A limit on the evolutionary rescue of an Antarctic bacterium from rising temperatures

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

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

Staphylococcal phages and pathogenicity islands drive plasmid evolution

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

Structure and Age Jointly Influence Rates of Protein Evolution

What factors determine a protein's rate of evolution are actively debated. Especially unclear is the relative role of intrinsic factors of present-day proteins versus historical factors such as protein age. Here we study the interplay of structural properties and evolutionary age, as determinants of protein evolutionary rate. We use a large set of one-to-one orthologs between human and mouse proteins, with mapped PDB structures. We report that previously observed structural correlations also hold within each age group – including relationships between solvent accessibility, designabililty, and evolutionary rates. However, age also plays a crucial role: age modulates the relationship between solvent accessibility and rate. Additionally, younger proteins, despite being less designable, tend to evolve faster than older proteins. We show that previously reported relationships between age and rate cannot be explained by structural biases among age groups. Finally, we introduce a knowledge-based potential function to study the stability of proteins through large-scale computation. We find that older proteins are more stable for their native structure, and more robust to mutations, than younger ones. Our results underscore that several determinants, both intrinsic and historical, can interact to determine rates of protein evolution

Mechanisms of evolutionary innovation in mammalian genes

Actualment, degut a la disponibilitat d’un gran nombre de genomes seqüenciats, el camp de la genòmica comparativa està experimentant grans avenços. Ara són possibles una àmplia gama d’estudis que fins fa poc eren inimaginables. En aquesta tesi hem volgut estudiar les innovacions evolutives en els genomes de mamífers. Hem escollit centrar l’estudi en mamífers degut a que els seus genomes tenen bona qualitat i hi ha més informació disponible, a més el fet d’incloure l’espècie humana afegeix interès. Ens hem centrat en tres qüestions interessants en el camp de l’evolució. Primer hem volgut determinar quina és la fracció de gens ortòlegs de mamífers que presenten desviacions específiques de llinatge en les tasses evolutives. Hem obtingut que al voltant del 25% dels gens tenen evidencies d’haver estat sotmesos a acceleracions i deceleracions específiques de branca. Hem trobat que sorprenentment, els gens accelerats normalment no solapen amb els gens amb evidencia de selecció positiva, demostrant que els tests emprats per detectar selecció positiva són massa conservadors. En segon lloc, hem aprofundit en quins són els determinants de l’evolució proteica, centrant-nos en l’edat d’origen i en les característiques estructurals. Per estudiar-ho hem utilitzat tant dominis com estructures proteiques i principalment hem trobat que l’edat d’origen és un dels determinants més importants. Finalment, hem investigat les característiques i els mecanismes d’origen d’un grup de gens molt joves: els gens específics de primats. Hem trobat que els gens específics de primats evolucionen ràpid, són curts i específics de teixit. Pel que fa al seu mecanisme d’origen, al voltant d’un 53% dels gens presenten evidencies d’haver-se originat a través de l’exaptació de transposons, 24% a partir de duplicacions parcials o totals i sorprenentment, 5.5% de novo a partir de regions no codificants de mamífers.With the availability of a high number of sequenced genomes the comparative genomics field has experienced a great advance. A wide range of studies that some years ago were unconceivable are now possible. In this thesis we aimed to study evolutionary innovations in mammalian genomes. We chose to centre our studies in mammalian species because at that moment were the genomes with higher quality and also more additional information was available for them, and of course, the inclusion of human species added a point of interest. We wished to give insights into three exciting questions in the field of evolution. First we wanted to assess which is the fraction of mammalian orthologous genes that present lineage-specific deviations in the rate of evolution. We obtained that around 25% of the genes had evidence of accelerations and decelerations specific of a branch and, surprisingly, accelerated cases did not usually overlap with cases of genes experiencing positive selection, showing that tests to detect positive selection are excessively conservative. Secondly, we wanted to deepen into the determinants driving protein evolution, centering on age of origin and structural characteristics. We used protein domains and structures to study them and we mainly found that age of origin seems to be one of the most important determinants. And finally, we investigated the characteristics and mechanisms of origin of a group of very young genes: primate-specific genes. We report that primate-specific genes evolve fast, are short and highly tissue specific. Regarding their mechanism of origin, about 53% of them showed evidence of transposable elements exaptation, 24% of partial or total duplication and surprisingly 5.5% of de novo origination from mammalian noncoding regions

Emergence of novel domains in proteins

Proteins are composed of a combination of discrete, well-defined, sequence domains, associated with specific functions that have arisen at different times during evolutionary history. The emergence of novel domains is related to protein functional diversification and adaptation. But currently little is known about how novel domains arise and how they subsequently evolve. To gain insights into the impact of recently emerged domains in protein evolution we have identified all human young protein domains that have emerged in approximately the past 550 million years. We have classified them into vertebrate-specific and mammalian-specific groups, and compared them to older domains. We have found 426 different annotated young domains, totalling 995 domain occurrences, which represent about 12.3% of all human domains. We have observed that 61.3% of them arose in newly formed genes, while the remaining 38.7% are found combined with older domains, and have very likely emerged in the context of a previously existing protein. Young domains are preferentially located at the N-terminus of the protein, indicating that, at least in vertebrates, novel functional sequences often emerge there. Furthermore, young domains show significantly higher non-synonymous to synonymous substitution rates than older domains using human and mouse orthologous sequence comparisons. This is also true when we compare young and old domains located in the same protein, suggesting that recently arisen domains tend to evolve in a less constrained manner than older domains. We conclude that proteins tend to gain domains over time, becoming progressively longer. We show that many proteins are made of domains of different age, and that the fastest evolving parts correspond to the domains that have been acquired more recently.We received financial support from Ministerio de Educación (FPU to M.T.-R.), Ministerio de Innovación y Tecnología grant BIO2009-08160, Ministerio de Economía y Competitividad grant BFU2012-36820, and Institució Catalana de Recerca i Estudis Avançats (ICREA contract to M.M.A.)

Emergence of novel domains in proteins

Proteins are composed of a combination of discrete, well-defined, sequence domains, associated with specific functions that have arisen at different times during evolutionary history. The emergence of novel domains is related to protein functional diversification and adaptation. But currently little is known about how novel domains arise and how they subsequently evolve. To gain insights into the impact of recently emerged domains in protein evolution we have identified all human young protein domains that have emerged in approximately the past 550 million years. We have classified them into vertebrate-specific and mammalian-specific groups, and compared them to older domains. We have found 426 different annotated young domains, totalling 995 domain occurrences, which represent about 12.3% of all human domains. We have observed that 61.3% of them arose in newly formed genes, while the remaining 38.7% are found combined with older domains, and have very likely emerged in the context of a previously existing protein. Young domains are preferentially located at the N-terminus of the protein, indicating that, at least in vertebrates, novel functional sequences often emerge there. Furthermore, young domains show significantly higher non-synonymous to synonymous substitution rates than older domains using human and mouse orthologous sequence comparisons. This is also true when we compare young and old domains located in the same protein, suggesting that recently arisen domains tend to evolve in a less constrained manner than older domains. We conclude that proteins tend to gain domains over time, becoming progressively longer. We show that many proteins are made of domains of different age, and that the fastest evolving parts correspond to the domains that have been acquired more recently.We received financial support from Ministerio de Educación (FPU to M.T.-R.), Ministerio de Innovación y Tecnología grant BIO2009-08160, Ministerio de Economía y Competitividad grant BFU2012-36820, and Institució Catalana de Recerca i Estudis Avançats (ICREA contract to M.M.A.)