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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.

Host-associated microbes are vital for combatting infections and maintaining health. In amphibians, certain skin-associated bacteria inhibit the fungal pathogen Batrachochytrium dendrobatidis ( Bd ), yet our understanding of host microbial ecology and its role in disease outbreaks is limited. We sampled skin-associated bacteria and Bd from Pyrenean midwife toad populations exhibiting enzootic or epizootic disease dynamics. We demonstrate that bacterial communities differ between life stages with few shared taxa, indicative of restructuring at metamorphosis. We detected a significant effect of infection history on metamorph skin microbiota, with reduced bacterial diversity in epizootic populations and differences in community structure and predicted function. Genome sequencing of Bd isolates supports a single introduction to the Pyrenees and reveals no association between pathogen genetics and epidemiological trends. Our findings provide an ecologically relevant insight into the microbial ecology of amphibian skin and highlight the relative importance of host microbiota and pathogen genetics in predicting disease outcome. Amphibian skin microbe communities have been putatively associated with the severity of chytrid fungal disease. Here, the authors show that different types of disease dynamics (enzootic versus epizootic) are associated with different microbiota in the host populations.

Chytridiomycosis caused by the fungal pathogen Batrachochytrium dendrobatidis ( Bd ) is pushing amphibians towards extinction. Whilst mitigation methods were suggested a decade ago, we lack field trials testing their efficacy. We used the agrochemical fungicide, tebuconazole, to treat Bd infected breeding waterbodies of an endangered species that is highly susceptible to the fungus. Just two applications of tebuconazole led to a significant reduction in infection loads in the vast majority of sites, and at six sites the disinfection remained one/two-years post-application. Tebuconazole values drastically decreased in the waterbodies within a week after application, with no significant effects on their hydrochemical and hydrobiological characteristics. Although the use of chemicals in natural populations is undesirable, the growing existential threat to amphibians all over the world indicates that effective interventions in selected populations of endangered species are urgently needed.

The Saiga are migratory antelopes inhabiting the grasslands of Eurasia. Over the last century, Saiga have been pushed to the brink of extinction by mass mortality events and intense poaching. Yet, despite the high profile of the Saiga as an animal of conservation concern, little is known of its biology. In particular, the gut microbiota of Saiga has not been studied, despite its potential importance in health. Here, we characterise the gut microbiota of Saiga from two geographically distinct populations in Kazakhstan and compare it with that of other antelope species. We identified a consistent gut microbial diversity and composition among individuals and across two Saiga populations during a year without die-offs, with over 85% of bacterial genera being common to both populations despite vast geographic separation. We further show that the Saiga gut microbiota resembled that of five other antelopes. The putative causative agent of Saiga mass die-offs, Pasteurella multocida , was not detected in the Saiga microbiota. Our findings provide the first description of the Saiga gut microbiota, generating a baseline for future work investigating the microbiota’s role in health and mass die-offs, and supporting the conservation of this critically endangered species.

Background The fungal pathogen Batrachochytrium dendrobatidis ( Bd ) threatens amphibian biodiversity and ecosystem stability worldwide. Amphibian skin microbial community structure has been linked to the clinical outcome of Bd infections, yet its overall functional importance is poorly understood. Methods Microbiome taxonomic and functional profiles were assessed using high-throughput bacterial 16S rRNA and fungal ITS2 gene sequencing, bacterial shotgun metagenomics and skin mucosal metabolomics. We sampled 56 wild midwife toads ( Alytes obstetricans ) from montane populations exhibiting Bd epizootic or enzootic disease dynamics. In addition, to assess whether disease-specific microbiome profiles were linked to microbe-mediated protection or Bd -induced perturbation, we performed a laboratory Bd challenge experiment whereby 40 young adult A. obstetricans were exposed to Bd or a control sham infection. We measured temporal changes in the microbiome as well as functional profiles of Bd -exposed and control animals at peak infection. Results Microbiome community structure and function differed in wild populations based on infection history and in experimental control versus Bd- exposed animals. Bd exposure in the laboratory resulted in dynamic changes in microbiome community structure and functional differences, with infection clearance in all but one infected animal. Sphingobacterium , Stenotrophomonas and an unclassified Commamonadaceae were associated with wild epizootic dynamics and also had reduced abundance in laboratory Bd -exposed animals that cleared infection, indicating a negative association with Bd resistance. This was further supported by microbe-metabolite integration which identified functionally relevant taxa driving disease outcome, of which Sphingobacterium and Bd were most influential in wild epizootic dynamics. The strong correlation between microbial taxonomic community composition and skin metabolome in the laboratory and field is inconsistent with microbial functional redundancy, indicating that differences in microbial taxonomy drive functional variation. Shotgun metagenomic analyses support these findings, with similar disease-associated patterns in beta diversity. Analysis of differentially abundant bacterial genes and pathways indicated that bacterial environmental sensing and Bd resource competition are likely to be important in driving infection outcomes. Conclusions Bd infection drives altered microbiome taxonomic and functional profiles across laboratory and field environments. Our application of multi-omics analyses in experimental and field settings robustly predicts Bd disease dynamics and identifies novel candidate biomarkers of infection. 6u4HXENqNsd5f8SBedLBdG Video Abstract

Sex-based differences in animal microbiota are increasingly recognized as of biological importance. While most animal biomass is found in aquatic ecosystems and many water-dwelling species are of high economic and ecological value, biological sex is rarely included as an explanatory variable in studies of the aquatic animal microbiota. In this opinion piece, we argue for greater consideration of host sex in studying the microbiota of aquatic animals, emphasizing the many advancements that this information could provide in the life sciences, from the evolution of sex to aquaculture.

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.

The disease pyramid conceptualizes the predictors of host infection risk, linking the host, the pathogen, environmental conditions, and both host and environmental microbiomes. However, the importance of the interaction between environmental and host-associated microbiomes in shaping infectious disease dynamics remains poorly understood. While the majority of studies have focused on bacteria, the role of micro-eukaryotes has been seldom investigated. Here, we explore three axes of the disease pyramid using an 18S rRNA gene metabarcoding approach to analyze the micro-eukaryotic assemblages of biofilm, water, and skin samples from three European amphibian species. Skin bacterial communities of the investigated amphibian populations have already been shown to be impacted by the presence of the lethal fungal pathogen ( ), with a higher abundance of protective bacteria in infected populations and a greater environmental microbial contribution to the skin microbiota in -positive lakes. Here, we explored the relationships between the micro-eukaryotic skin communities of these tadpole populations with their surrounding environment. Tadpoles were sampled at 22 mountain lakes located in the Pyrenees (France), 8 of which harbored amphibian populations infected by . We found that biofilms from -negative lakes had higher environmental micro-eukaryotic diversity and a greater abundance of putative anti- fungi, both in the environment and on the skin microbiota of and , but not of . Bayesian SourceTracker analysis further showed that the environmental contribution from biofilms to amphibian skin micro-eukaryotic assemblages was higher in -positive lakes for and , but not for .IMPORTANCEResearch on host-associated microbiomes and infectious diseases has mostly focused on bacteria, overlooking the potential contributions of micro-eukaryotes to infection dynamics. Here, we show that environmental and skin-associated micro-eukaryotes-especially putative anti- ( fungi-differ between -positive and -negative amphibian populations in mountain lakes. Our results suggest that micro-eukaryotes influence disease resistance and microbiome assembly, similarly to bacteria. Importantly, environmental reservoirs of micro-eukaryotes appear to contribute differently across infection contexts. These findings demonstrate the importance of adopting a broader microbiome perspective that includes micro-eukaryotes when investigating the ecological mechanisms underlying infectious disease risk.

Abstract Protective microbes have a major role in shaping host–pathogen interactions, but their relative importance in the structure of the host microbiota remains unclear. Here, we used a network approach to characterize the impact of a novel, experimentally evolved ‘protective microbial symbiont’ ( Enterococcus faecalis ) on the structure and predicted function of the natural microbiota of the model organism Caenorhabditis elegans . We used microbial network analysis to identify keystone taxa and describe the hierarchical placement of protective and non-protective symbionts in the microbiota. We found that early colonization with symbionts produce statistically significant changes in the structure of the community. Notably, only the protective E. faecalis became a keystone taxon in the nematode microbiota. Non-protective lineages of the same bacterial species remained comparatively unimportant to the community. Prediction of functional profiles in bacterial communities using PICRUSt2 showed that the presence of highly protective E. faecalis decreased the abundance of ergothioneine (EGT) biosynthesis pathway involved in the synthesis of the antioxidant molecule EGT, a potential public good. These data show that in addition to direct antagonism with virulent pathogens, keystone protective symbionts are linked to modified bacterial community structure and possible reductions in public goods, potentially driving decreased antioxidant defense. We suggest that this response could suppress infection via wholesale microbial community changes to further benefit the host. These findings extend the concept of protective symbionts beyond bodyguards to ecosystem engineers.