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Biology subjects

MacLean, R. C.

Publications and source records attributed to MacLean, R. C..

8 recordsLinked to original sources

Fitness costs of antibiotic resistance mutations in rich media do not reliably predict those in infection-like environments

The acquisition of antibiotic resistance is typically associated with a fitness cost, reducing the competitive ability of cells in the absence of antibiotics. Our ability to predict these costs informs our ability to predict how likely it is that resistance will subside in the absence of treatment. Fitness costs are typically measured in laboratory cultures using a nutritionally rich medium for growth. Here, we tested the impact of infection-like environments on the prevalence and magnitude of fitness costs associated with antibiotic resistance mutations in the opportunistic pathogen Pseudomonas aeruginosa. We assessed two different clinically relevant infection niches, the lung and urinary tract, through the use of infection-niche mimicking media that models the chemical compositions of these niches. The fitness costs of resistance mutations in rich media did not reliably predict those in infection-like environments, on average costs were increased in the lung-mimicking environment and costly mutations were less prevalent in the urinary tract-mimicking environment. Synthetic human urine significantly enhanced the fitness of P. aeruginosa with resistance mutations in nfxB, encoding a multidrug efflux pump transcriptional repressor, and we identified oxalate as the likely component driving this effect. Our findings highlight the importance of environmental chemical composition for shaping the fitness costs of resistance in P. aeruginosa and suggest that nfxB mutants may have a selective advantage in the urinary tract, mediated by the presence of oxalate.

microbiology↗

Conjugation structures plasmid populations through host-lineage restriction

Conjugation mediates plasmid transfer between bacterial species, driving the horizontal spread of traits like antibiotic resistance. However, genomic and experimental evidence indicates that many conjugative plasmids are restricted to particular host lineages despite broad theoretical host ranges. Using 4,281 plasmids from an epidemiologically coherent sample of 1,739 Escherichia coli bloodstream infection isolates, we quantify the host-lineage associations of 30 plasmid backbones and assess how these associations structure plasmid co-occurrence. To achieve this, we develop a novel Bayesian modelling framework that separates genuine backbone-backbone associations from patterns arising due to shared host ancestry or abundance. First, we find that conjugative backbones exhibit stronger host-lineage restriction than mobilisable backbones, and that restriction increases with plasmid size independently of mobility class. Consistent with this pattern, host-lineage restricted backbones demonstrate fewer independent acquisitions across the host phylogeny in ancestral state reconstructions. Comparison with global plasmid diversity shows that the most host-lineage restricted backbones remain restricted beyond the studied population, whereas the least restricted backbones span a mean of seven host species. Next, after accounting for host phylogeny and abundance, we find that two thirds of backbone pairs show no strong association or avoidance; however, backbones sharing host lineages co-occur more frequently than expected. Lastly, we identify a clique of strongly associated mobilisable backbones that appear to exploit a shared set of lineage-restricted conjugative partners. A mathematical model demonstrates that hostlineage restriction of conjugative backbones, together with specificity in conjugative-mobilisable transfer, is sufficient to generate clustering among mobilisable plasmids. Collectively, our findings reframe conjugation as a mechanism that promotes within-lineage persistence and shapes plasmid community structure, with potentially important consequences for the accumulation of resistance and virulence determinants.

microbiology↗

Competition constrains parasite adaptation to thermal heterogeneity

Temporal thermal heterogeneity is expected to favour intermediate, generalist phenotypes that can maintain growth across a broad thermal range but have sub-optimal growth at any single temperature. Yet, thermal variation typically occurs in the presence of additional selection pressures which may interact to constrain adaptation to temperature. We propagated competing lytic viral parasites (bacteriophages {phi}14-1 and {phi}LUZ19) of Pseudomonas aeruginosa under fluctuating temperatures (37-42{degrees}C) in monoculture and in co-culture. Without competition, fluctuating temperatures favoured intermediate thermal phenotypes in the phage {phi}14-1 and resulted in more variable evolutionary outcomes compared to static conditions. However, co-selection from fluctuating temperatures and competition led to restricted thermal adaptation, slower evolutionary rates, and fewer putative adaptive mutations in the {phi}LUZ19 competitor. Our study highlights the potential for reduced adaptive capacity in interacting communities amidst global climate change.

evolutionary biology↗

Evolutionary rescue accelerates competitive exclusion in a parasite community

Environmental stress drives biodiversity loss by altering competitive hierarchies and pushing taxa towards extinction. Parasites and their communities are particularly vulnerable to stress due to environmental sensitivity of infection steps, variation in species tolerance during co-infections, and dependence on host fitness. Parasite populations might avoid extinction through evolutionary rescue - whereby rapid adaptation to stress enables persistence - but whether this process can preserve community diversity remains unclear. Here, we study the impact of evolutionary rescue in a simple parasite community by propagating populations of two viral parasites (bacteriophages {phi}14-1 and {phi}LUZ19) of Pseudomonas aeruginosa in monoculture and co-culture under two thermal conditions, a control temperature (37{degrees}C) and a high temperature that restricts {phi}14-1 growth (42{degrees}C). We show that evolutionary rescue of {phi}14-1 prevented extinction in monoculture. Rescue of this phage in co-culture made it a superior competitor, and it replaced {phi}LUZ19 as the dominant phage at high temperature. We determine that evolutionary rescue occurred through mutations in genes linked to attachment to bacterial hosts and within-host replication. We also show that competitive suppression by {phi}14-1 constrained {phi}LUZ19 molecular evolution. Our findings suggest that evolutionary rescue can prevent the extinction of some parasites, but may inadvertently destabilise the community and facilitate further biodiversity loss. This work underscores the need to take an eco-evolutionary approach to predict the responses of communities to global climate change.

evolutionary biology↗

Adaptation of Pseudomonas aeruginosa to repeated invasion into a commensal competitor

The host-associated microbiome is an important barrier to bacterial pathogen colonization and can mediate protection through a variety of mechanisms. We wanted to investigate the potential consequences of selection imposed by commensal bacterial competitors on an invading bacterial pathogen. To do this, we tested the ability of the opportunistic pathogen Pseudomonas aeruginosa to invade pre-established communities of an abundant commensal bacterium in the human microbiome, Staphylococcus epidermidis. We passaged ten independent lines of P. aeruginosa through daily invasion into a pre-established S. epidermidis population (coculture evolved lines), alongside daily passage through monoculture conditions (monoculture evolved lines). The monoculture evolved lines showed strong parallel evolution in the Wsp (Wrinkly spreader phenotype) signal transducing system involved in biofilm formation, and significantly elevated biofilm formation. On the other hand, adaptation to S. epidermidis occurred via mutations in a diverse set of genes, and the coculture evolved lines showed much weaker evidence for parallel evolution, suggesting that the selective pressure imposed by competition with S. epidermidis is more complex than the pressure imposed by culture conditions. Interestingly, the elevated biofilm formation phenotype seen in the monoculture evolved lines was not observed in the lines evolved in the presence of S. epidermidis, raising the question of whether enhanced biofilm formation did not evolve with S. epidermidis present because it was not beneficial, or because S. epidermidis may be able to restrict this evolutionary path by inhibiting biofilm formation.

microbiology↗

Antibiotic resistance alters the ability of Pseudomonas aeruginosa to invade the respiratory microbiome

The emergence and spread of antibiotic resistance in bacterial pathogens is a global health threat. One important unanswered question is how antibiotic resistance influences the ability of a pathogen to invade the host-associated microbiome. Here we investigate how antibiotic resistance impacts the ability of the opportunistic bacterial pathogen Pseudomonas aeruginosa to invade the respiratory microbiome, by measuring the ability of P. aeruginosa spontaneous antibiotic resistant mutants to invade pre-established cultures of commensal respiratory microbes. We find that commensal respiratory microbes tend to inhibit the growth of P. aeruginosa, and antibiotic resistance is a double-edged sword that can either help or hinder the ability of P. aeruginosa to overcome this inhibition. The directionality of this help or hinderance depends on both P. aeruginosa genotype and respiratory microbe identity. Antibiotic resistance facilitates the invasion of P. aeruginosa into Staphylococcus lugdunensis, yet impairs invasion into Rothia mucilaginosa and Staphylococcus epidermidis. Streptococcus species provide the strongest inhibition to P. aeruginosa invasion, and this is maintained regardless of antibiotic resistance genotype. Our study demonstrates how antibiotic resistance can alter the ability of a bacterial pathogen to invade the respiratory microbiome and suggests that attempts to manipulate the microbiome should focus on promoting the growth of commensals that can provide robust inhibition of both wildtype and antibiotic resistant pathogen strains.

microbiology↗

Restriction-modification systems have shaped the evolution and distribution of plasmids across bacteria

Many novel traits such as antibiotic resistance are spread by plasmids between species. Yet plasmids have different host ranges. Restriction-modification systems (R-M systems) are by far the most abundant bacterial defense system and therefore represent one of the key barriers to plasmid spread. However, their effect on plasmid evolution and host range has been neglected. Here we analyse the avoidance of targets of the most abundant R-M systems (Type II) for complete genomes and plasmids across bacterial diversity. For the most common target length (6 bp) we show that target avoidance is strongly correlated with the taxonomic distribution of R-M systems and is greater in plasmid genes than core genes. We find stronger avoidance of R-M targets in plasmids which are smaller and have a broader host range. Our results suggest two different evolutionary strategies for plasmids: small plasmids primarily adapt to R-M systems by tuning their sequence composition, and large plasmids primarily adapt through the carriage of additional genes protecting from restriction. Our work provides systematic evidence that R-M systems are important barriers to plasmid transfer and have left their mark on plasmids over long evolutionary time.

microbiology↗

Polyclonal pathogen populations accelerate the evolution of antibiotic resistance in patients

Antibiotic resistance poses a global health threat, but the within-host drivers of resistance remain poorly understood. Pathogen populations are often assumed to be clonal within hosts, and resistance is thought to emerge due to selection for de novo variants. Here we show that pulmonary populations of the opportunistic pathogen P. aeruginosa are often polyclonal. Crucially, resistance evolves rapidly in patients colonized by polyclonal populations through selection for pre-existing resistant strains. In contrast, resistance evolves sporadically in patients colonized by monoclonal populations due to selection for novel resistance mutations. However, strong trade-offs between resistance and fitness occur in polyclonal populations that can drive the loss of resistant strains. In summary, we show that the within-host diversity of pathogen populations plays a key role in shaping the emergence of resistance in response to treatment. One sentence summaryAntibiotic resistance evolves quickly in patients colonized by polyclonal pathogen populations.

evolutionary biology↗