ABSTRACTAdultDrosophila melanogasterraised in the absence of symbiotic bacteria have fewer intestinal stem cell divisions and a longer life span than their conventionally reared counterparts. However, we do not know if increased stem cell divisions are essential for symbiont-dependent regulation of longevity. To determine if individual symbionts cause aging-dependent death inDrosophila, we examined the impacts of common symbionts on host longevity. We found that monoassociation of adultDrosophilawithLactobacillus plantarum, a widely reported fly symbiont and member of the probioticLactobacillusgenus, curtails adult longevity relative to germfree counterparts. The effects ofLactobacillus plantarumon life span were independent of intestinal aging. Instead, we found that association withLactobacillus plantarumcauses an extensive intestinal pathology within the host, characterized by loss of stem cells, impaired epithelial renewal, and a gradual erosion of epithelial ultrastructure. Our study uncovers an unknown aspect ofLactobacillus plantarum-Drosophilainteractions and establishes a simple model to characterize symbiont-dependent disruption of intestinal homeostasis.IMPORTANCEUnder homeostatic conditions, gut bacteria provide molecular signals that support the organization and function of the host intestine. Sudden shifts in the composition or distribution of gut bacterial communities impact host receipt of bacterial cues and disrupt tightly regulated homeostatic networks. We used theDrosophila melanogastermodel to determine the effects of prominent fly symbionts on host longevity and intestinal homeostasis. We found that monoassociation withLactobacillus plantarumleads to a loss of intestinal progenitor cells, impaired epithelial renewal, and disruption of gut architecture as flies age. These observations uncover a novel phenotype caused by monoassociation of a germfree host with a common symbiont and establish a simple model to characterize symbiont-dependent loss of intestinal homeostasis.
Testing evolutionary explanations for the lifespan benefit of dietary restriction in fruit flies (
Drosophila melanogaster
)
