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. 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. a reversible change of a physiological trait in response to an environmental change. a disease that either has appeared and affected a population for the first time, or has existed previously but is rapidly spreading, either in terms of the number of individuals getting infected, or to new geographical areas. Emerging infectious diseases are caused by pathogens that are increasing in their incidence, geographic or host range, and virulence. a symbiotic system, composed of the host and its microbial partners (bacteria, archaea, viruses, and eukaryotes). microbial communities living on (e.g., skin microbiome) or in (e.g., gut microbiome) the host. Skin and gut microbiomes are currently better described, but other host microbial communities exist, for example, in the mouth, nose, pharynx, and respiratory and urogenital tracts. the communities of microorganisms including bacteria, yeast, fungi, protists, and archaea in combination with their genomes. the collection of microorganisms that exists in a given environment, habitat, or host (inside or on the host). microscopic organisms that exist as single cells or cell clusters. They include bacteria, protozoa, archaea, microscopic fungi, and microscopic algae. We include here also viruses, which are microscopic but not cellular, although there is ongoing scientific discussion regarding their characterization as ‘micro-organisms’. ‘operational taxonomic unit’, used to refer to a cluster of DNA sequences of microorganisms, which are grouped by sequence similarity of a defined taxonomic marker gene present in their DNA. initially, the pathobiome concept was defined as the pathogenic agent integrated within its microbial community (i.e., the pathogen interacting with the environmental microbiome [13.Vayssier-Taussat M. et al.Shifting the paradigm from pathogens to pathobiome: new concepts in the light of meta-omics.Front. Cell. Infect. Microbiol. 2014; 4: 29Crossref PubMed Scopus (155) Google Scholar]). This concept has now evolved to host-associated microorganisms (prokaryotes, eukaryotes, and viruses) negatively impacting the health of the host, with the interaction between the host and its pathobiome inevitably moderated by the environment within the host and immediately surrounding it [14.Bass D. et al.The pathobiome in animal and plant diseases.Trends Ecol. Evol. 2019; 34: 996-1008Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar]. the extent to which an organism can change its physiology, behavior, morphology, and/or development in response to environmental cues. a known infectious disease increasing in incidence after a period of reduced incidence, or even disappearance, of the disease.