The Lolal-dpp axis mediates the regulation of host reproduction by gut symbionts in insects.

Abstract

Gut commensal microbiota can play an integral role in shaping insect reproduction, but the underlying mechanisms remain largely unexplored. Here, we report that gut bacteria promote host reproduction in the oriental fruit fly Bactrocera dorsalis by inducing ubiquitin-proteasome system (UPS)-mediated degradation of the key transcription factor Longitudinals lacking-like (Lolal). Antibiotic-induced gut bacterial depletion impairs ovarian development and fertility. These reproductive defects can be reversed by nicotinic acid (NA) supplementation or recolonization with a potent NA provider, Enterobacter hormaechei. Gut bacteria-derived NA enhances coenzyme nicotinamide adenine dinucleotide (NAD) biosynthesis and mitochondrial energy production, thereby activating the UPS. Ubiquitinome analysis reveals that gut bacteria enhance Lolal ubiquitination and promote its degradation. Lolal overabundance in gut bacteria-depleted females leads to decapentaplegic (dpp) overexpression and impaired reproduction. Conversely, Lolal knockdown suppresses dpp expression, resulting in disrupted mature egg formation. Our results reveal a link between gut bacteria-derived metabolites and host protein homeostasis which determines host reproductive success.