Metagenomic Shotgun Analyses Reveal Complex Patterns of Intra- and Interspecific Variation in the Intestinal Microbiomes of Codfishes

Abstract

The relative importance of host-specific selection or environmental factors in determining the composition of the intestinal microbiome in wild vertebrates remains poorly understood. Here, we used metagenomic shotgun sequencing of individual specimens to compare the levels of intra- and interspecific variation of intestinal microbiome communities in two ecotypes (NEAC and NCC) of Atlantic cod (Gadus morhua) that have distinct behavior and habitats and three Gadidae species that occupy a range of ecological niches. Interestingly, we found significantly diverged microbiomes among the two Atlantic cod ecotypes. Interspecific patterns of variation are more variable, with significantly diverged communities for most species’ comparisons, apart from the comparison between coastal cod (NCC) and Norway pout (Trisopterus esmarkii), whose community compositions are not significantly diverged. The absence of consistent species-specific microbiomes suggests that external environmental factors, such as temperature, diet, or a combination thereof, comprise major drivers of the intestinal community composition of codfishes. IMPORTANCE The composition of the intestinal microbial community associated with teleost fish is influenced by a diversity of factors, ranging from internal factors (such as host-specific selection) to external factors (such as niche occupation). These factors are often difficult to separate, as differences in niche occupation (e.g., diet, temperature, or salinity) may correlate with distinct evolutionary trajectories. Here, we investigate four gadoid species with contrasting levels of evolutionary separation and niche occupation. Using metagenomic shotgun sequencing, we observed distinct microbiomes among two Atlantic cod (Gadus morhua) ecotypes (NEAC and NCC) with distinct behavior and habitats. In contrast, interspecific patterns of variation were more variable. For instance, we did not observe interspecific differentiation between the microbiomes of coastal cod (NCC) and Norway pout (Trisopterus esmarkii), whose lineages underwent evolutionary separation over 20 million years ago. The observed pattern of microbiome variation in these gadoid species is therefore most parsimoniously explained by differences in niche occupation.

Characterization and comparison of the digestive physiology of two scombrids, Katsuwonus pelamis and Sarda sarda, in the Gulf of Cádiz

“…Results suggest that species-specific selection, but also environmental factors comprise the major drivers of the intestinal community composition of the skipjack tuna. This intra-specific variability in the bacterial relative abundance has been also described for other fish species such as the grey mullet ( Mugil cephalus ) [ 70 ] and codfishes [ 71 ]. Tenericutes has been also identified as the dominant gut community in the southern bluefin tuna and king mackerel, while Firmicutes in Spanish mackerel [ 65 , 68 ], suggesting that both phyla are part of the microbiota of scombrids.…”

Effects of Thermal Stress on the Gut Microbiome of Juvenile Milkfish (Chanos chanos)

“…However, given the strong documented interactions between host and gut microbiome [20] it appears unlikely that temperature alone would determine gut microbiome composition. Yet, temperature may modulate physiological effects on the gut microbiome [88]. Similarly, additional environmental factors would need to be considered in a coastal aquaculture setting, where the majority of the milkfish production is taking place in open cages or pens [3].…”

Response of gut microbiota to feed‐borne bacteria depends on fish growth rate: a snapshot survey of farmed juvenile Takifugu obscurus

“…On the other hand, unlike the pond water and sediment, the feed and gut are inherently linked by the high nutrient niche, which might impose a strong environmental selection of microbiota with functional traits linked to copiotroph (De Schryver and Vadstein, 2014 ; Troussellier et al ., 2017 ). Despite the evidences for the broad existence of core gut microbiota, accumulating studies had also showed substantial inter‐individual variation in the gut microbial communities for both cultured (Li, et al ., 2017 ; Perry, et al ., 2020 ) and wild‐captured fish species (Star, et al ., 2013 ; Egerton, et al ., 2018 ; Riiser, et al ., 2020 ). Several factors can contribute to such variability, including environmental filtering either by the host, for example variations between regions of the gastrointestinal tract, state of health and nutrition; or by the rearing environments such as diet (Wong, et al ., 2013 ; Clements, et al ., 2014 ).…”