The ecology and plasticity of fish skin and gill microbiomes: seeking what matters in health and disease

Abstract

The microbiomes of skin and gill mucosal surfaces are critical components in fish health and homeostasis by competitively excluding pathogens, secreting beneficial compounds, and priming the immune system. Disruption of these microbiomes can compromise their capacity for disease resilience and maintaining host homeostasis. However, the extent and nature of microbiome disruption required to impact fish health negatively remains poorly understood. This review examines how various stressors influence the community composition and functionality of fish skin and gill microbiomes, and the subsequent effects on fish health. Our findings highlight that the impact of stressors on skin and gill microbiomes may differ for different body sites and are highly context-dependent, influenced by a complex interplay of host-specific factors, stressor characteristics, and environmental conditions. By evaluating current knowledge on the genesis and homeostasis of these microbiomes, we highlight a strong influence of environmental factors especially on skin and gill microbiomes compared with fish gut microbiomes, which appear to be more closely regulated by the host's homeostatic and immunological systems. This review emphasizes the importance of understanding the ecology and plasticity of fish skin and gill microbiomes to identify critical thresholds for microbiome shifts that impact fish health and disease resilience.

Keywords: animal health; aquaculture; dysbiosis; environment; immune; mucous; stressor.

Figure 1.

Host-immune factors influencing the microbiota in the skin mucosal microbiome. (A) TLRs recognize microbe-associated molecular patterns, activating proinflammatory signalling cascades (MyD88) and transcription factors (NF-κB) to prime the immune system whilst also preventing excessive inflammation through negative feedback mechanisms. (B) Mucosal microbiomes may harbour transient taxa from the aquatic environment, potentially colonizing if mucosal conditions change. (C) Microbes adapted to mucosal niche conditions successfully colonize the host microbiome under niche appropriation theory, regardless of rarity in the surrounding environment. (D) Secretory IgT binds commensals and pathogens in skin mucous, preventing migration into subepithelial structures. (E) Secretory mucins bind and confine microbes to the mucosal layer, influenced by variable glycosylation patterns. (F) Somatic mutations of B- and T-cell receptors during development lead to the creation of unique sets of immune receptors for each individual, shaping microbiota selection. Other innate immune components that can contribute to shaping mucosal microbiome compositions include antimicrobial peptides, macrophages, and lysozymes. Created with BioRender.

Figure 2.

Microbiome shifts impacting animal health. Left-hand side (LHS): stressor-induced microbiome shifts depend on three factors: (1) stressor characteristics—duration and intensity must be sufficient to cause change. (2) Host individuality—each host’s unique microbiome affects its susceptibility and resilience to shifts, influenced by factors such as age, species, and immune status. (3) Environmental conditions—factors such as temperature, pH, and diurnal/seasonal patterns can impose selective pressures on mucosal physiology. The aquatic environment also acts as a reservoir for potential pathogens that exploit microbiome shifts. Right-hand side (RHS): the impact of stressors, the host, and/or environmental conditions may vary depending on the relative strength of the stressor/environmental condition and susceptibility of the host (indicated as low, medium, or high). Even a low strength stressor can alter microbiome functionality if the host is highly susceptible, or the environment amplifies the effect. Health outcomes decline only if microbiome functionality is disrupted.

Figure 3.

Stress-induced perturbations of fish skin and gill microbiomes. (1) Stressors can shift a microbiome from one stable state to another. (2) In this new state, microbial composition changes, often with an increase in pathobionts and a decrease in commensals, but overall functionality for maintaining health is preserved. This stable state resists reversion due to the high ‘conceptual’ energy required for the shift. (3) Despite functional resilience, altered microbiomes may become more vulnerable to disease, as the ‘conceptual’ energy needed to push the system into dysbiosis is reduced. Subsequent stressors may trigger this transition, leading to disease onset.