Full length articleHot water extract of Pleurotus pulmonarius stalk waste enhances innate immune response and immune-related gene expression in red hybrid tilapia Oreochromis sp. following challenge with pathogen-associated molecular patterns
Graphical abstract
Introduction
Aquaculture is growing exponentially in most countries to meet the high global demand for aquatic food product. To date, aquaculture accounted for 52% of fish to the food-producing sector worldwide, with the value of about USD 250 billion [1]. In aquaculture, fish are usually reared in high density and overcrowded environment such as in cages, tanks or ponds to boost the production in a short period of time [2]. However, this stressful environment may cause adverse effects to the fish's health and increase chances of disease spreading. The outbreak of infectious diseases is one of the major aquaculture production issues faced by fish farmers, as it reduces productivity and causes huge economic loss [3]. Generally, antibiotics and chemotherapeutics are used to halt these infections in aquaculture [4]. However, due to the development of antibiotics-resistant bacteria, accumulation of antibiotic residue and rising concern on the consumer liability, fish farmers are encouraged to reduce the usage of antibiotics and chemotherapeutics in aquaculture [5].
Recently, the use of immunostimulants, such as mushroom polysaccharides, as an alternative approach to improve the immune system and disease resistance in fish is widely reported. Mushrooms contain various types of polysaccharides such as α- and β-glucans, mannans, galactans, xylans, chitin, and hemicellulose [6]. Among these polysaccharides, β-glucans gained the most attentions and has been identified as the major bioactive compounds that possess immunomodulatory, anti-inflammatory, antioxidant, anti-tumour, antimicrobial and antiviral properties [7]. The administration of mushroom polysaccharides to various fish species has been shown to stimulate the non-specific immune responses like phagocytic activity, respiratory burst activity, alternative complement activity and lysozyme activity [8,9] Furthermore, many studies have reported that mushroom polysaccharides supplementation increased the survival rate and disease resistance of fish against bacterial infections [10,11]. Mushroom polysaccharides were also able to modulate the expression of several immune-related genes that encode for proteins such as IL-1β, TNF-α, IL-10 and IFN-γ in different immune organs of fish [12,13].
In this study, oyster mushroom Pleurotus pulmonarius was used as the source of mushroom polysaccharides. Oyster mushroom is not only an edible mushroom, but also used as a medicinal mushroom due to presence of biologically active compounds such as glucans, vitamin C and phenol [14]. Due to the high consumption worldwide, the cultivation of oyster mushroom has gained popularity in the Asian countries. The mature fruiting bodies of oyster mushrooms are harvested as the commercial edible part. However, the mushroom stalk waste (MSW), which is the end part of the fruiting body embedded in the sawdust substrate, are not consumed and are discarded. As the mushroom industries are growing exponentially, the volume of MSW is rapidly increasing in these years. Therefore, the disposal of MSW is becoming one of the critical problems in mushroom industries [15]. In the previous study, fish feed supplemented with MSW extracts that contain high level of polysaccharides were shown to enhance the growth performance, antioxidant enzyme activities, and survival rate of Nile tilapia Oreochromis niloticus fingerlings under stressed condition like pH fluctuation [15,16]. Moreover, Nile tilapia fed with the spent mushroom substrate of Cordyceps militaris was also shown to have an improved innate immune parameters and disease resistance against Streptococcus agalactiae [17]. Therefore, the administration of the undesirable mushroom part (MSW) as dietary supplement in fish are thought to be able to enhance the health status and immune system of fish.
Tilapia Oreochromis sp. is one of the most important farmed fish in aquaculture as it provides high nutrition animal protein and contributes to food security when the global population keep increasing [18]. Like other fish species, farmed tilapia can also be easily infected by various pathogenic organisms such as Streptococcus, Aeromonas and Tilapia Lake Virus [19]. To our knowledge, limited works have been reported on the usage of Pleurotus stalk waste extract in fish feed, in order to enhance the immune system of fish. Thus, this study was carried out to evaluate the effect of hot water extract (HWE) of MSW as a fish feed supplement on the immune response of red hybrid tilapia Oreochromis sp. following intraperitoneal challenge with pathogen-associated molecular pattern (PAMPs) such as lipopolysaccharides (LPS) and polyinosinic:polycytidylic acid (poly (I:C)). This study could provide a better understanding in the effects of HWE on the immune responses of fish upon PAMPs stimulation, as well as the growth performance after HWE supplementation.
Section snippets
Preparation of hot water extract
Oyster mushroom stalk waste (MSW) was collected from Arra Mushroom Sdn Bhd, Negeri Sembilan, Malaysia. The MSW (Fig. 1.) was washed using clean tap water and then oven-dried at 60 °C for 4 h to remove the water content. The oven-dried sample was ground in a blender and stored at 4 °C until further use. The hot water extraction procedure began with the boiling of the ground MSW using distilled water (1:20 w/v) for 5 h. The boiled sample was then cooled at room temperature and filtered twice
Proximate composition of hot water extract
Estimated chemical composition of HWE was shown in Table 3. Since the extraction was water based, HWE was mainly composed of water-soluble carbohydrate and protein. Lipid on the other hand, made up of less than 1% of the total composition.
Estimation of β-glucan
Out of 42.91% of total carbohydrate, about half of it was glucan which made up of 24.81% of total HWE composition. The glucan was mainly in β-form which was 22.44% of total HWE, while the α-glucan was remarkably low (2.37%).
Toxicity evaluation of HWE-supplemented feed
The toxicity of HWE-supplemented
Discussion
Incorporation of polysaccharide, particularly β-glucan, in animal feed has gained interest in animal feed research. Inducing resistance towards infections in livestock would definitely benefit the farmers. However, adding costly pure immunostimulatory compounds such as β-glucan into the feed would increase the cost of feed production. With the aim to reduce the production cost of fish feed with immunomodulatory activity, this study was carried out to observe whether crude extraction of
Conclusion
In conclusion, our results showed that HWE supplementation did not have significant effect on the body weight gain and specific growth rate of red hybrid tilapia, but clearly imply a positive effect on the feed utilisation compared to the basal diet. Furthermore, administration of HWE could enhance the innate immune parameters and serum bactericidal activity against S. agalactiae in red hybrid tilapia. Results of the immune-related gene expression revealed that HWE supplementation could
CRediT authorship contribution statement
Joo Jie Ching: Visualization, Investigation, Writing – original draft, preparation. Adawiyah Suriza Shuib: Conceptualization, Methodology, Supervision, Project administration, Writing – review & editing. Noorlidah Abdullah: Conceptualization, Methodology, Resources. Nazia Abdul Majid: Data curation, Writing – review & editing. Norhidayah Mohd Taufek: Data curation, Writing – review & editing. Jumria Sutra: Investigation. Mohammad Noor Amal Azmai: Resources, Writing – review & editing.
Declaration of competing interest
The authors declare that there are no conflicts of interest associated with this publication.
Acknowledgement
This research was financially supported by the Fundamental Research Grant Scheme (FRGS/1/2018/STG05/UM/02/3) from Ministry of Higher Education, Malaysia.
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