Functional Convergence and Taxonomic Divergence in the Anchoveta (Engraulis ringens) Microbiome

Gut microbial community assembly involves a critical bioenergetic trade-off, yet the gut microbes with roles in influencing intestinal metabolic homeostasis remain poorly understood in pelagic ecosystems. A central unresolved question is whether microbiome structure is primarily governed by stochastic geographic drift or by deterministic metabolic filters imposed by diet. Here, we test the metabolic release hypothesis, which posits that access to high-quality prey physiologically “releases” the host from obligate dependence on diverse fermentative symbionts. By integrating δ15N analysis with 16S rRNA metabarcoding in the anchoveta from the South Pacific waters (Engraulis ringens), we reveal a profound, diet-induced restructuring of the gut ecosystem. We demonstrate that trophic ascent triggers a deterministic collapse in microbial alpha diversity (rs = −0.683), driven by the near-complete competitive exclusion of fermentative bacteria (rs = −0.874) and the resulting dominance of a specialized proteolytic core. Mechanistically, the bioavailability of zooplankton-derived protein favors efficient endogenous hydrolysis over costly microbial fermentation, rendering functional redundancy obsolete. Crucially, we find that while metabolic function converges, taxonomic identity remains geographically structured (r = 0.532), suggesting that local environments supply the specific taxa to fulfill universal metabolic roles. These findings establish a link between δ15N as a nutritional physiology proxy of anchoveta and its gut for microbial functional state, bridging the gap between nutritional physiology and ecosystem modeling to better inform the management of global forage fish stocks.