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

• Published in: Microbiology Spectrum
• Main Authors: Schwob, Guillaume, Cabrol, Léa, Saucède, Thomas, Gérard, Karin, Poulin, Elie, Orlando, Julieta
• Other Authors: Universidad de Chile = University of Chile Santiago (UCHILE), Institut méditerranéen d'océanologie (MIO), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Toulon (UTLN)-Centre National de la Recherche Scientifique (CNRS), Biogéosciences UMR 6282 (BGS), Université de Bourgogne (UB)-Centre National de la Recherche Scientifique (CNRS), Universidad de Magallanes (UMAG)
• Format: Article in Journal/Newspaper
• Language: English
• Published: HAL CCSD 2024
• Subjects: microbiome; phylosymbiosis; co-phylogeny; co-diversification; Harpagifer; Aliivibrio; teleost; Southern Ocean; [SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology; [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]; [SDV.EE.IEO]Life Sciences [q-bio]/Ecology; environment/Symbiosis; [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
• Online Access: https://hal.science/hal-04552885; https://hal.science/hal-04552885/document; https://hal.science/hal-04552885/file/38-schwob_2024_cophylogeny%20Harpagifer-gut-microbiome.pdf; https://doi.org/10.1128/spectrum.03830-23

International audience 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.