Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data

A priority in gut microbiome research is to develop methods to investigate ecological processes shaping microbial populations in the host from readily accessible data, such as fecal samples. Here, we demonstrate that these processes can be inferred from the proportion of ingested microorganisms that is egested and their egestion time distribution, by using general mathematical models that link within-host processes to statistics from fecal time series. We apply this framework to Drosophila melanogaster and its gut bacterium Acetobacter tropicalis. Specifically, we investigate changes in their interactions following ingestion of a food bolus containing bacteria in a set of treatments varying the following key parameters: the density of exogenous bacteria ingested by the flies (low/high) and the association status of the host (axenic or monoassociated with A. tropicalis). At 5 h post-ingestion, ~35% of the intact bacterial cells have transited through the gut with the food bolus and ~10% are retained in a viable and culturable state, leaving ~55% that have likely been lysed in the gut. Our models imply that lysis and retention occur over a short spatial range within the gut when the bacteria are ingested from a low density, but more broadly in the host gut when ingested from a high density, by both gnotobiotic and axenic hosts. Our study illustrates how time series data complement the analysis of static abundance patterns to infer ecological processes as bacteria traverse the host. Our approach can be extended to investigate how different bacterial species interact within the host to understand the processes shaping microbial community assembly.