Unveiling the co-phylogeny signal between plunderfishHarpagiferspp. and their gut microbiomes across the Southern Ocean

Abstract

Understanding the factors that sculpt fish gut microbiome is challenging, especially in natural populations characterized by high environmental and host genomic complexity. Yet, closely related hosts are valuable models for deciphering the contribution of host evolutionary history to microbiome assembly, through the underscoring of phylosymbiosis and co-phylogeny patterns. Here, we hypothesized that the recent allopatric speciation ofHarpagiferacross the Southern Ocean (1.2–0.8 Myr) will promote the detection of robust phylogenetic congruence between the host and its microbiome.We characterized the gut mucosa microbiome of 77 individuals from four field-collected species of the plunderfishHarpagifer(Teleostei, Notothenioidei), distributed across three biogeographic regions of the Southern Ocean. We found that seawater physicochemical properties, host phylogeny and geography collectively explained 35% of the variation in bacterial community composition inHarpagifergut mucosa. The core microbiome ofHarpagiferspp. gut mucosa was characterized by a low diversity, mostly driven by selective processes, and dominated by a singleAliivibriotaxon detected in more than 80% of the individuals. Almost half of the core microbiome taxa, includingAliivibrio, harbored co-phylogeny signal at microdiversity resolution withHarpagiferphylogeny. This suggests an intimate symbiotic relationship and a shared evolutionary history withHarpagifer.The robust phylosymbiosis signal emphasizes the relevance of theHarpagifermodel to understanding the contribution of fish evolutionary history to the gut microbiome assembly. We propose that the recent allopatric speciation ofHarpagiferacross the Southern Ocean may have generated the diversification ofAliivibriointo patterns recapitulating the host phylogeny.ImportanceAlthough challenging to detect in wild populations, phylogenetic congruence between marine fish and its microbiome is critical, as it allows highlighting potential intimate associations between the hosts and ecologically relevant microbial symbionts.Through a natural system consisting of closely related fish species of the Southern Ocean, our study provides foundational information about the contribution of host evolutionary trajectory on gut microbiome assembly, that represents an important yet underappreciated driver of the global marine fish holobiont. Notably, we unveiled striking evidence of co-diversification betweenHarpagiferand its microbiome, demonstrating both phylosymbiosis of gut bacterial communities, and co-phylogeny of specific bacterial symbionts, in patterns that mirror the host diversification. Considering the increasing threats that fish species are facing in the Southern Ocean, understanding how the host evolutionary history could drive its microbial symbiont diversification represents a major challenge to better predict the consequences of environmental disturbances on microbiome and host fitness.