Insights into the circulating microbiome of Atlantic and Greenland halibut populations: the role of species-specific and environmental factors

Abstract

Establishing long-term microbiome-based monitoring programs is critical for managing and conserving wild fish populations in response to climate change. In most cases, these studies have been conducted on gut and, to a lesser extent, skin (mucus) microbiomes. Here, we exploited the concept of liquid biopsy to study the circulating bacterial microbiome of two Northern halibut species of economic and ecological importance. Amplification and sequencing of the 16S rRNA gene were achieved using a single drop of blood fixed on FTA cards to identify the core blood microbiome of Atlantic and Greenland halibut populations inhabiting the Gulf of St. Lawrence, Canada. We provide evidence that the circulating microbiome DNA (cmDNA) is driven by genetic and environmental factors. More specifically, we found that the circulating microbiome signatures are species-specific and vary according to sex, size, temperature, condition factor, and geographical localization. Overall, our study provides a novel approach for detecting dysbiosis signatures and the risk of disease in wild fish populations for fisheries management, most notably in the context of climate change.

Divergent bacterial landscapes: unraveling geographically driven microbiomes in Atlantic cod

“…At the phylum level, the blood microbiome signature was dominated by Proteobacteria , Bacteroidetes , Acidobacteria and Actinobacteria. Apart from a few minor differences, particularly concerning the lower prevalence of Firmicutes , this taxonomic structure at the phylum level was similar to that recently described in the circulating microbiome of the Greenland halibut ( Reinhardtius hippoglossoides ) and Atlantic halibut ( Hippoglossus hippoglossus ) in the Gulf of St. Lawrence 20 . However, we could distinguish two populations with distinct blood microbiome signatures at the lower ranks.…”

“…An ASV was considered part of the core microbiome if it had a minimum prevalence (rate of presence in the group of samples) of 70%, with a detection threshold of 0.01% relative abundance, as described by Palanisamy and colleagues 27 . A similar decision tree was applied for the core genera (abundance of ASVs of the same genus summed up) but with 90% prevalence and a detection threshold of 0.01%, as described by Fronton and colleagues 20 .…”

“…Recent studies have applied this concept to marine species, including invertebrates and fish populations 18 , 19 . For example, using a single drop of blood fixed on cellulose paper, we recently reported that the circulating microbiome signature of wild halibut populations is sensitive to physiological and environmental factors 20 .…”

A niche-adapted brain microbiome in salmonids at homeostasis

“…Presence of bacteria in the healthy brain is a matter of debate (16)(17)(18)(19)(20). Under physiological conditions, culturable bacteria can be recovered from the blood and other internal organs of teleosts (11,13). Thus, we sought to investigate if the teleost brain is also colonized by bacteria at the steady state.…”

“…For instance, culturable bacteria could be recovered from the blood and kidney of healthy salmonids ( 11 ); the biological and functional significance of this observation is still unexplored. More recently, the microbial communities from the spleen of healthy and diseased tilapia were sequenced ( 12 ), and blood microbiomes have been proposed as a health biomarker in halibut ( 13 ). This peculiar relationship between teleosts and systemic bacteria is further illustrated by the lack of an endotoxic shock response to lipopolysaccharide injection, a 60-year-old observation that further underscores that teleost internal organs coexist with bacteria ( 14 , 15 ).…”