Longitudinal sampling of external mucosae in farmed European seabass reveals the impact of water temperature on bacterial dynamics

Abstract

Fish microbiota are intrinsically linked to health and fitness, but they are highly variable and influenced by both biotic and abiotic factors. Water temperature particularly limits bacterial adhesion and growth, impacting microbial diversity and bacterial infections on the skin and gills. Aquaculture is heavily affected by infectious diseases, especially in warmer months, and industry practices often promote stress and microbial dysbiosis, leading to an increased abundance of potentially pathogenic bacteria. In this regard, fish mucosa health is extremely important because it provides a primary barrier against pathogens. We used 16 rRNA V4 metataxonomics to characterize the skin and gill microbiota of the European seabass, Dicentrarchus labrax, and the surrounding water over 12 months, assessing the impact of water temperature on microbial diversity and function. We show that the microbiota of external mucosae are highly dynamic with consistent longitudinal trends in taxon diversity. Several potentially pathogenic genera (Aliivibrio, Photobacterium, Pseudomonas, and Vibrio) were highly abundant, showing complex interactions with other bacterial genera, some of which with recognized probiotic activity, and were also significantly impacted by changes in temperature. The surrounding water temperature influenced fish microbial composition, structure and function over time (days and months). Additionally, dysbiosis was more frequent in warmer months and during transitions between cold/warm months. We also detected a strong seasonal effect in the fish microbiota, which is likely to result from the compound action of several unmeasured environmental factors (e.g., pH, nutrient availability) beyond temperature. Our results highlight the importance of performing longitudinal studies to assess the impact of environmental factors on fish microbiotas.

Temporal changes in skin and gill microbiomes of Atlantic salmon in a recirculating aquaculture system – Why do they matter?

“…The occurrence of dysbiosis could potentially be a direct consequence of the short photoperiod, associated with changes in osmoregulatory physiology known to accompany smoltification or the result of an interaction between environmental and host factors. For example, water temperature is also a strong predictor of microbiome dynamics with dysbiotic events and associated proliferation of potentially pathogenic taxa associated with warmer temperatures or shifts from cold to warm temperatures annually (Rosado et al, 2021). Indeed, in the current study, a period of increased FW rearing water temperature coincided with a reduction in microbial diversity in both water and external mucosa.…”

“…In addition, fish are in constant contact with external environments which are rarely stable. Microbiome composition is sensitive to a number of environmental factors including temperature (Rosado et al, 2021), salinity (Lokesh and Kiron, 2016;Dehler et al, 2017), rearing system (Minich et al, 2020a), stress (Boutin et al, 2013;Minniti et al, 2017), as well as factors associated with host biology including developmental stage (Lokesh et al, 2019;Heys et al, 2020) and body site (Uren Webster et al, 2018;Minich et al, 2020a).…”

“…Many of the previous studies have focussed on a single time point, which would assume a stable microbial community. Year-long temporal analyses in pond-reared European seabass (Rosado et al, 2021) and wild marine Pacific chub mackerel (Minich et al, 2020b) identified highly dynamic external microbiomes impacted strongly by water temperature. In this study we analyse the temporal dynamics of the gill and skin microbiomes in Atlantic salmon in a commerical RAS, considered a stable system, and post-seawater transfer (SWT).…”

Fish disease and intestinal microbiota: A close and indivisible relationship

“…Fish microbial composition and structure are driven by intrinsic and extrinsic factors, including antibiotic administration or any other chemical additive to improve hygiene in animals, a deficient diet and the physiochemical properties of the water. 41,204,205 6.1 | Antibiotic treatment Antibiotic treatment, typically used in aquaculture to prevent diseases, is one of the most potent factors that can lead to a microbial imbalance. 166,206 Antibiotics can produce adverse effects on mammals' health, such as increased levels of secretory-IgA, upregulation of the antimicrobial lectin Reg3g, toll-like receptors and downregulation of the antimicrobial peptide Resisting-like Molecule-b.…”

“…However, there are different factors besides pathogens that may induce dysbiosis in fish (Figure 3). Fish microbial composition and structure are driven by intrinsic and extrinsic factors, including antibiotic administration or any other chemical additive to improve hygiene in animals, a deficient diet and the physiochemical properties of the water 41,204,205 …”