How are gut microbes transmitted? An integrative approach to quantify the ecological factors driving microbiome transfer in guppies

Microorganisms play an essential role in the health, growth and development of animals, collectively forming the microbiota. Despite their renowned importance, the ecological factors that drive microbiome transfer - such as host contact and dispersal - remain poorly understood. Fish, which comprise the majority of vertebrate species, offer unique advantages for studying microbiome ecology, particularly due to their suitability for controlled experiments and their relevance in aquaculture and conservation contexts. In this study, we chose to investigate the transmission dynamics of the gut microbiome in the guppy (Poecilia reticulata). Guppies have been extensively studied in behavioural and ecological research, thus providing a tractable system for accurate measurement of animal contact. Specifically, we aimed to quantify the relative contributions of host contact and dispersal through water to microbiome transfer across individuals. To achieve this, we generated microbiome-depleted guppies, co-housed them in tanks with conventional animals with and without physical contact, and used a multi-faceted experimental approach. This included: (1) identification and quantification of host-host interactions (e.g. contact, mating, nipping) (2) bacterial growth analysis, (3) metagenomic profiling of the fish gut, and (4) fluorescence in situ hybridization. By integrating these parameters, we identified the predominant transmission routes of microbial populations and elucidated the ecological factors driving the transfer of specific microbial species. This study provides important insights into microbiome dynamics in aquatic environments and highlights the ecological processes underlying microbial transmission in fish, with potential applications for sustainable aquaculture and environmental management.