skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Diet- and salinity-induced modifications of the gut microbiota are associated with differential physiological responses to ranavirus infection in Rana sylvatica
Greater knowledge of how host–microbiome interactions vary with anthropogenic environmental change and influence pathogenic infections is needed to better understand stress-mediated disease outcomes. We investigated how increasing salinization in freshwaters (e.g. due to road de-icing salt runoff) and associated increases in growth of nutritional algae influenced gut bacterial assembly, host physiology and responses to ranavirus exposure in larval wood frogs (Rana sylvatica). Elevating salinity and supplementing a basic larval diet with algae increased larval growth and also increased ranavirus loads. However, larvae given algae did not exhibit elevated kidney corticosterone levels, accelerated development or weight loss post-infection, whereas larvae fed a basic diet did. Thus, algal supplementation reversed a potentially maladaptive stress response to infection observed in prior studies in this system. Algae supplementation also reduced gut bacterial diversity. Notably, we observed higher relative abundances of Firmicutes in treatments with algae—a pattern consistent with increased growth and fat deposition in mammals—that may contribute to the diminished stress responses to infection via regulation of host metabolism and endocrine function. Our study informs mechanistic hypotheses about the role of microbiome mediation of host responses to infection that can be tested in future experiments in this host–pathogen system  more » « less
Award ID(s):
1754474
PAR ID:
10512318
Author(s) / Creator(s):
; ; ; ; ; ; ;
Publisher / Repository:
The Royal Society Publishing
Date Published:
Journal Name:
Philosophical Transactions of the Royal Society B: Biological Sciences
Volume:
378
Issue:
1882
ISSN:
0962-8436
Page Range / eLocation ID:
20220121
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Microbiomes are major determinants of host growth, development and survival. In amphibians, host-associated bacteria in the skin can inhibit pathogen infection, but many processes can influence the structure and composition of the community. Here we quantified the shifts in skin-associated bacteria across developmental stages in the striped newt (Notophthalmus perstriatus), a threatened salamander species with a complex life history and vulnerable to infection by the amphibian chytrid fungusBatrachochytrium dendrobatidisand ranavirus. Our analyses show that pre-metamorphic larval and paedomorphic stages share similar bacterial compositions, and that the changes in the microbiome coincided with physiological restructuring during metamorphosis. Newts undergoing metamorphosis exhibited microbiome compositions that were intermediate between paedomorphic and post-metamorphic stages, further supporting the idea that metamorphosis is a major driver of host-associated microbes in amphibians. We did not find support for infection-related disruption of the microbiome, though infection replicates were small for each respective life stage. 
    more » « less
  2. Bonneaud, Camille (Ed.)
    Abstract Macronutrients play a vital role in host immunity and can influence host–pathogen dynamics, potentially through dietary effects on gut microbiota. To increase our understanding of how dietary macronutrients affect physiology and gut microbiota and investigate whether feeding behaviour is influenced by an immune threat, we conducted two experiments. First, we determined whether zebra finches (Taeniopygia guttata) exhibit shifts in physiology and gut microbiota when fed diets differing in macronutrient ratios. We found the type and amount of diet consumed affected gut microbiota alpha diversity, where microbial richness and Shannon diversity increased with caloric intake in birds fed a high‐fat diet and decreased with caloric intake in birds fed a high protein diet. Diet macronutrient content did not affect physiological metrics, but lower caloric intake was associated with higher complement activity. In our second experiment, we simulated an infection in birds using the bacterial endotoxin lipopolysaccharide (LPS) and quantified feeding behaviour in immune challenged and control individuals, as well as birds housed near either a control pair (no immune threat), or birds housed near a pair given an immune challenge with LPS (social cue of heightened infection risk). We also examined whether social cues of infection alter physiological responses relevant to responding to an immune threat, an effect that could be mediated through shifts in feeding behaviour. LPS induced a reduction in caloric intake driven by a decrease in protein, but not fat consumption. No evidence was found for socially induced shifts in feeding behaviour, physiology or gut microbiota. Our findings carry implications for host health, as sickness‐induced anorexia and diet‐induced shifts in the microbiome could shape host–pathogen interactions. 
    more » « less
  3. The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genusNeotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts. 
    more » « less
  4. Abstract Diet profoundly influences the composition of an animal’s microbiome, especially in holometabolous insects, offering a valuable model to explore the impact of diet on gut microbiome dynamics throughout metamorphosis. Here, we use monarch butterflies (Danaus plexippus), specialist herbivores that feed as larvae on many species of chemically well-defined milkweed plants (Asclepias sp.), to investigate the impacts of development and diet on the composition of the gut microbial community. While a few microbial taxa are conserved across life stages of monarchs, the microbiome appears to be highly dynamic throughout the life cycle. Microbial diversity gradually diminishes throughout the larval instars, ultimately reaching its lowest point during the pupal stage and then recovering again in the adult stage. The microbial composition then undergoes a substantial shift upon the transition from pupa to adult, with female adults having significantly different microbial communities than the eggs that they lay, indicating limited evidence for vertical transmission of gut microbiota. While diet did not significantly impact overall microbial composition, our results suggest that fourth instar larvae exhibit higher microbial diversity when consuming milkweed with high concentrations of toxic cardenolide phytochemicals. This study underscores how diet and developmental stage collectively shape the monarch’s gut microbiota. 
    more » « less
  5. ABSTRACT The present work aimed to study whether a high sugar diet can alter immune responses and the gut microbiome in green iguanas. Thirty-six iguanas were split into four treatment groups using a 2×2 design. Iguanas received either a sugar-supplemented diet or a control diet, and either a lipopolysaccharide (LPS) injection or a phosphate-buffered saline (PBS) injection. Iguanas were given their respective diet treatment through the entire study (∼3 months) and received a primary immune challenge 1 and 2 months into the experiment. Blood samples and cloacal swabs were taken at various points in the experiment and used to measure changes in the immune system (bacterial killing ability, lysis and agglutination scores, LPS-specific IgY concentrations), and alterations in the gut microbiome. We found that a sugar diet reduces bacterial killing ability following an LPS challenge, and sugar and the immune challenge temporarily alters gut microbiome composition while reducing alpha diversity. Although sugar did not directly reduce lysis and agglutination following the immune challenge, the change in these scores over a 24-h period following an immune challenge was more drastic (it decreased) relative to the control diet group. Moreover, sugar increased constitutive agglutination outside of the immune challenges (i.e. pre-challenge levels). In this study, we provide evidence that a high sugar diet affects the immune system of green iguanas (in a disruptive manner) and alters the gut microbiome. 
    more » « less