Host-associated microbiomes are predicted by immune system complexity and climate

Abstract

Background: Host-associated microbiomes, the microorganisms occurring inside and on host surfaces, influence evolutionary, immunological, and ecological processes. Interactions between host and microbiome affect metabolism and contribute to host adaptation to changing environments. Meta-analyses of hostassociated bacterial communities have the potential to elucidate global-scale patterns of microbial community structure and function. It is possible that host surface-associated (external) microbiomes respond more strongly to variations in environmental factors, whereas internal microbiomes are more tightly linked to host factors. Results: Here, we use the dataset from the Earth Microbiome Project and accumulate data from 50 additional studies totaling 654 host species and over 15,000 samples to examine global-scale patterns of bacterial diversity and function. We analyze microbiomes from non-captive hosts sampled from natural habitats and find patterns with bioclimate and geophysical factors, as well as land use, host phylogeny, and trophic level/ diet. Specifically, external microbiomes are best explained by variations in mean daily temperature range and precipitation seasonality. In contrast, internal microbiomes are best explained by host factors such as phylogeny/immune complexity and trophic level/diet, plus climate. Conclusions: Internal microbiomes are predominantly associated with top-down effects, while climatic factors are stronger determinants of microbiomes on host external surfaces. Host immunity may act on microbiome diversity through top-down regulation analogous to predators in non-microbial ecosystems. Noting gaps in geographic and host sampling, this combined dataset represents a global baseline available for interrogation by future microbial ecology studies.

Coupled Microbiome Analyses Highlights Relative Functional Roles of Bacteria in a Bivalve Hatchery

“…Some of the taxa detected in our study may be part of the microbiome essential for an effective immune response and survival, but it is di cult to discern which taxa this would be without differential mortality between larval cohorts. There is a correlation between host microbiome diversity and the complexity of the immune system, with more stable microbiomes in invertebrates with innate immune systems [48]. It is worth identifying this stable, core microbiome in ecologically and commercially important taxa as a means to better understand mechanisms of environmental response and survival.…”

Skin microbiome correlates with bioclimate and Batrachochytrium dendrobatidis infection intensity in Brazil’s Atlantic Forest treefrogs

“…The microbial communities associated with the skin (i.e., skin or cutaneous microbiome) play a significant role in pathogen defense and may, therefore be involved in predisposition to different diseases and contribute to host fitness 6 – 8 . Due to its direct exposure to the environment, the skin microbiome is thought to be much more dynamic than the microbiome of other parts of the animal such as the gut 9 , 10 , and consequently, the role of the environment is expected to be strong in shaping its composition, diversity and function 11 , 12 . Moreover, host-specific factors such pH, sebum production, temperature and moisture are known to shape the skin microbiome and its defensive function 7 , 13 , 14 .…”

“…Host associated factors are less studied but clearly also play a role because multiple studies have demonstrated that the skin microbiomes of co-occurring species are significantly different 18 , 29 , 36 , 37 . Only few general patterns have been identified for host-associated factors, whereas global-scale patterns in microbial diversity have been tied to environmental factors such as bioclimate and habitat 10 , 19 . Amphibians depend on microbial environmental reservoirs, such as forest soil, to maintain diverse skin microbiomes 30 , 38 and the peculiar conditions of the amphibian skin selects for particular microbial taxa to be integrated in the skin-associated communities 37 , 39 .…”

Consistent patterns in 16S and 18S microbial diversity from the shells of the common and widespread red-eared slider turtle (Trachemys scripta)

“…The turtle shell microbiome may simultaneously serve as an indicator of both turtle health and overall ecosystem status. Very generally, the external microbiomes of organisms are influenced by climatic effects, rather than "top-down" or species-specific effects [2]. This suggests that turtles could be susceptible to pathogenic microbial growth on external surfaces, including for novel reptile-associated [3] and known human pathogens [4] present in the environment.…”