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 nine 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.

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 stressinduced 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.…”

Application of ecological and evolutionary theory to microbiome community dynamics across systems

“…Microbiome transplant studies represent an important and increasingly applied approach to characterize host-microbiota interactions. While stating that although there is a clear need for highly controlled microbiome transplant experiments, Greyson-Gaito et al [8] reviewed the breadth of ecological reality in microbiome transplant studies and identified nine experimental conditions that affect EcoReality. Their analysis suggests that the 'EcoReality' of microbiota transplant studies has increased over time, and they present a roadmap for enhancing EcoReality in future transplantation experiments.…”

“…However, manipulating host-microbiota interactions in animal hosts is arguably a more challenging endeavour. Greyson-Gaito et al [8] explore the power of microbiota transplants for testing the impact of gut microbiota on host health and phenotype, cautioning about the importance of considering the ecological realism of the transplant when interpreting the results.…”

“…This special feature addresses key research gaps in microbiome research by developing theoretical and conceptual frameworks to describe factors that influence microbiome assembly and stability, including a generalist-specialist game theory model of infant gut microbiome maturation [16], a metabolite-explicit model of microbial cross-feeding and invasion [17] and theoretical models on the role of mixed modes of transmission on stable host-microbota associations [9]. Additional advances include conceptual and methodological frameworks for detection of host phylogeny and microbiome relationships [12,14], rapid microbial evolution and ecological opportunity in gut microbiomes [11], and approaches to enhance the ecological reality of microbiome transplant studies [8]. The deterministic assembly of teleost fish microbiomes and possibilities for microbiome manipulation for sustainable aquaculture are also discussed [21].…”

“…A key theme emanating from this feature is the power of combining complementary approaches from different disciplines to address such questions. In addition to providing new theoretical and conceptual models to assess the ecology and evolution of host-associated microbiomes, the articles presented in this special feature also highlight ongoing research gaps and future research priorities for the field, including: (i) the validity of highly controlled microbiome transplant experiments, but guidelines for broadening Eco-Reality in future experiments [8], as appropriate, (ii) greater consideration of host physiology and its impacts on microbiome assembly and dynamics [10], (iii) the need for applied experimental evolution studies to characterize rapid evolution within microbiomes [11], and (iv) integrated theoretical, conceptual and empirical approaches are required to address complex host-microbiome-environment interactions. This may include combinations of experimental evolution and genomics approaches to study rapid evolution and functional consequences [11], host physiology [10], applying conceptual frameworks for statistical analysis of quantitative signals of phylosymbiosis across taxa [12,14], microbiota transplants [7,8], or the combination of reductionist and emergentist approaches to disentangle complex host-microbiota-insect interactions associated with disease [18].…”