AbstractIn an era of unprecedented environmental change, there have been increasing ecological and global public health concerns associated with exposure to anthropogenic pollutants. While there is a pressing need to remediate polluted ecosystems, human intervention strategies might unwittingly oppose selection for natural detoxification, which is primarily carried out by microbes. We test this possibility in the context of a ubiquitous chemical remediation strategy aimed at targeting toxic metal pollution: the addition of lime-containing materials. Here we show that raising pH by liming decreased the availability of toxic metals in acidic mine-degraded soils, but as a consequence selected against microbial taxa that naturally remediate soil through the production of metal-scavenging siderophores. Understanding the ecological and evolutionary consequences of human intervention on key traits is crucial for the engineering of evolutionary resilient microbial communities, having important implications for human health and biotechnology.

AbstractWith rising antibiotic resistance, there has been increasing interest in treating pathogenic bacteria with bacteriophages (phage therapy). One limitation of phage therapy is the ease at which bacteria can evolve resistance. Negative effects of resistance may be mitigated when resistance results in reduced bacterial growth and virulence, or when phage coevolve to overcome resistance. Resistance evolution and its consequences are contingent on the bacteria-phage combination and their environmental context, making therapeutic outcomes hard to predict. One solution might be to conduct “in vitro evolutionary simulations” using bacteria-phage combinations from the therapeutic context. Overall, our aim was to investigate parallels between in vitro experiments and in vivo dynamics in a human participant. Evolutionary dynamics were similar, with high levels of resistance evolving quickly with limited evidence of phage evolution. Resistant bacteria – evolved in vitro and in vivo - had lower virulence. In vivo, this was linked to lower growth rates of resistant isolates, whereas in vitro phage resistant isolates evolved greater biofilm production. Population sequencing suggests resistance resulted from selection on de novo mutations rather than sorting of existing variants. These results highlight the speed at which phage resistance can evolve in vivo, and in vitro experiments may give useful insights for clinical evolutionary outcomes.

AbstractThe ability of species to mutually invade from rare is the defining measure of species coexistence. However, it is unknown whether invasion growth rates predict any characteristic of long-term community dynamics. Here, we use a model five-species microbial community to investigate the link between short-term growth rate and long-term relative abundance. We manipulated diversity and tested the ability of species to coexist in different combinations. Across all diversity levels and species combinations, populations re-established from rare in 71 of 75 combinations and all combinations were stable in long-term culture. Moreover, short-term relative invader growth rate was positively associated with long-term equilibrium proportion, despite large variation in interactions between species and communities. This finding was confirmed using a modelling approach and suggests that the short-term invasion growth rate can predict long-term relative abundance within that community.

AbstractThermal 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 whether temperature-dependent changes in a microbial host-parasite interaction (the bacterium Pseudomonas fluorescens, and its bacteriophage, SBWФ2) changes the host TPC. The bacteriophage had a narrower infectivity range, 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 had a higher optimum temperature and a lower maximum growth rate. These changes were driven by a temperature-dependent evolution, and cost, of resistance; the largest cost of resistance occurring where 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.Data accessibility statementAll data and R code used in the analysis will be made available on GitHub and archived on Zenodo.

ABSTRACTGross primary production (GPP) is the largest flux in the carbon cycle, yet its response to global warming is highly uncertain. The temperature sensitivity of GPP is directly linked to photosynthetic physiology, but the response of GPP to warming over longer timescales could also be shaped by ecological and evolutionary processes that drive variation community structure and functional trait distributions. Here, we show that selection on photosynthetic traits within and across taxa dampen the effects of temperature on GPP across a catchment of geothermally heated streams. Autotrophs from cold streams had higher photosynthetic rates and after accounting for differences in biomass among sites, rates of ecosystem-level GPP were independent of temperature, despite a 20 ºC thermal gradient. Our results suggest that thermal adaptation constrains the long-term temperature dependence of GPP, and highlights the importance of considering physiological, ecological and evolutionary mechanisms when predicting how ecosystem-level processes respond to warming.

Accumulation of plastics in the marine environment has widespread detrimental consequences for ecosystems and wildlife. Marine plastics are rapidly colonised by a wide diversity of bacteria, including human pathogens, posing potential risks to health. Here, we investigate the effect of polymer type, residence time and estuarine location on bacterial colonisation of common household plastics, including pathogenic bacteria. We submerged five main household plastic types: low-density PE (LDPE), high-density PE (HDPE), polypropylene (PP), polyvinyl chloride (PVC) and polyethylene terephthalate (PET) at an estuarine site in Cornwall (U.K.) and tracked bacterial colonisation dynamics. Using both culture-dependent and culture-independent approaches, we found that bacteria rapidly colonised plastics irrespective of polymer type, reaching culturable densities of up to 1000 cells cm3 after 7 weeks. Community composition of the biofilms changed over time, but not among polymer types. The presence of pathogenic bacteria, quantified using the insect model Galleria mellonella, increased dramatically over a five-week period, with Galleria mortality increasing from 4% in week one to 65% in week five. No consistent differences in virulence were observed between polymer types. Pathogens isolated from plastic biofilms using Galleria enrichment included Serratia and Enterococcus species and they harboured a wide range of antimicrobial resistance genes. Our findings show that plastics in coastal waters are rapidly colonised by a wide diversity of bacteria independent of polymer type. Further, our results show that marine plastic biofilms become increasingly associated with virulent bacteria over time.

Disturbances can facilitate biological invasions, with the associated increase in resource availability being a proposed cause. Here, we experimentally tested the interactive effects of disturbance regime (different frequencies of biomass removal at equal intensities) and resource abundance on invasion success using a factorial design containing five disturbance frequencies and three resource levels. We invaded populations of the bacterium Pseudomonas fluorescens with two ecologically different invader morphotypes: a fast-growing "colonizer" type and a slower growing "competitor" type. As resident populations were altered by the treatments, we additionally tested their effect on invader success. Disturbance frequency and resource abundance interacted to affect the success of both invaders, but this interaction differed between the invader types. The success of the colonizer type was positively affected by disturbance under high resources but negatively under low. However, disturbance negatively affected the success of the competitor type under high resource abundance but not under low or medium. Resident population changes did not alter invader success beyond direct treatment effects. We therefore demonstrate that the same disturbance regime can either be beneficial or detrimental for an invader depending on both community resource abundance and its life history. These results may help to explain some of the inconsistencies found in the disturbance-invasion literature.

With rising antibiotic resistance, there has been increasing interest in treating pathogenic bacteria with bacteriophages (phage therapy). One limitation of phage therapy is the ease at which bacteria can evolve resistance. Negative effects of resistance may be mitigated when resistance results in reduced bacterial growth and virulence, or when phage coevolves to overcome resistance. Resistance evolution and its consequences are contingent on the bacteria-phage combination and their environmental context, making therapeutic outcomes hard to predict. One solution might be to conduct 'in vitro evolutionary simulations' using bacteria-phage combinations from the therapeutic context. Overall, our aim was to investigate parallels between in vitro experiments and in vivo dynamics in a human participant. Evolutionary dynamics were similar, with high levels of resistance evolving quickly with limited evidence of phage evolution. Resistant bacteria-evolved in vitro and in vivo-had lower virulence. In vivo, this was linked to lower growth rates of resistant isolates, whereas in vitro phage resistant isolates evolved greater biofilm production. Population sequencing suggests resistance resulted from selection on de novo mutations rather than sorting of existing variants. These results highlight the speed at which phage resistance can evolve in vivo, and how in vitro experiments may give useful insights for clinical evolutionary outcomes.

Spatial resource heterogeneity is expected to be a key driver for the evolution of diversity. However, direct empirical support for this prediction is limited to studies carried out in simplified laboratory environments. Here, we investigate how altering spatial heterogeneity of potting compost-by the addition of water and mixing-affects the evolutionary diversification of a bacterial species, Pseudomonas fluorescens, that is naturally found in the environment. There was a greater propensity of resource specialists to evolve in the unmanipulated compost, while more generalist phenotypes dominated the compost-water mix. Genomic data were consistent with these phenotypic findings. Competition experiments strongly suggest these results are due to diversifying selection as a result of resource heterogeneity, as opposed to other covariables. Overall, our findings corroborate theoretical and in vitro findings, but in semi-natural, more realistic conditions.

Microbes can invade as whole communities, but the ecology of whole community invasions is poorly understood. Here, we investigate how invader propagule pressure (the number of invading organisms) affects the composition and function of invaded laboratory methanogenic communities. An invading community was equally successful at establishing itself in a resident community regardless of propagule pressure, which varied between 0.01 and 10% of the size resident community. Invasion resulted in enhanced biogas production (to the level of the pure invading community) but only when propagule pressure was 1% or greater. This inconsistency between invasion success and changes in function can be explained by a lower richness of invading taxa at lower propagule pressures, and an important functional role of the taxa that were absent. Our results highlight that whole community invasion ecology cannot simply be extrapolated from our understanding of single species invasions. Moreover, we show that methane production can be enhanced by invading poorly performing reactors with a better performing community at levels that may be practical in industrial settings.

Community coalescence, the mixing of different communities, is widespread throughout microbial ecology. Coalescence can result in approximately equal contributions from the founding communities or dominance of one community over another. These different outcomes have ramifications for community structure and function in natural communities, and the use of microbial communities in biotechnology and medicine. However, we have little understanding of when a particular outcome might be expected. Here, we integrate existing theory and data to speculate on how a crucial characteristic of microbial communities-the type of species interaction that dominates the community-might affect the outcome of microbial community coalescence. Given the often comparable timescales of microbial ecology and microevolution, we explicitly consider ecological and evolutionary dynamics, and their interplay, in determining coalescence outcomes. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.

Rapid within-species evolution can alter community structure, yet the mechanisms underpinning this effect remain unknown. Populations that rapidly evolve large amounts of phenotypic diversity are likely to interact with more species and have the largest impact on community structure. However, the evolution of phenotypic diversity is, in turn, influenced by the presence of other species. Here, we investigate how microbial community structure changes as a consequence of rapidly evolved within-species diversity using Pseudomonas fluorescens as a focal species. Evolved P. fluorescens populations showed substantial phenotypic diversification in resource-use (and correlated genomic change) irrespective of whether they were pre-adapted in isolation or in a community context. Manipulating diversity revealed that more diverse P. fluorescens populations had the greatest impact on community structure, by suppressing some bacterial taxa, but facilitating others. These findings suggest that conditions that promote the evolution of high within-population diversity should result in a larger impact on community structure.

Interspecific coevolutionary interactions can result in rapid biotic adaptation, but most studies have focused only on species pairs. Here, we (co)evolved five microbial species in replicate polycultures and monocultures and quantified local adaptation. Specifically, growth rate assays were used to determine adaptations of each species' populations to (1) the presence of the other four species in general and (2) sympatric vs. allopatric communities. We found that species did not show an increase in net biotic adaptation:ancestral, polyculture- and monoculture-evolved populations did not have significantly different growth rates within communities. However, 4/5 species' growth rates were significantly lower within the community they evolved in relative to an allopatric community. 'Local maladaptation' suggests that species evolved increased competitive interactions to sympatric species' populations. This increased competition did not affect community stability or productivity. Our results suggest that (co)evolution within communities can increase competitive interactions that are specific to (co)evolved community members.

Thermal 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.

Community coalescence, the mixing of multiple communities, is ubiquitous in natural microbial communities. During coalescence, theory suggests the success of a population will be enhanced by the presence of species it has coevolved with (relative to foreign species), because coevolution will result in greater resource specialization to minimize competition. Thus, more coevolved communities should dominate over less coevolved communities during coalescence events. We test these hypotheses using the bacterium Pseudomonas fluorescens which diversifies into coexisting niche-specialist morphotypes. We first evolved replicate populations for ~40 generations and then isolated evolved genotypes. In a series of competition trials, we determined if using coevolved versus random genotypes affected the relative performance of "communities" of single and multiple genotypes. We found no effect of coevolutionary history on either genotype fitness or community performance, which suggests parallel (co)evolution between communities. However, fitness was enhanced by the presence of other genotypes of the same strain type (wild-type or an isogenic strain with a LacZ marker; the inclusion of the latter necessary to distinguish genotypes during competition), indicative of local adaptation with respect to genetic background. Our results are the first to investigate the effect of (co)evolution on the outcome of coalescence and suggest that when input populations are functionally similar and added at equal mixing ratios, the outcome community may not be asymmetrically dominated by either input population.

In an era of unprecedented environmental change, there have been increasing ecological and global public health concerns associated with exposure to anthropogenic pollutants. While there is a pressing need to remediate polluted ecosystems, human intervention might unwittingly oppose selection for natural detoxification, which is primarily carried out by microbes. We test this possibility in the context of a ubiquitous chemical remediation strategy aimed at targeting metal pollution: the addition of lime-containing materials. Here, we show that raising pH by liming decreased the availability of toxic metals in acidic mine-degraded soils, but as a consequence selected against microbial taxa that naturally remediate soil through the production of metal-binding siderophores. Our results therefore highlight the crucial need to consider the eco-evolutionary consequences of human environmental strategies on microbial ecosystem services and other traits.

Relating the temperature dependence of photosynthetic biomass production to underlying metabolic rates in autotrophs is crucial for predicting the effects of climatic temperature fluctuations on the carbon balance of ecosystems. We present a mathematical model that links thermal performance curves (TPCs) of photosynthesis, respiration, and carbon allocation efficiency to the exponential growth rate of a population of photosynthetic autotroph cells. Using experiments with the green alga, Chlorella vulgaris, we apply the model to show that the temperature dependence of carbon allocation efficiency is key to understanding responses of growth rates to warming at both ecological and longer-term evolutionary timescales. Finally, we assemble a dataset of multiple terrestrial and aquatic autotroph species to show that the effects of temperature-dependent carbon allocation efficiency on potential growth rate TPCs are expected to be consistent across taxa. In particular, both the thermal sensitivity and the optimal temperature of growth rates are expected to change significantly due to temperature dependence of carbon allocation efficiency alone. Our study provides a foundation for understanding how the temperature dependence of carbon allocation determines how population growth rates respond to temperature.

Trophic interactions are important determinants of the structure and functioning of ecosystems. Because the metabolism and consumption rates of ectotherms increase sharply with temperature, there are major concerns that global warming will increase the strength of trophic interactions, destabilizing food webs, and altering ecosystem structure and function. We used geothermally warmed streams that span an 11°C temperature gradient to investigate the interplay between temperature-driven selection on traits related to metabolism and resource acquisition, and the interaction strength between the keystone gastropod grazer, Radix balthica, and a common algal resource. Populations from a warm stream (~28°C) had higher maximal metabolic rates and optimal temperatures than their counterparts from a cold stream (~17°C). We found that metabolic rates of the population originating from the warmer stream were higher across all measurement temperatures. A reciprocal transplant experiment demonstrated that the interaction strengths between the grazer and its algal resource were highest for both populations when transplanted into the warm stream. In line with the thermal dependence of respiration, interaction strengths involving grazers from the warm stream were always higher than those with grazers from the cold stream. These results imply that increases in metabolism and resource consumption mediated by the direct, thermodynamic effects of higher temperatures on physiological rates are not mitigated by metabolic compensation in the long term, and suggest that warming could increase the strength of algal-grazer interactions with likely knock-on effects for the biodiversity and productivity of aquatic ecosystems.

Understanding the mechanisms that determine how phytoplankton adapt to warming will substantially improve the realism of models describing ecological and biogeochemical effects of climate change. Here, we quantify the evolution of elevated thermal tolerance in the phytoplankton, Chlorella vulgaris. Initially, population growth was limited at higher temperatures because respiration was more sensitive to temperature than photosynthesis meaning less carbon was available for growth. Tolerance to high temperature evolved after ≈ 100 generations via greater down-regulation of respiration relative to photosynthesis. By down-regulating respiration, phytoplankton overcame the metabolic constraint imposed by the greater temperature sensitivity of respiration and more efficiently allocated fixed carbon to growth. Rapid evolution of carbon-use efficiency provides a potentially general mechanism for thermal adaptation in phytoplankton and implies that evolutionary responses in phytoplankton will modify biogeochemical cycles and hence food web structure and function under warming. Models of climate futures that ignore adaptation would usefully be revisited. Copyright

Understanding the mechanisms that determine how phytoplankton adapt to warming will substantially improve the realism of models describing ecological and biogeochemical effects of climate change. Here, we quantify the evolution of elevated thermal tolerance in the phytoplankton, Chlorella vulgaris. Initially, population growth was limited at higher temperatures because respiration was more sensitive to temperature than photosynthesis meaning less carbon was available for growth. Tolerance to high temperature evolved after ≈ 100 generations via greater down-regulation of respiration relative to photosynthesis. By down-regulating respiration, phytoplankton overcame the metabolic constraint imposed by the greater temperature sensitivity of respiration and more efficiently allocated fixed carbon to growth. Rapid evolution of carbon-use efficiency provides a potentially general mechanism for thermal adaptation in phytoplankton and implies that evolutionary responses in phytoplankton will modify biogeochemical cycles and hence food web structure and function under warming. Models of climate futures that ignore adaptation would usefully be revisited.