Environmental Factors and Host Microbiomes Shape Host–Pathogen Dynamics

In many cases, interactions among host, pathogen, and environment are insufficient to describe disease dynamics in the wild.
The host microbiome plays an important role in host immunity, at the interface between the host and the pathogen, and affects disease outcome.
The environment, as well as environmental microbiomes, influence the host microbiome, and also influence simultaneously the host and the pathogen.

The three-edged disease triangle needs to become a four-edged disease pyramid to study interactions among host, host microbiome, pathogen, and environment.
Microorganisms are increasingly recognized as ecosystem-relevant components because they affect the population dynamics of hosts. Functioning at the interface of the host and pathogen, skin and gut microbiomes are vital components of immunity. Recent work reveals a strong influence of biotic and abiotic environmental factors (including the environmental microbiome) on disease dynamics, yet the importance of the host–host microbiome–pathogen–environment interaction has been poorly reflected in theory.

We use amphibians and the disease chytridiomycosis caused by the fungal pathogen Batrachochytrium dendrobatidis to show how interactions between host, host microbiome, pathogen, and the environment all affect disease outcome. Our review provides new perspectives that improve our understanding of disease dynamics and ecology by incorporating environmental factors and microbiomes into disease theory.