Full length articleAntioxidant and immune responses of the Oriental river prawn Macrobrachium nipponense to the isopod parasite Tachaea chinensis
Introduction
Parasitic isopods are widely distributed across a diverse range of habitats, including freshwater, brackish water, and marine environments [[1], [2], [3]]. They are unique in using fish and crustaceans as both intermediate and definitive hosts, and feed on the blood, mucus, and tissue of hosts using specialized mouthparts [[4], [5], [6]]. As vectors of other disease, they can predispose hosts to opportunistic pathogens, including viruses, bacteria, fungi, and other parasites [7,8]. Parasitic isopod infections in commercial aquacultured fish and crustaceans can result considerable economic losses [[9], [10], [11]]. Isopod parasites can stunt growth, or injure and kill their hosts due to nutrient deprivation and destruction of the defense system, but aspects of crustacean host defense remain poorly understood.
Tachaea chinensis, a common isopod ectoparasite of economically important shrimp species, is widely distributed in Asia [11,12], and parasitizes various cultured shrimps, including Palaemonetes sinensis, Exopalaemon carinicauda, Litopenaeus vannamei, and Macrobrachium nipponense [11]. We previously found that T. chinensis secretes antihemostatic, anti-inflammatory, and immunomodulatory molecules to facilitate blood meal acquisition and inhibit the shrimp immune system during parasitism [6]. However, immune-related genes and proteins in shrimp hosts are not significantly affected after a 14-day exposure to parasitism (midterm infection) [6,13,14]. It has been widely established that immune responses in fish hosts are markedly influenced by ectoparasite exposure duration, and that the ability to suppress and reject parasites shortly after infection can be associated with innate immunity. This is particularly important as it can substantially influence subsequent immune progress [[15], [16], [17], [18]]. However, the early immune responses of crustaceans against isopod ectoparasite infection have yet to be clarified.
The Oriental river prawn M. nipponense is an economically and nutritionally important species, and is considered one of the most important freshwater prawns for aquaculture in China, Korea, Vietnam, and Japan [19]. As an extensively cultured and popularly consumed species, the annual production of M. nipponense in China has gradually increased in recent years to about 234,358 tons in 2018 with an annual output value of >20 billion RMB (2.8 billion USD). It has become an important means of increasing agricultural efficiency and farmers' incomes [20]. However, recent studies have shown that T. chinensis has parasitized both aquacultured and wild M. nipponense in China and neighboring countries [11,12]. Our knowledge of the immune responses of M. nipponense their roles in protection against parasites is limited. Many studies indicate that antioxidant and immune related enzymes including superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), malondialdehyde (MDA), lysozyme (LZM), phenol oxidase (PO), acid phosphatase (ACP), and alkaline phosphatase (AKP) represent the first line of defense in nonspecific immune responses in crustacean [21,22]. In this study, we evaluated these nonspecific immune defense responses during the early infection period by investigating the activity of antioxidant defense enzymes. We also performed transcriptome analysis to determine the integrated molecular mechanisms underlying T. chinensis parasitism of M. nipponense and the resultant host responses.
Section snippets
Animals and sample collection
M. nipponense individuals (weight: 1.86 ± 0.44 g, length: 4.45 ± 0.57 cm) were purchased from a local aquaculture market in Shenyang City, Liaoning Province, China. T. chinensis (weight: 0.04 ± 0.01 g, length: 1.12 ± 0.23 cm) were collected from a rice field in Panjin City, Liaoning Province, China. Both prawns and parasites were acclimatized in an aerated recycling freshwater system. The water temperature was maintained at 22 ± 0.5 °C and with a light:dark cycle of 12:12 h. After acclimation
Survival, molting, total weight loss, and daily weight loss during parasite exposure
The survival rate was observed to decrease with increasing exposure duration (Fig. 1A). After 15 days, survival reached approximately 70%, whereas the molt rate increased continuously throughout exposure to approximately 55%. Total weight loss increased by 8% at day 3 but was not significantly different compared with that at the other assessed time points (Fig. 1B). However, the rate of daily weight loss decreased with an increase in exposure duration and was significantly higher at 3 days than
Discussion
Numerous studies have indicated that ectoparasitic isopods feed on host blood (hemolymph) and exudates, eventually resulting in host death or weight loss [3,[23], [24], [25]]. Here, we found that the mortality rate of M. nipponense increased concomitantly with infection duration, and reached 30% after 15 day of T. chinensis parasitism. We previously observed that T. chinensis parasitism can cause 50% mortality in the Chinese grass shrimp Palaemonetes sinensis after infection for 2 weeks [6,13,26
Conclusions
In this study, we provide the first findings indicating that the isopod parasite T. chinensis can adversely affect the antioxidant and immune systems of its shrimp host M. nipponense. Notably, multiple enzymes and genes associated with the antioxidant and immune systems, including SOD, MDA, AKP, ACP and GST, exhibited patterns characterized by an initial increase and subsequent decrease in response to infection, suggesting that parasitism could perturb these host defense systems during the
CRediT authorship contribution statement
Yingdong Li: Writing - original draft, Writing - review & editing. Zhibin Han: Writing - original draft. Weibin Xu: Formal analysis, Investigation. Xin Li: Formal analysis, Investigation. Yingying Zhao: Data curation. Hua Wei: Data curation. Xiaodong Li: Resources. Qijun Chen: Writing - review & editing, Supervision, Project administration, Funding acquisition.
Declaration of competing interest
The authors declare no conflicts of interest.
Acknowledgments
This work was supported by the earmarked fund for Modern Agro-industry Technology Research System (No. CARS-48), the Liaoning Provincial Natural Science Foundation of China (No. 2019MS274), and the Talent Introduction Program of Shenyang Agricultural University (No. 880417024). We thank Panjin Guanghe Fisheries Co. Ltd for providing shrimps and parasites.
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These authors contributed equally to the study.