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

Abstract

The establishment of long-term microbiome-based monitoring programs is critical for the management and conservation of 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 was 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 both species-specific 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 the detection of dysbiotic 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 dual microbiomes in Atlantic cod (Gadus morhua) from the southern Gulf of St. Lawrence

“…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.…”

“…The presence of Nitrobacter and Sediminibacterium in population A contrasted with the microbiome pro le of population B, where we found DNA derived from Pseudoalteromonas, a genus of marine bacteria commonly found in marine species, such as sponges, shell sh, macroalgae and sh, including wild sh populations of the Greenland halibut and Atlantic halibut of the Gulf of St. Lawrence [20,[54][55][56][57]. Considered a mutualistic bacterium that plays a vital role in the tness and survival of its host, this genus is known to adapt well to cold environments.…”

“…In medicine, the characterization of the peripheral blood-derived microbiome signature, de ned as blood microbial DNA, is increasingly used by clinicians to assess an individual's health status, detect dysbiosis and potential pathogens, or as a biomarker to inform disease severity and progression [33][34][35][36][37]. This concept is also gaining momentum in ecology as the circulating microbiome of dogs, bovine, wild birds and wild sh populations were recently studied, showing that the genetic structure of the blood microbiome, just as in humans, is modulated by genetic and spatiotemporal factors, as well as disease conditions [20,[38][39][40][41]. In the present study, the observed shift toward the dominance of Nitrobacter and Sediminibacterium suggests that environmental factors severely impact the blood microbiome signature.…”

“…For example, using a single drop of blood xed 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

“…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 ).…”