Social evolution of toxic metal bioremediation in Pseudomonas aeruginosa

This is the final version. Available on open access from the Royal Society via the DOI in this recordThere is another ORE record for this publication: http://hdl.handle.net/10871/16448Bacteria are often iron-limited, and hence produce extracellular iron-scavenging siderophores. A crucial feature of siderophore production is that it can be an altruistic behaviour (individually costly but benefitting neighbouring cells), thus siderophore producers can be invaded by non-producing social 'cheats'. Recent studies have shown that siderophores can also bind other heavy metals (such as Cu and Zn), but in this case siderophore chelation actually reduces metal uptake by bacteria. These complexes reduce heavy metal toxicity, hence siderophore production may contribute to toxic metal bioremediation. Here, we show that siderophore production in the context of bioremediation is also an altruistic trait and can be exploited by cheating phenotypes in the opportunistic pathogen Pseudomonas aeruginosa. Specifically, we show that in toxic copper concentrations (i) siderophore non-producers evolve de novo and reach high frequencies, and (ii) producing strains are fitter than isogenic non-producing strains in monoculture, and vice versa in co-culture. Moreover, we show that the evolutionary effect copper has on reducing siderophore production is greater than the reduction observed under iron-limited conditions. We discuss the relevance of these results to the evolution of siderophore production in natural communities and heavy metal bioremediation. © 2014 The Authors Published by the Royal Society. All rights reserved.AXANatural Environment Research Council (NERC)University of Exete

Sexual selection in bacteria?

This is the final version. Available from the publisher via the DOI in this record.A main mechanism of lateral gene transfer in bacteria is transformation, where cells take up free DNA from the environment which subsequently can be recombined into the genome. Bacteria are also known to actively release DNA into the environment through secretion or lysis, which could aid uptake via transformation. Various evolutionary benefits of DNA uptake and DNA release have been proposed but these have all been framed in the context of natural selection. Here, we interpret bacterial DNA uptake and release in the context of sexual selection theory, which has been central to our understanding of the bewildering diversity of traits associated with sexual reproduction in the eukaryote world but has never been applied to prokaryotes. Specifically, we explore potential scenarios where bacteria releasing DNA into the environment could compete for successful uptake by other cells, or where bacteria could selectively take up DNA to enhance their fitness. We conclude that there is potential for sexual selection to act in bacteria, and that this might in part explain the considerable diversity in transformation-related behaviours.Royal SocietyNatural Environment Research Council (NERC

Temperature-dependent changes to host-parasite interactions alter the thermal performance of a bacterial host.

This is the author accepted manuscriptThermal performance curves (TPCs) are used to predict changes in species interactions, and hence, range shifts, disease dynamics and community composition, under forecasted climate change. Species interactions might in turn affect TPCs. Here, we investigate how temperature-dependent changes in a microbial host-parasite interaction (the bacterium Pseudomonas fluorescens, and its lytic bacteriophage, SBW[Formula: see text]) changes the host TPC and the ecological and evolutionary mechanisms underlying these changes. The bacteriophage had a narrower thermal tolerance for infection, with their critical thermal maximum ~6 °C lower than those at which the bacteria still had high growth. Consequently, in the presence of phage, the host TPC changed, resulting in a lower maximum growth rate. These changes were not just driven by differences in thermal tolerance, with temperature-dependent costs of evolved resistance also playing a major role: the largest cost of resistance occurred at the temperature at which bacteria grew best in the absence of phage. Our work highlights how ecological and evolutionary mechanisms can alter the effect of a parasite on host thermal performance, even over very short timescales.NER

Bacteria from natural populations transfer plasmids mostly towards their kin

This is the final version. Available on open access from the Royal Society via the DOI in this recordData accessibility: The datasets supporting this article are available from the Dryad Digital Repository at https://doi.org/10.5061/dryad.ff045t7 [52].Plasmids play a key role in microbial ecology and evolution, yet the determinants of plasmid transfer rates are poorly understood. Particularly, interactions between donor hosts and potential recipients are understudied. Here, we investigate the importance of genetic similarity between naturally co-occurring Escherichia coli isolates in plasmid transfer. We uncover extensive variability, spanning over five orders of magnitude, in the ability of isolates to donate and receive two different plasmids, R1 and RP4. Overall, transfer is strongly biased towards clone-mates, but not correlated to genetic distance when donors and recipients are not clone-mates. Transfer is limited by the presence of a functional restriction-modification system in recipients, suggesting sharing of strain-specific defence systems contributes to bias towards kin. Such restriction of transfer to kin sets the stage for longer-term coevolutionary interactions leading to mutualism between plasmids and bacterial hosts in natural communities.Medical Research Council (MRC

Fast-killing parasites can be favoured in spatially structured populations

This is the final version of the article. Available from the publisher via the DOI in this record.It is becoming increasingly clear that the evolution of infectious disease is influenced by host population structure. Theory predicts that parasites should be more 'prudent'-less transmissible-in spatially structured host populations. However, here we (i) highlight how low transmission, the phenotype being selected for in this in context, may also be achieved by rapacious host exploitation, if fast host exploitation confers a local, within-host competitive advantage and (ii) test this novel concept in a bacteria-virus system. We found that limited host availability and, to a lesser extent, low relatedness favour faster-killing parasites with reduced transmission. By contrast, high host availability and high relatedness favour slower-killing, more transmissible parasites. Our results suggest high, rather than low, virulence may be selected in spatially structured host-parasite communities where local competition and hence selection for a within-host fitness advantage is high.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.This work was funded by NERC, AXA Research fund, BBSRC, the Royal Society and The Royal Commission for the Exhibition of 185

Bacteria from natural populations transfer plasmids mostly towards their kin

This is the final version. Available on open access from the Royal Society via the DOI in this recordData accessibility: The datasets supporting this article are available from the Dryad Digital Repository at https://doi.org/10.5061/dryad.ff045t7 [52].Plasmids play a key role in microbial ecology and evolution, yet the determinants of plasmid transfer rates are poorly understood. Particularly, interactions between donor hosts and potential recipients are understudied. Here, we investigate the importance of genetic similarity between naturally co-occurring Escherichia coli isolates in plasmid transfer. We uncover extensive variability, spanning over five orders of magnitude, in the ability of isolates to donate and receive two different plasmids, R1 and RP4. Overall, transfer is strongly biased towards clone-mates, but not correlated to genetic distance when donors and recipients are not clone-mates. Transfer is limited by the presence of a functional restriction-modification system in recipients, suggesting sharing of strain-specific defence systems contributes to bias towards kin. Such restriction of transfer to kin sets the stage for longer-term coevolutionary interactions leading to mutualism between plasmids and bacterial hosts in natural communities.Medical Research Council (MRC

Targeting antibiotic resistant bacteria with phage reduces bacterial density in an insect host

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this recordData accessibility: Data are available from the Dryad Digital Repository at: http://dx.doi.org/10.5061/dryad.sc54383Phage therapy is attracting growing interest among clinicians as antibiotic resistance continues becoming harder to control. However, clinical trials and animal model studies on bacteriophage treatment are still scarce and results on the efficacy vary. Recent research suggests that using traditional antimicrobials in concert with phage could have desirable synergistic effects that hinder the evolution of resistance. Here, we present a novel insect gut model to study phage-antibiotic interaction in a system where antibiotic resistance initially exists in very low frequency and phage specifically targets the resistance bearing cells. We demonstrate that while phage therapy could not reduce the frequency of target bacteria in the population during positive selection by antibiotics, it alleviated the antibiotic induced blooming by lowering the overall load of resistant cells. The highly structured gut environment had pharmacokinetic effects on both phage and antibiotic dynamics compared with in vitro: antibiotics did not reduce the overall amount of bacteria, demonstrating a simple turnover of gut microbiota from non-resistant to resistant population with little cost. The results imply moderate potential for using phage as an aid to target antibiotic resistant gut infections, and question the usefulness of in vitro inferences.Medical Research Council (MRC)Academy of FinlandEmil Aaltonen Foundatio

Evolutionary temperature compensation of carbon fixation in marine phytoplankton

The efficiency of carbon sequestration by the biological pump could decline in the coming decades because respiration tends to increase more with temperature than photosynthesis. Despite these differences in the short-term temperature sensitivities of photosynthesis and respiration, it remains unknown whether the long-term impacts of global warming on metabolic rates of phytoplankton can be modulated by evolutionary adaptation. We found that respiration was consistently more temperature dependent than photosynthesis across 18 diverse marine phytoplankton, resulting in universal declines in the rate of carbon fixation with short-term increases in temperature. Long-term experimental evolution under high temperature reversed the short-term stimulation of metabolic rates, resulting in increased rates of carbon fixation. Our findings suggest that thermal adaptation may therefore have an ameliorating impact on the efficiency of phytoplankton as primary mediators of the biological carbon pump

Spatial heterogeneity lowers rather than increases host-parasite specialization.

This is the final version of the article. Available from the publisher via the DOI in this record.Abiotic environmental heterogeneity can promote the evolution of diverse resource specialists, which in turn may increase the degree of host-parasite specialization. We coevolved Pseudomonas fluorescens and lytic phage ϕ2 in spatially structured populations, each consisting of two interconnected subpopulations evolving in the same or different nutrient media (homogeneous and heterogeneous environments, respectively). Counter to the normal expectation, host-parasite specialization was significantly lower in heterogeneous compared with homogeneous environments. This result could not be explained by dispersal homogenizing populations, as this would have resulted in the heterogeneous treatments having levels of specialization equal to or greater than that of the homogeneous environments. We argue that selection for costly generalists is greatest when the coevolving species are exposed to diverse environmental conditions and that this can provide an explanation for our results. A simple coevolutionary model of this process suggests that this can be a general mechanism by which environmental heterogeneity can reduce rather than increase host-parasite specialization.This project was funded by NERC (NE/G006938/2), BBSRC and the AXA Research Fund. ABu is supported by a Royal Society Wolfson Research Merit Award. ABe is supported by a Leverhulme Early Career Research Fellowship

The impact of resource availability on bacterial resistance to phages in soil

This is the final version of the article. Available from Public Library of Science via the DOI in this recordResource availability can affect the coevolutionary dynamics between host and parasites, shaping communities and hence ecosystem function. A key finding from theoretical and in vitro studies is that host resistance evolves to greater levels with increased resources, but the relevance to natural communities is less clear. We took two complementary approaches to investigate the effect of resource availability on the evolution of bacterial resistance to phages in soil. First, we measured the resistance and infectivity of natural communities of soil bacteria and phage in the presence and absence of nutrient-providing plants. Second, we followed the real-time coevolution between defined bacteria and phage populations with resource availability manipulated by the addition or not of an artificial plant root exudate. Increased resource availability resulted in increases in bacterial resistance to phages, but without a concomitant increase in phage infectivity. These results suggest that phages may have a reduced impact on the control of bacterial densities and community composition in stable, high resource environments.The work was supported by NERC, the AXA research fund, BBSRC, the Royal Society (A.B.), and European Research Council funding under the European Union's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 268504 (K.J.G.)