Full length articleResponse of gut health and microbiota to sulfide exposure in Pacific white shrimp Litopenaeus vannamei
Introduction
The animal gut is a vital organ for food storage, digestion and nutrient absorption [1]. Additionally, the gut plays a role in immune function together with symbiotic bacteria and serves as a biochemical barrier to contain gastric acid and glycoprotein [2]. The integrity and the inflammatory status of the animal gut have been used to evaluate the gut health status of animals [3]. Usually, a normal gut has closely arranged epithelial cells, a clear intercellular space, an inner wall of columnar epithelial tissue, and villi with an integrated structure [4]. The intestinal epithelial cells separate the basement membrane and will disintegrate if the gut wall is damaged [5]. In addition, a functional and stable gut microbiota is important to the host's health, as the gut microbiota can perform beneficial functions to the host such as balancing the immune response, absorbing nutrients, and maintain homeostasis [6]. Previous studies have shown that manipulation of the microbial composition in the gut of farmed fish and crustaceans can have a marked effect on animal health, growth, and survival [7]. Previous studies have shown that the gut microbiota can contribute to the absorption of fatty acids and the formation of lipid droplets in the intestinal epithelium of zebrafish [8]. Additionally, feeding Epinephelus coioides a diet containing Bacillus subtilis E20 improved growth, innate immune response, and disease resistance [9]. It has been proposed that modulating the gut microbiota will be a clean, ecological and prospective technology in dealing with the challenge of shrimp disease [10]. Therefore, the maintenance of gut physiological function in an animal is of significance for the growth and development of aquatic animals.
Many factors, such as water quality, infection with pathogenic bacteria or virus, and diet composition, can affect the gut health of aquatic animals [11], [12], [13], [14]. Among these factors, water quality can directly impact the gut health of aquatic animals [15], as some toxicants are generated from the intensive aquaculture system [16]. Sulfide is one of these toxicants. It has been associated with fish farming and can affect mitochondrial respiration through the inhibition of cytochrome C oxidase [17], [18] and lead to a condition favorable for bacterial proliferation [19]. Previous studies have found that sulfide can potentially threaten the gut health of aquatic animals [20] and shape the composition of the gut microbiota [21]. However, our understanding regarding the toxic effect of sulfide on the gut health of aquatic animals is still limited. There is a need for further systematic investigation.
Sulfide can be accumulated in an aquatic environment when organic material is decomposed under anaerobic conditions. It is commonly found in the interface between the water and sediment in the aquatic environment [22]. Therefore, the species dwelling in the benthic zone on the bottom of a pond are susceptible to sulfide exposure and toxicity. The Pacific white shrimp Litopenaeus vannamei starts benthic life soon after the mysis stage, or the early stage of post larvae. Therefore, L. vannamei is inevitably affected by exposure to sulfide released from the pond sediment. However, our understanding of the effect of sulfide toxicity on L. vannamei is limited to its immune response and its susceptibility to Vibrio alginolyticus under sulfide stress [13].
In this study, we aimed to examine the impact of sulfide on L. vannamei from the perspectives of gut histology, expression of inflammatory and immune related factors (TNF-α, CTL3, MSTN and HSF1), and the microbiota under chronic, sub-lethal concentrations of sulfide. The lethal concentration (LC50) of sulfide for L. vannamei was pre-determined for 96 h, which provided the basis for choosing the concentration of sulfide used in the present study. The results of this study will provide insight into our understanding of the mechanism of sulfide toxicity for L. vannamei.
Section snippets
Experimental shrimp
Juvenile Pacific white shrimp L. vannamei (3.2 ± 0.16 g) were obtained from South China Sea Fisheries Research Institute in Shenzhen, China. L. vannamei were acclimated at a salinity of 25 psu for one week prior to the start of the experiment. Seawater together with the tap water from Dayawan, Shenzhen was filtered through an activated carbon cartridge for at least three days before use. During the experiment, the water quality parameters in the experiment were maintained at a temperature of
Gut histology
The epithelial cells of the shrimp intestine in the control were arranged closely with a clear cell gap, and the intestinal walls were found to be composed of tissues with a tall, columnar epithelium (Fig. 1-a). There were spaces between the partial intestinal and epithelial cells in shrimp exposed to low sulfide at 425.5 μg/L, and part of the intestinal epithelial cells were disassociated from the basement membrane (Fig. 1-b). The intestinal epithelial cells of shrimp exposed to the high
Discussion
Field investigations have established that sulfide is often present in natural aquatic ecosystems at levels that are toxic to fish and invertebrates [11]. In this study, sulfide exposure led to the injury of the L. vannamei gut, and this intestinal damage intensified with increasing sulfide concentration. The damaged gut in L. vannamei can be related to the toxic mechanism of sulfide to animals. Sulfide inhibits the activity of cytochrome C oxidase, causing damage to aerobic respiration and
Acknowledgements
This study was supported by grants from the Agriculture Ministry Key Laboratory of Healthy Freshwater Aquaculture, the Key Laboratory of Freshwater Aquaculture Genetic and Breeding of Zhejiang Province of the Zhejiang Institute of Freshwater Fisheries (ZJK201503), and the National Natural Science Foundation of China (No. 31472291).
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