations. Our experiment exemplifies how a number of evolutionary processes can interact to increase the success of adaptation, a particularly relevant finding in our rapidly changing world.
Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids
San Millan, Alvaro; Peña-Miller, Rafael; Toll Riera, Macarena; et al. (2014)
Nature Communications
Plasmids are important drivers of bacterial evolution, but it is challenging to understand how plasmids persist over the long term because plasmid carriage is costly. Classical models predict that horizontal transfer is necessary for plasmid persistence, but recent work shows that almost half of plasmids are non-transmissible. Here we use a combination of mathematical modelling and experimental evolution to investigate how a costly, non-transmissible plasmid, pNUK73, can be maintained in populations of Pseudomonas aeruginosa. Compensatory adaptation increases plasmid stability by eliminating the cost of plasmid carriage. However, positive selection for plasmid-encoded antibiotic resistance is required to maintain the plasmid by offsetting reductions in plasmid frequency due to segregational loss. Crucially, we show that compensatory adaptation and positive selection reinforce each other’s effects. Our study provides a new understanding of how plasmids persist in bacterial populations, and it helps to explain why resistance can be maintained after antibiotic use is stopped.
Integrative analysis of fitness and metabolic effects of plasmids in Pseudomonas aeruginosa PAO1
San Millan, Alvaro; Toll Riera, Macarena; Qi, Qin; et al. (2018)
The ISME Journal
Horizontal gene transfer (HGT) mediated by the spread of plasmids fuels evolution in prokaryotes. Although plasmids provide bacteria with new adaptive genes, they also produce physiological alterations that often translate into a reduction in bacterial fitness. The fitness costs associated with plasmids represent an important limit to plasmid maintenance in bacterial communities, but their molecular origins remain largely unknown. In this work, we combine phenomics, transcriptomics and metabolomics to study the fitness effects produced by a collection of diverse plasmids in the opportunistic pathogen Pseudomonas aeruginosa PAO1. Using this approach, we scan the physiological changes imposed by plasmids and test the generality of some main mechanisms that have been proposed to explain the cost of HGT, including increased biosynthetic burden, reduced translational efficiency, and impaired chromosomal replication. Our results suggest that the fitness effects of plasmids have a complex origin, since none of these mechanisms could individually provide a general explanation for the cost of plasmid carriage. Interestingly, our results also showed that plasmids alter the expression of a common set of metabolic genes in PAO1, and produce convergent changes in host cell metabolism. These surprising results suggest that there is a common metabolic response to plasmids in P. aeruginosa PAO1.
Genetic dominance governs the evolution and spread of mobile genetic elements in bacteria
Rodríguez-Beltrán, Jerónimo; Sørum, Vidar; Toll Riera, Macarena; et al. (2020)
Proceedings of the National Academy of Sciences of the United States of America
Mobile genetic elements (MGEs), such as plasmids, promote bacterial evolution through horizontal gene transfer (HGT). However, the rules governing the repertoire of traits encoded on MGEs remain unclear. In this study, we uncovered the central role of genetic dominance shaping genetic cargo in MGEs, using antibiotic resistance as a model system. MGEs are typically present in more than one copy per host bacterium, and as a consequence, genetic dominance favors the fixation of dominant mutations over recessive ones. In addition, genetic dominance also determines the phenotypic effects of horizontally acquired MGE-encoded genes, silencing recessive alleles if the recipient bacterium already carries a wild-type copy of the gene. The combination of these two effects governs the catalog of genes encoded on MGEs. Our results help to understand how MGEs evolve and spread, uncovering the neglected influence of genetic dominance on bacterial evolution. Moreover, our findings offer a framework to forecast the spread and evolvability of MGE-encoded genes, which encode traits of key human interest, such as virulence or antibiotic resistance.
New insights on Pseudoalteromonas haloplanktis TAC125 genome organization and benchmarks of genome assembly applications using next and third generation sequencing technologies
Qi, Weihong; Colarusso, Andrea; Olombrada, Miriam; et al. (2019)
Scientific Reports
Pseudoalteromonas haloplanktis TAC125 is among the most commonly studied bacteria adapted to cold environments. Aside from its ecological relevance, P. haloplanktis has a potential use for biotechnological applications. Due to its importance, we decided to take advantage of next generation sequencing (Illumina) and third generation sequencing (PacBio and Oxford Nanopore) technologies to resequence its genome. The availability of a reference genome, obtained using whole genome shotgun sequencing, allowed us to study and compare the results obtained by the different technologies and draw useful conclusions for future de novo genome assembly projects. We found that assembly polishing using Illumina reads is needed to achieve a consensus accuracy over 99.9% when using Oxford Nanopore sequencing, but not in PacBio sequencing. However, the dependency of consensus accuracy on coverage is lower in Oxford Nanopore than in PacBio, suggesting that a cost-effective solution might be the use of low coverage Oxford Nanopore sequencing together with Illumina reads. Despite the differences in consensus accuracy, all sequencing technologies revealed the presence of a large plasmid, pMEGA, which was undiscovered until now. Among the most interesting features of pMEGA is the presence of a putative error-prone polymerase regulated through the SOS response. Aside from the characterization of the newly discovered plasmid, we confirmed the sequence of the small plasmid pMtBL and uncovered the presence of a potential partitioning system. Crucially, this study shows that the combination of next and third generation sequencing technologies give us an unprecedented opportunity to characterize our bacterial model organisms at a very detailed level.
Staphylococcal phages and pathogenicity islands drive plasmid evolution
Humphrey, Suzanne; San Millán, Álvaro; Toll Riera, Macarena; et al. (2021)
Nature Communications
Conjugation has classically been considered the main mechanism driving plasmid transfer in nature. Yet bacteria frequently carry so-called non-transmissible plasmids, raising questions about how these plasmids spread. Interestingly, the size of many mobilisable and non-transmissible plasmids coincides with the average size of phages (~40 kb) or that of a family of pathogenicity islands, the phage-inducible chromosomal islands (PICIs, ~11 kb). Here, we show that phages and PICIs from Staphylococcus aureus can mediate intra- and inter-species plasmid transfer via generalised transduction, potentially contributing to non-transmissible plasmid spread in nature. Further, staphylococcal PICIs enhance plasmid packaging efficiency, and phages and PICIs exert selective pressures on plasmids via the physical capacity of their capsids, explaining the bimodal size distribution observed for non-conjugative plasmids. Our results highlight that transducing agents (phages, PICIs) have important roles in bacterial plasmid evolution and, potentially, in antimicrobial resistance transmission.
The genomic basis of adaptation to the fitness cost of rifampicin resistance in Pseudomonas aeruginosa
Qi, Qin; Toll Riera, Macarena; Heilbron, Karl; et al. (2016)
Proceedings of the Royal Society B: Biological Sciences
Antibiotic resistance carries a fitness cost that must be overcome in order for resistance to persist over the long term. Compensatory mutations that recover the functional defects associated with resistance mutations have been argued to play a key role in overcoming the cost of resistance, but compensatory mutations are expected to be rare relative to generally beneficial mutations that increase fitness, irrespective of antibiotic resistance. Given this asymmetry, population genetics theory predicts that populations should adapt by compensatory mutations when the cost of resistance is large, whereas generally beneficial mutations should drive adaptation when the cost of resistance is small. We tested this prediction by determining the genomic mechanisms underpinning adaptation to antibiotic-free conditions in populations of the pathogenic bacterium Pseudomonas aeruginosa that carry costly antibiotic resistance mutations. Whole-genome sequencing revealed that populations founded by high-cost rifampicin-resistant mutants adapted via compensatory mutations in three genes of the RNA polymerase core enzyme, whereas populations founded by low-cost mutants adapted by generally beneficial mutations, predominantly in the quorum-sensing transcriptional regulator gene lasR. Even though the importance of compensatory evolution in maintaining resistance has been widely recognized, our study shows that the roles of general adaptation in maintaining resistance should not be underestimated and highlights the need to understand how selection at other sites in the genome influences the dynamics of resistance alleles in clinical settings.
A limit on the evolutionary rescue of an Antarctic bacterium from rising temperatures
Toll Riera, Macarena; Olombrada, Miriam; Castro-Giner, Francesc; et al. (2022)
Science Advances
Climate change is gradual, but it can also cause brief extreme heat waves that can exceed the upper thermal limit of any one organism. To study the evolutionary potential of upper thermal tolerance, we evolved the cold-adapted Antarctic bacterium Pseudoalteromonas haloplanktis to survive at 30°C, beyond its ancestral thermal limit. This high-temperature adaptation occurred rapidly and in multiple populations. It involved genomic changes that occurred in a highly parallel fashion and mitigated the effects of protein misfolding. However, it also confronted a physiological limit, because populations failed to grow beyond 30°C. Our experiments aimed to facilitate evolutionary rescue by using a small organism with large populations living at temperatures several degrees below their upper thermal limit. Larger organisms with smaller populations and living at temperatures closer to their upper thermal tolerances are even more likely to go extinct during extreme heat waves.
Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa
San Millan, Alvaro; Toll Riera, Macarena; Qi, Qin; et al. (2015)
Nature Communications
Horizontal gene transfer (HGT) plays a key role in bacterial evolution, especially with respect to antibiotic resistance. Fitness costs associated with mobile genetic elements (MGEs) are thought to constrain HGT, but our understanding of these costs remains fragmentary, making it difficult to predict the success of HGT events. Here we use the interaction between P. aeruginosa and a costly plasmid (pNUK73) to investigate the molecular basis of the cost of HGT. Using RNA-Seq, we show that the acquisition of pNUK73 results in a profound alteration of the transcriptional profile of chromosomal genes. Mutations that inactivate two genes encoded on chromosomally integrated MGEs recover these fitness costs and transcriptional changes by decreasing the expression of the pNUK73 replication gene. Our study demonstrates that interactions between MGEs can compromise bacterial fitness via altered gene expression, and we argue that conflicts between mobile elements impose a general constraint on evolution by HGT.

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Macarena Toll Riera

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