RESUMEN
Host-parasite interactions are highly susceptible to changes in temperature due to mismatches in species thermal responses. In nature, parasites often exist in communities, and responses to temperature are expected to vary between host-parasite pairs. Temperature change thus has consequences for both host-parasite dynamics and parasite-parasite interactions. Here, we investigate the impact of warming (37°C, 40°C, and 42°C) on parasite life-history traits and competition using the opportunistic bacterial pathogen Pseudomonas aeruginosa (host) and a panel of three genetically diverse lytic bacteriophages (parasites). We show that phages vary in their responses to temperature. While 37°C and 40°C did not have a major effect on phage infectivity, infection by two phages was restricted at 42°C. This outcome was attributed to disruption of different phage life-history traits including host attachment and replication inside hosts. Furthermore, we show that temperature mediates competition between phages by altering their competitiveness. These results highlight phage trait variation across thermal regimes with the potential to drive community dynamics. Our results have important implications for eukaryotic viromes and the design of phage cocktail therapies.IMPORTANCEMammalian hosts often elevate their body temperatures through fevers to restrict the growth of bacterial infections. However, the extent to which fever temperatures affect the communities of phages with the ability to parasitize those bacteria remains unclear. In this study, we investigate the impact of warming across a fever temperature range (37°C, 40°C, and 42°C) on phage life-history traits and competition using a bacterium (host) and bacteriophage (parasite) system. We show that phages vary in their responses to temperature due to disruption of different phage life-history traits. Furthermore, we show that temperature can alter phage competitiveness and shape phage-phage competition outcomes. These results suggest that fever temperatures have the potential to restrict phage infectivity and drive phage community dynamics. We discuss implications for the role of temperature in shaping host-parasite interactions more widely.
Asunto(s)
Pseudomonas aeruginosa , Pseudomonas aeruginosa/virología , Pseudomonas aeruginosa/fisiología , Bacteriófagos/fisiología , Calor , Fagos Pseudomonas/fisiología , Fagos Pseudomonas/crecimiento & desarrollo , Rasgos de la Historia de Vida , TemperaturaRESUMEN
Symbiosis can benefit hosts in numerous ways, but less is known about whether interactions with hosts benefit symbionts-the smaller species in the relationship. To determine the fitness impact of host association on symbionts in likely mutualisms, we conducted a meta-analysis across 91 unique host-symbiont pairings under a range of spatial and temporal contexts. Specifically, we assess the consequences to symbiont fitness when in and out of symbiosis, as well as when the symbiosis is under suboptimal or varying environments and biological conditions (e.g., host age). We find that some intracellular symbionts associated with protists tend to have greater fitness when the symbiosis is under stressful conditions. Symbionts of plants and animals did not exhibit this trend, suggesting that symbionts of multicellular hosts are more robust to perturbations. Symbiont fitness also generally increased with host age. Lastly, we show that symbionts able to proliferate in- and outside host cells exhibit greater fitness than those found exclusively inside or outside cells. The ability to grow in multiple locations may thus help symbionts thrive. We discuss these fitness patterns in light of host-driven factors, whereby hosts exert influence over symbionts to suit their own needs. Supplementary Information: The online version contains supplementary material available at 10.1007/s13199-024-00984-6.
RESUMEN
Animals live in symbiosis with numerous microbe species. While some can protect hosts from infection and benefit host health, components of the microbiota or changes to the microbial landscape have the potential to facilitate infections and worsen disease severity. Pathogens and pathobionts can exploit microbiota metabolites, or can take advantage of a depletion in host defences and changing conditions within a host, to cause opportunistic infection. The microbiota might also favour a more virulent evolutionary trajectory for invading pathogens. In this review, we consider the ways in which a host microbiota contributes to infectious disease throughout the host's life and potentially across evolutionary time. We further discuss the implications of these negative outcomes for microbiota manipulation and engineering in disease management.
Asunto(s)
Bacterias/patogenicidad , Infecciones Bacterianas/microbiología , Evolución Biológica , Interacciones Huésped-Patógeno , Microbiota , Animales , Infecciones Bacterianas/patología , HumanosRESUMEN
Global climate change has led to more extreme thermal events. Plants and animals harbour diverse microbial communities, which may be vital for their physiological performance and help them survive stressful climatic conditions. The extent to which microbiome communities change in response to warming or cooling may be important for predicting host performance under global change. Using a meta-analysis of 1377 microbiomes from 43 terrestrial and aquatic species, we found a decrease in the amplicon sequence variant-level microbiome phylogenetic diversity and alteration of microbiome composition under both experimental warming and cooling. Microbiome beta dispersion was not affected by temperature changes. We showed that the host habitat and experimental factors affected microbiome diversity and composition more than host biological traits. In particular, aquatic organisms-especially in marine habitats-experienced a greater depletion in microbiome diversity under cold conditions, compared to terrestrial hosts. Exposure involving a sudden long and static temperature shift was associated with microbiome diversity loss, but this reduction was attenuated by prior-experimental lab acclimation or when a ramped regime (i.e., warming) was used. Microbial differential abundance and co-occurrence network analyses revealed several potential indicator bacterial classes for hosts in heated environments and on different biome levels. Overall, our findings improve our understanding on the impact of global temperature changes on animal and plant microbiome structures across a diverse range of habitats. The next step is to link these changes to measures of host fitness, as well as microbial community functions, to determine whether microbiomes can buffer some species against a more thermally variable and extreme world.
Asunto(s)
Biodiversidad , Microbiota , Animales , Temperatura , Filogenia , Bacterias/genética , PlantasRESUMEN
Virulence, the harm to hosts caused by parasite infection, can be selected for by several ecological factors acting synergistically or antagonistically. Here, we focus on the potential for interspecific host competition to shape virulence through such a network of effects. We first summarize how host natural mortality, body mass changes, population density and community diversity affect virulence evolution. We then introduce an initial conceptual framework highlighting how these host factors, which change during host competition, may drive virulence evolution via impacts on life-history trade-offs. We argue that the multi-faceted nature of both interspecific host competition and virulence evolution still requires consideration and experimentation to disentangle contrasting mechanisms. It also necessitates a differential treatment for parasites with various transmission strategies. However, such a comprehensive approach focusing on the role of interspecific host competition is essential to understand the processes driving the evolution of virulence in a tangled bank.
Asunto(s)
Parásitos , Animales , Virulencia , Interacciones Huésped-Parásitos , Evolución BiológicaRESUMEN
Agricultural crops infected with vector-borne pathogens can suffer severe negative consequences, but the extent to which phytopathogens affect the fitness of their vector hosts remains unclear. Evolutionary theory predicts that selection on vector-borne pathogens will favour low virulence or mutualistic phenotypes in the vector, traits facilitating effective transmission between plant hosts. Here, we use a multivariate meta-analytic approach on 115 effect sizes across 34 unique plant-vector-pathogen systems to quantify the overall effect of phytopathogens on vector host fitness. In support of theoretical models, we report that phytopathogens overall have a neutral fitness effect on vector hosts. However, the range of fitness outcomes is diverse and span the parasitism-mutualism continuum. We found no evidence that various transmission strategies, or direct effects and indirect (plant-mediated) effects, of phytopathogens have divergent fitness outcomes for the vector. Our finding emphasizes diversity in tripartite interactions and the necessity for pathosystem-specific approaches to vector control.
Asunto(s)
Insectos Vectores , Simbiosis , Animales , Evolución Biológica , Fenotipo , VirulenciaRESUMEN
For infections to be maintained in a population, pathogens must compete to colonize hosts and transmit between them. We use an experimental approach to investigate within-and-between host dynamics using the pathogen Pseudomonas aeruginosa and the animal host Caenorhabditis elegans. Within-host interactions can involve the production of goods that are beneficial to all pathogens in the local environment but susceptible to exploitation by non-producers. We exposed the nematode host to 'producer' and two 'non-producer' bacterial strains (specifically for siderophore production and quorum sensing), in single infections and coinfections, to investigate within-host colonization. Subsequently, we introduced infected nematodes to pathogen-naive populations to allow natural transmission between hosts. We find that producer pathogens are consistently better at colonizing hosts and transmitting between them than non-producers during coinfection and single infection. Non-producers were poor at colonizing hosts and between-host transmission, even when coinfecting with producers. Understanding pathogen dynamics across these multiple levels will ultimately help us predict and control the spread of infections, as well as contribute to explanations for the persistence of cooperative genotypes in natural populations.
Asunto(s)
Bacterias , Coinfección , Animales , Percepción de Quorum , Caenorhabditis elegans/microbiología , Pseudomonas aeruginosa/genética , Coinfección/microbiologíaRESUMEN
Microbiota can protect their hosts from infection. The short timescales in which microbes can evolve presents the possibility that "protective microbes" can take-over from the immune system of longer-lived hosts in the coevolutionary race against pathogens. Here, we found that coevolution between a protective bacterium (Enterococcus faecalis) and a virulent pathogen (Staphylococcus aureus) within an animal population (Caenorhabditis elegans) resulted in more disease suppression than when the protective bacterium adapted to uninfected hosts. At the same time, more protective E. faecalis populations became costlier to harbor and altered the expression of 134 host genes. Many of these genes appear to be related to the mechanism of protection, reactive oxygen species production. Crucially, more protective E. faecalis populations downregulated a key immune gene, , known to be effective against S. aureus infection. These results suggest that a microbial line of defense is favored by microbial coevolution and may cause hosts to plastically divest of their own immunity.
Asunto(s)
Coevolución Biológica , Enterococcus faecalis/genética , Interacciones Huésped-Patógeno/inmunología , Staphylococcus aureus/genética , Animales , Caenorhabditis elegans , Enterococcus faecalis/metabolismo , Hierro/metabolismo , Microbiota , Especies Reactivas de Oxígeno/metabolismo , SimbiosisRESUMEN
AbstractSymbionts can provide hosts with effective protection from natural enemies, but it can sometimes come at a cost. It is unclear to what extent the density of symbionts modulates the cost and benefits of conferred protection. Here, we use a meta-analysis of 103 effect sizes from a broad taxonomic range of protective symbioses to show that the degree of both protection and cost afforded to hosts is a positive function of symbiont density. We found that the effects of symbiont density on protection and cost are robust across ecological contexts. Density-function relationships did not vary with host type, symbiont localization, or transmission mode, nor did they vary with the method of density manipulation. Taken together, our results suggest that symbiont density can be a key variable determining the costs and benefits of a protective interaction.
Asunto(s)
SimbiosisRESUMEN
Protective symbionts can defend hosts from parasites through several mechanisms, from direct interference to modulating host immunity, with subsequent effects on host and parasite fitness. While research on symbiont-mediated immune priming (SMIP) has focused on ecological impacts and agriculturally important organisms, the evolutionary implications of SMIP are less clear. Here, we review recent advances made in elucidating the ecological and molecular mechanisms by which SMIP occurs. We draw on current works to discuss the potential for this phenomenon to drive host, parasite, and symbiont evolution. We also suggest approaches that can be used to address questions regarding the impact of immune priming on host-microbe dynamics and population structures. Finally, due to the transient nature of some symbionts involved in SMIP, we discuss what it means to be a protective symbiont from ecological and evolutionary perspectives and how such interactions can affect long-term persistence of the symbiosis.
Asunto(s)
Sistema Inmunológico , Simbiosis , Animales , Ecología , Sistema Inmunológico/fisiología , ParásitosRESUMEN
Many host organisms live in polymicrobial environments and must respond to a diversity of pathogens. The degree to which host defences towards one pathogen species affect susceptibility to others is unclear. We used a panel of Caenorhabditis elegans nematode isolates to test for natural genetic variation in fitness costs of immune upregulation and pathogen damage, as well as for trade-offs in defence against two pathogen species, Staphylococcus aureus and Pseudomonas aeruginosa. We examined the fitness impacts of transient pathogen exposure (pathogen damage and immune upregulation) or exposure to heat-killed culture (immune upregulation only) by measuring host population sizes, which allowed us to simultaneously capture changes in reproductive output, developmental time and survival. We found significant decreases in population sizes for hosts exposed to live versus heat-killed S. aureus and found increased reproductive output after live P. aeruginosa exposure, compared with the corresponding heat-killed challenge. Nematode isolates with relatively higher population sizes after live P. aeruginosa infection produced fewer offspring after live S. aureus challenge. These findings reveal that wild C. elegans genotypes display a trade-off in defences against two distinct pathogen species that are evident in subsequent generations.
Asunto(s)
Caenorhabditis elegans , Staphylococcus aureus , Animales , Caenorhabditis elegans/genética , Genotipo , Pseudomonas aeruginosa/genética , Reproducción , Staphylococcus aureus/genéticaRESUMEN
Microbes that protect against infection inhabit hosts across the tree of life. It is unclear whether and how the host immune system may affect the formation of new protective symbioses. We investigated the transcriptomic response of Caenorhabditis elegans following novel interactions with a protective microbe (Enterococcus faecalis) able to defend against infection by pathogenic Staphylococcus aureus. We have previously shown that E. faecalis can directly limit pathogen growth within hosts. In this study, we show that colonisation by protective E. faecalis caused the differential expression of 1,557 genes in pathogen infected hosts, including the upregulation of immune genes such as lysozymes and C-type lectins. The most significantly upregulated host lysozyme gene, lys-7, impacted the competitive abilities of E. faecalis and S. aureus when knocked out. E. faecalis has an increased ability to resist lysozyme activity compared to S. aureus, suggesting that the protective microbe could gain a competitive advantage from this host response. Our finding that protective microbes can benefit from immune-mediated competition after introduction opens up new possibilities for biocontrol design and our understanding of symbiosis evolution. Crosstalk between the host immune response and microbe-mediated protection should favour the continued investment in host immunity and avoid the potentially risky evolution of host dependence.
Asunto(s)
Muramidasa , Staphylococcus aureus , Animales , Staphylococcus aureus/genética , Muramidasa/genética , Caenorhabditis elegans/genética , Enterococcus faecalis/genética , SimbiosisRESUMEN
Organisms harbour myriad microbes which can be parasitic or protective against harm. The costs and benefits resulting from these symbiotic relationships can be context-dependent, but the evolutionary consequences to hosts of these transitions remain unclear. Here, we mapped the Leucobacter genus across 13,715 microbiome samples (163 studies) to reveal a global distribution as a free-living microbe or a symbiont of animals and plants. We showed that across geographically distant locations (South Africa, France, Cape Verde), Leucobacter isolates vary substantially in their virulence to an associated animal host, Caenorhabditis nematodes. We further found that multiple Leucobacter sequence variants co-occur in wild Caenorhabditis spp. which combined with natural variation in virulence provides real-world potential for Leucobacter community composition to influence host fitness. We examined this by competing C. elegans genotypes that differed in susceptibility to different Leucobacter species in an evolution experiment. One Leucobacter species was found to be host-protective against another, virulent parasitic species. We tested the impact of host genetic background and Leucobacter community composition on patterns of host-based defence evolution. We found host genotypes conferring defence against the parasitic species were maintained during infection. However, when hosts were protected during coinfection, host-based defences were nearly lost from the population. Overall, our results provide insight into the role of community context in shaping host evolution during symbioses.
Asunto(s)
Microbiota , Nematodos , Parásitos , Animales , Caenorhabditis elegans , Simbiosis/genéticaRESUMEN
Natural and anthropogenic stressors, including parasites and pesticides, may induce oxidative stress in animals. Measuring oxidative stress responses in sentinel species that are particularly responsive to environmental perturbations not only provides insight into host physiology but is also a useful readout of ecosystem health. Newly metamorphosed northern leopard frogs (Lithobates pipiens), a sentinel species, were collected from agricultural and non-agricultural wetlands exposed to varying concentrations of the herbicide atrazine. Significant effects of certain parasites' abundance and their interaction with atrazine exposure on frog oxidative stress were identified. Specifically, increased protein levels were detected in frogs infected with echinostome metacercariae. In addition, the nematode Oswaldocruzia sp. was significantly associated with increased thiol concentration and catalase activity. Significant parasite × atrazine interactions were observed for atrazine exposure and the abundance of Oswaldocruzia sp. on thiol, as thiol concentrations increased with parasite abundance at low atrazine localities and decreased in high atrazine wetlands. In addition, a significant interaction between the abundances of Oswaldocruzia sp. and gorgoderid trematodes on thiol concentrations was observed. These findings demonstrate that studies of oxidative stress on animals in natural ecosystems should account for the confounding effects of parasitism, particularly for amphibians in agricultural landscapes.
Asunto(s)
Atrazina/toxicidad , Herbicidas/toxicidad , Rana pipiens , Estrés Fisiológico , Infecciones por Strongylida/veterinaria , Infecciones por Trematodos/veterinaria , Animales , Molineoidae/aislamiento & purificación , Prevalencia , Quebec/epidemiología , Infecciones por Strongylida/epidemiología , Infecciones por Strongylida/parasitología , Trematodos/aislamiento & purificación , Infecciones por Trematodos/epidemiología , Infecciones por Trematodos/parasitología , HumedalesRESUMEN
BACKGROUND: Bacteria adapted to live within animals can protect their hosts against harmful infections. Beyond antagonism with pathogens, a 'defensive' bacterial symbiont could engage in additional interactions with other colonizing micro-organisms. A single bacterium might thus have cascading ecological impacts on the whole microbiome that are rarely investigated. Here, we assess the role of a defensive symbiont as a driver of host-associated microbiota composition by using a bacterial species (Enterococcus faecalis) that was previously experimentally adapted to a nematode host model (Caenorhabditis elegans). RESULTS: An analysis of 16S rRNA data from C. elegans exposed to E. faecalis and subsequently reared in soil, reveal that symbiont adaptation to host environment or its protective potential had minimal impact on microbiota diversity. Whilst the abundance of Pseudomonas was higher in the microbiota of hosts with protective E.faecalis (and another protective species tested), a few other genera - including Serratia and Salinispora - were less abundant in hosts colonized by all E. faecalis strains. In addition, the protective effect of E. faecalis against virulent Staphylococcus aureus pathogens was maintained despite multi-species interactions within the microbiota. CONCLUSIONS: Our results reveal the degree to which a new, evolving symbiont can colonise and maintain pathogen-resistance with minimal disruption to host microbiota diversity.
Asunto(s)
Bacterias/clasificación , Caenorhabditis elegans/microbiología , Resistencia a la Enfermedad , Enterococcus faecalis/fisiología , ARN Ribosómico 16S/genética , Animales , Bacterias/genética , Bacterias/aislamiento & purificación , ADN Bacteriano/genética , ADN Ribosómico/genética , Microbiota , Filogenia , Análisis de Secuencia de ADN , SimbiosisRESUMEN
There is evidence that human activities are reducing the population genetic diversity of species worldwide. Given the prediction that parasites better exploit genetically homogeneous host populations, many species could be vulnerable to disease outbreaks. While agricultural studies have shown the devastating effects of infectious disease in crop monocultures, the widespread nature of this diversity-disease relationship remains unclear in natural systems. Here, we provide broad support that high population genetic diversity can protect against infectious disease by conducting a meta-analysis of 23 studies, with a total of 67 effect sizes. We found that parasite functional group (micro- or macroparasite) affects the presence of the effect and study setting (field or laboratory-based environment) influences the magnitude. Our study also suggests that host genetic diversity is overall a robust defence against infection regardless of host reproduction, parasite host range, parasite diversity, virulence and the method by which parasite success was recorded. Combined, these results highlight the importance of monitoring declines of host population genetic diversity as shifts in parasite distributions could have devastating effects on at-risk populations in nature.
Asunto(s)
Agricultura , Variación Genética , Interacciones Huésped-Parásitos , Parásitos/fisiología , Animales , Genética de Población , Especificidad del Huésped , Humanos , VirulenciaRESUMEN
Climate change and anthropogenic activity are currently driving large changes in nutritional availability across ecosystems, with consequences for infectious disease. An increase in host nutrition could lead to more resources for hosts to expend on the immune system or for pathogens to exploit. In this paper, we report a meta-analysis of studies on host-pathogen systems across the tree of life, to examine the impact of host nutritional quality and quantity on pathogen virulence. We did not find broad support across studies for a one-way effect of nutrient availability on pathogen virulence. We thus discuss a hypothesis that there is a balance between the effect of host nutrition on the immune system and on pathogen resources, with the pivot point of the balance differing for vertebrate and invertebrate hosts. Our results suggest that variation in nutrition, caused by natural or anthropogenic factors, can have diverse effects on infectious disease outcomes across species.
Asunto(s)
Interacciones Huésped-Patógeno/inmunología , Interacciones Huésped-Patógeno/fisiología , Estado Nutricional/fisiología , Virulencia , Fenómenos Fisiológicos Nutricionales de los Animales , Animales , Enfermedades Transmisibles/inmunología , Enfermedades Transmisibles/fisiopatología , Humanos , Estado Nutricional/inmunología , Enfermedades de las Plantas , PlantasRESUMEN
In an ideal world, funding agencies could identify the best scientists and projects and provide them with the resources to undertake these projects. Most scientists would agree that in practice, how funding for scientific research is allocated is far from ideal and likely compromises research quality. We, nine evolutionary biologists from different countries and career stages, provide a comparative summary of our impressions on funding strategies for evolutionary biology across eleven different funding agencies. We also assess whether and how funding effectiveness might be improved. We focused this assessment on 14 elements within four broad categories: (a) topical shaping of science, (b) distribution of funds, (c) application and review procedures, and (d) incentives for mobility and diversity. These comparisons revealed striking among-country variation in those elements, including wide variation in funding rates, the effort and burden required for grant applications, and the extent of emphasis on societal relevance and individual mobility. We use these observations to provide constructive suggestions for the future and urge the need to further gather informed considerations from scientists on the effects of funding policies on science across countries and research fields.
Asunto(s)
Evolución Biológica , Financiación del Capital , Apoyo a la Investigación como Asunto , Ciencia/economía , Política Pública , Estados UnidosRESUMEN
Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. Whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. For instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. Despite this, horizontal transmission, and the host contact structures that facilitates it, have not been considered in heritable symbiont epidemiology. Here, we tested for the importance of host contact, and resulting horizontal transmission, for the epidemiology of a male-killing heritable symbiont (Arsenophonus nasoniae) in parasitoid wasp hosts. We observed that host contact through superparasitism is necessary for this symbiont's spread in populations of its primary host Nasonia vitripennis, such that when superparasitism rates are high, A. nasoniae almost reaches fixation, causes highly female biased population sex ratios and consequently causes local host extinction. We further tested if natural interspecific variation in superparasitism behaviours predicted symbiont dynamics among parasitoid species. We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts. The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence. Our results thus indicate that host contact behaviour is a key factor for heritable microbe dynamics when horizontal transmission is possible, and that 'reproductive parasite' phenotypes, such as male-killing, may be of secondary importance in the dynamics of such symbiont infections.
Asunto(s)
Transmisión de Enfermedad Infecciosa/veterinaria , Proteobacteria/patogenicidad , Simbiosis/fisiología , Avispas/parasitología , Animales , Femenino , Masculino , Razón de MasculinidadRESUMEN
BACKGROUND: Animal and plant species can harbour microbes that provide them with protection against enemies. These beneficial microbes can be a significant component of host defence that complement or replaces a repertoire of immunity, but they can also be costly. Given their impact on host and parasite fitness, defensive microbes have the potential to influence host-parasite interactions on an evolutionary timescale. RESULTS: Using a phenotypic framework, we explore the evolutionary and coevolutionary dynamics of a host-parasite interaction in the presence of defensive microbes. We show that costs of host-defensive microbe systems are critical in determining whether a defensive microbe based system or an immune system provides better host protection investment. Partitioning the coevolutionary dynamics yields testable predictions. The density of defensive microbes influences the strength of selection resulting from host - defensive microbe - parasite coevolutionary interactions. We find that they lessen the negative effects of infection on hosts and reduce infectivity by directly competing with parasites. CONCLUSIONS: Defensive microbes might thus play a central role in host-parasite interactions, by outright replacing host-based defences, engaging in within-host competition with parasites, and ultimately driving tripartite coevolutionary dynamics.