A globally ubiquitous symbiont can drive experimental host evolution

Bates, Kieran A.; Bolton, Jai S; King, Kayla C.

doi:10.1111/mec.15998

Cited by 9 publications

(8 citation statements)

References 75 publications

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“…Prior studies have identified bacterialderived antimicrobial compounds that inhibit Bd growth [12-14, 17, 18]; however, determining overall microbiome community function remains challenging due to the complex web of interactions occurring amongst microbes [17,19]. Microbial taxa can also switch from being inhibitory to promoting pathogen growth based on community composition [19] and in more extreme cases can shift from being beneficial to parasitic (or vice-versa) in processes that may be mediated by host factors [20,21], the abiotic environment [22] or microbial community ecology [23]. As well as their role in defence, microbial communities are important in maintaining host dermal homeostasis [24][25][26][27].…”

Section: Introductionmentioning

confidence: 99%

Microbiome function predicts amphibian chytridiomycosis disease dynamics

et al. 2022

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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.

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Section: Introductionmentioning

confidence: 99%

Microbiome function predicts amphibian chytridiomycosis disease dynamics

et al. 2022

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“…Leucobacter musarum causes severe rectal disease and ultimately death in C. elegans [ 34 ] . Other species of this genus have been found naturally infecting C. elegans [ 35 , 36 ] . For parasite exposures, L. musarum was grown in LB broth at 30°C overnight, and the culture was standardized to OD(600) 0.3.…”

Section: Methodsmentioning

confidence: 99%

“…For parasite exposures, L. musarum was grown in LB broth at 30°C overnight, and the culture was standardized to OD(600) 0.3. The infection exposure plates were prepared by streaking 74 µl of inoculum containing 20% L. musarum and 80% OP50 (standardized to OD(600) 1) onto 5.5 cm NGM plates and incubating at 25°C for 24 h [ 36 ]. Control plates were prepared by spreading a similar amount of OP50 culture.…”

Section: Methodsmentioning

confidence: 99%

“…Worm populations were sampled before they were transferred to infection plates (labelled ‘pre-adult’) and after 10 h (labelled ‘adult’) under all temperature treatments. We sampled worm microbiomes at 10 h post-parasite exposure to ensure that host microbiomes were sampled from mostly live, infected hosts [ 36 ]. To collect host gut microbiomes, we washed worms off the NGM plate using M9 buffer.…”

Section: Methodsmentioning

confidence: 99%

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Dual stressors of infection and warming can destabilize host microbiomes

Li,

Gao,

Stevens

et al. 2024

Phil. Trans. R. Soc. B

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Climate change is causing extreme heating events and intensifying infectious disease outbreaks. Animals harbour microbial communities, which are vital for their survival and fitness under stressful conditions. Understanding how microbiome structures change in response to infection and warming may be important for forecasting host performance under global change. Here, we evaluated alterations in the microbiomes of several wild Caenorhabditis elegans isolates spanning a range of latitudes, upon warming temperatures and infection by the parasite Leucobacter musarum . Using 16S rRNA sequencing, we found that microbiome diversity decreased, and dispersion increased over time, with the former being more prominent in uninfected adults and the latter aggravated by infection. Infection reduced dominance of specific microbial taxa, and increased microbiome dispersion, indicating destabilizing effects on host microbial communities. Exposing infected hosts to warming did not have an additive destabilizing effect on their microbiomes. Moreover, warming during pre-adult development alleviated the destabilizing effects of infection on host microbiomes. These results revealed an opposing interaction between biotic and abiotic factors on microbiome structure. Lastly, we showed that increased microbiome dispersion might be associated with decreased variability in microbial species interaction strength. Overall, these findings improve our understanding of animal microbiome dynamics amidst concurrent climate change and epidemics. This article is part of the theme issue ‘Sculpting the microbiome: how host factors determine and respond to microbial colonization’.

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“…This has been observed, for example, in contexts as diverse as viral infections (Martinez et al 2014), the autoimmune response (Langan et al 2019), drug therapy (Pryor et al 2019), metabolic dysfunction (Ussar et al 2016), exposure to high temperatures (Xie et al 2013; Howells et al 2016), and chemical toxicity (Coryell et al 2018). Microbes can therefore impact adaptation of host populations to conditions that are apparently unrelated to the host-microbe interaction itself (Martinez et al 2016; Faria et al 2016; Bates et al 2021; Hoang et al 2021). This ability of microbes to modulate host adaptation to various stressors might thus play a fundamental but still poorly understood role in shaping the evolution of host life history and aging.…”

Section: Introductionmentioning

confidence: 99%

Microbes are potential key players in the evolution of life histories and aging inCaenorhabditis elegans

Santos

Matos

Flatt

et al. 2022

Preprint

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Microbes can have profound effects on host fitness and health and the appearance of late-onset diseases. Host-microbe interactions thus represent a major environmental context for healthy aging of the host and might also mediate trade-offs between life-history traits in the evolution of host senescence. Here we have used the nematode Caenorhadbitis elegans to examine whether host-microbe interactions might modulate the evolution of host life-history and aging. We first characterized the effects of two non-pathogenic Escherichia coli strains, a pathogenic E. coli strain and a pathogenic Serratia marcescens strain on the reproductive schedule and survival of an outbred C. elegans population, to be used in an experimental evolution study. Secondly, to investigate the dependency of these effects on host genotype, we assayed population growth rates and survival of five representative C. elegans inbred strains in response to these microbes. Our results show that host-microbe interactions have a substantial, host-genotype-dependent impact on reproductive effort and survival of the nematode host. Although pathogenic bacteria reduced host survival, as expected, they did not necessarily decrease host fertility or population growth rate. Given such microbe-specific genotypic differences in host life history, we predict that the evolution of reproductive schedules and senescence in this system might be critically contingent upon host-microbe interactions, a hypothesis which we will be testing using experimental evolution in future work.

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A globally ubiquitous symbiont can drive experimental host evolution

Cited by 9 publications

References 75 publications

Microbiome function predicts amphibian chytridiomycosis disease dynamics

Microbiome function predicts amphibian chytridiomycosis disease dynamics

Dual stressors of infection and warming can destabilize host microbiomes

Microbes are potential key players in the evolution of life histories and aging inCaenorhabditis elegans

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