Unveiling the co-phylogeny signal between plunderfish Harpagifer spp. and their gut microbiomes across the Southern Ocean

Author:

Schwob Guillaume123ORCID,Cabrol Léa134ORCID,Saucède Thomas5,Gérard Karin167,Poulin Elie123,Orlando Julieta12

Affiliation:

1. Millennium Institute Biodiversity of Antarctic and Subantarctic Ecosystems (BASE), Santiago, Chile

2. Department of Ecological Sciences, Faculty of Sciences, University of Chile, Santiago, Chile

3. Institute of Ecology and Biodiversity, Santiago, Chile

4. Aix Marseille University, Univ Toulon, CNRS, IRD, Mediterranean Institute of Oceanography (MIO) UM 110, Marseille, France, Marseille, France

5. UMR 6282 Biogeosciences, University Bourgogne Franche-Comté, CNRS, EPHE, Dijon, France

6. Laboratory of Antarctic and Subantarctic Marine Ecosystems, Faculty of Sciences, University of Magallanes, Punta Arenas, Chile

7. Cape Horn International Center, Puerto Williams, Chile

Abstract

ABSTRACT Understanding the factors that sculpt fish gut microbiome is challenging, especially in natural populations characterized by high environmental and host genomic complexity. However, 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 propose that the recent diversification of several Harpagifer species across the Southern Ocean would allow 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 plunderfish Harpagifer (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 in Harpagifer gut mucosa. The core microbiome of Harpagifer spp. gut mucosa was characterized by a low diversity, mostly driven by selective processes, and dominated by a single Aliivibrio Operational Taxonomic Unit (OTU) detected in more than 80% of the individuals. Nearly half of the core microbiome taxa, including Aliivibrio , harbored co-phylogeny signal at microdiversity resolution with host phylogeny, indicating an intimate symbiotic relationship and a shared evolutionary history with Harpagifer . The clear phylosymbiosis and co-phylogeny signals underscore the relevance of the Harpagifer model in understanding the role of fish evolutionary history in shaping the gut microbiome assembly. We propose that the recent diversification of Harpagifer may have led to the diversification of Aliivibrio , exhibiting patterns that mirror the host phylogeny. IMPORTANCE Although challenging to detect in wild populations, phylogenetic congruence between marine fish and its microbiome is critical, as it highlights intimate associations between hosts and ecologically relevant microbial symbionts. Our study leverages a natural system of closely related fish species in the Southern Ocean to unveil new insights into the contribution of host evolutionary trajectory on gut microbiome assembly, an underappreciated driver of the global marine fish holobiont. Notably, we unveiled striking evidence of co-diversification between Harpagifer and its microbiome, demonstrating both phylosymbiosis of gut bacterial communities and co-phylogeny of some specific bacterial symbionts, mirroring the host diversification patterns. Given Harpagifer ’s significance as a trophic resource in coastal areas and its vulnerability to climatic and anthropic pressures, understanding the potential evolutionary interdependence between the hosts and its microbiome provides valuable microbial candidates for future monitoring, as they may play a pivotal role in host species acclimatization to a rapidly changing environment.

Funder

ANID FONDECYT Postdoctoral Project

ANID FONDECYT Regular Project

ANID-Millenium Science Initiative Program

Publisher

American Society for Microbiology

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