Into the wild: microbiome transplant studies need broader ecological reality

Abstract

Gut microbial communities (microbiomes) profoundly shape the ecology and evolution of multicellular life. Interactions between host and microbiome appear to be reciprocal, and ecological theory is now being applied to better understand how hosts and their microbiome influence each other. However, some ecological processes that underlie reciprocal host-microbiome interactions may be obscured by the current convention of highly-controlled transplantation experiments. Although these approaches have yielded invaluable insights, there is a need for a broader array of approaches to fully understand host-microbiome reciprocity. Using a directed review, we surveyed the breadth of ecological reality in the current literature on gut microbiome transplants with non-human recipients. For 55 studies, we categorized 9 key experimental conditions that impact the ecological reality (EcoReality) of the transplant, including host taxon match and donor environment. Using these categories, we rated the EcoReality of each transplant. Encouragingly, the breadth of EcoReality has increased over time, but some components of EcoReality are still relatively unexplored, including recipient host environment and microbiome state. The conceptual framework we develop here maps the landscape of possible EcoReality to highlight where fundamental ecological processes can be considered in future transplant experiments.

The microbiota of intertidal macroalgae Fucus distichus is site‐specific and resistant to change following transplant

“…Thus, we used reciprocal transplants in the field to investigate the stability of the F . distichus microbiota in ecologically realistic conditions (Greyson‐Gaito et al ., 2020). Again, we found that existing differences by site of origin were resistant to change over the 6‐day experiment (Figs 3 and 4) and significant differences in microbiota by site of origin persisted.…”

“…distichus and the microbiota. Field‐based transplant studies are a crucial yet underutilized tool to understand host–microbiota associations in ecologically realistic conditions (Greyson‐Gaito et al ., 2020). We hypothesized that the microbiota of transplanted F .…”

“…We used common garden and reciprocal transplant experiments to test the stability of associations between F. distichus and the microbiota. Field-based transplant studies are a crucial yet underutilized tool to understand host-microbiota associations in ecologically realistic conditions (Greyson-Gaito et al, 2020). We hypothesized that the microbiota of transplanted F. distichus would rapidly shift to reflect the contemporary environment of the host because environmental conditions pose a strong selective filter and also alter the microbial source pools available to colonize the host.…”

Diet induces parallel changes to the gut microbiota and problem solving performance in a wild bird

“…Here we ruled out stress as a determining factor as baseline and stress-induced corticosterone did not explain PSP. Further manipulative experiments, such as using a wide range of food rewards, or microbial transplantation experiments 12 , 61 in the absence of dietary differences would provide additional support that the microbiome itself caused the change in problem solving performance.…”

Stabilization and optimization of host-microbe-environment interactions as a potential reason for the behavior of natal philopatry

“…First, a thorough understanding of the basic microbial ecology of animal systems that engage in natal philopatry is still lacking. Overall, microbiome research has been largely biased towards model systems and biomedical studies [122][123][124]. In many wild systems we still lack thorough knowledge on the routes of microbial acquisition, microbial sharing, and the effects of microbial communities on performance and fitness.…”