Journal Article

Manipulation of gut microbiota during critical developmental windows affects host physiological performance and disease susceptibility across ontogeny

Warne, Robin W., Zeglin, Lydia, Kirschman, Lucas

2019

Overview

Colonization of gut microbiomes during early life can shape metabolism and immunity of adult animals. However, most data are derived from antibiotic‐treated or germ‐free laboratory mammals. Furthermore, few studies have explored how microbial colonization during critical windows influences a suite of other fitness‐related traits in wild animals. This study tested whether hatching constitutes a critical developmental window for gut microbiome colonization in wild‐caught amphibians and whether perturbations to gut microbiota at hatching shape fitness‐related traits of larval growth, metabolism, metamorphosis and disease susceptibility. We sterilized wood frog eggs and then inoculated them with microbes from differing sources, including from another species (bullfrogs) that differ in disease resistance and life history. We measured development, growth and metabolic rates through metamorphosis among individuals from each microbial treatment. A separate group was exposed to an LD50 dose of ranavirus—an emerging disease—to test for microbiome effects on disease susceptibility. We also quantified rates of deformities to test for microbial treatment effects on overall health. Manipulation of microbiota on eggs altered the trajectory of gut microbiome communities across larval ontogeny, though disruption appeared to be transitory. While microbiome structure converged among the treatments by metamorphosis, the effects of disruption on host phenotypes persisted. Larvae inoculated with the bullfrog gut microbiota exhibited accelerated growth and development rates compared to controls. By contrast, sterilized larvae maintained in sterile water for several days after hatching exhibited greater disruption to their gut microbiota across ontogeny, as well as altered metabolism, more tail deformities, and were more likely to die when exposed to an LD50 dose of ranavirus compared to the other treatments. These results suggest perturbations to the microbiota during critical developmental windows can alter the trajectory of the gut microbiome, and have long‐term effects on fitness‐related traits in larval amphibians. These results suggest that explicit tests of how changes in the composition and abundance of the microbial community shape phenotypes across ontogeny in amphibians could shed light on host–microbe interactions in wildlife, as well as inform conservation efforts to mitigate emerging diseases. This study shows that hatching is apparently a critical developmental window for bacterial colonization of larval amphibian guts. Perturbation at hatching alters the trajectory of gut microbiomes across ontogeny and shapes host phenotypes. Altered gut microbiota influenced larval amphibian growth, development, metabolism, morphological asymmetry and susceptibility to an emerging disease.

• Publisher: Wiley,Blackwell Publishing Ltd
• Subject: adults / amphibian microbiome / Amphibians / Animals / Antibiotics / carry‐over effects / Colonization / Deformation effects / digestive system / Disease / disease control / Disease resistance / Disease Susceptibility / Disruption / Eggs / emerging disease / emerging diseases / Fitness / fluctuating asymmetry / Gastrointestinal Microbiome / Hatching / host-pathogen relationships / Immunity / intestinal microbiota resilience / Intestinal microflora / intestinal microorganisms / Larvae / Larval development / lethal dose 50 / Life history / Lithobates sylvaticus / Long-term effects / Metabolic rate / Metabolism / Metamorphosis / microbial colonization / microbial communities / microbiome / Microbiomes / Microbiota / Microorganisms / Ontogeny / Ovum / phenotype / Phenotypes / phenotypic plasticity / Ranavirus / Ranidae / RESEARCH ARTICLE / tail / Trajectories / Wild animals / Wildlife / Wildlife conservation