Elsevier

Fish & Shellfish Immunology

Volume 114, July 2021, Pages 238-252
Fish & Shellfish Immunology

Full length article
Effect of diet enriched with Agaricus bisporus polysaccharides (ABPs) on antioxidant property, innate-adaptive immune response and pro-anti inflammatory genes expression in Ctenopharyngodon idella against Aeromonas hydrophila

https://doi.org/10.1016/j.fsi.2021.04.025Get rights and content

Highlights

  • A 100% in normal fish fed without or with any ABPs diet.

  • Hematology profile significant in both groups fed with 1.0 and 1.5 mg kg-1 ABPs diets.

  • Antioxidant activity significant both groups fed with 1.0 and 1.5 mg kg-1 ABPs diets.

  • Immune activity significant both groups fed with 1.0 mg kg-1 ABPs diets.

  • Immune genes were significantly expression with .0 mg kg-1 ABPs diets.

Abstract

The effect of Agaricus bisporus polysaccharides (ABPs) supplemented diet on growth rate, antioxidant capacity, innate-adaptive immune response, proinflammatory and antiinflammatory genes expression in Ctenopharyngodon idella against Aeromonas hydrophila is reported. In both normal and challenged groups fed with 1.0 and 1.5 mg kg−1 ABPs diets resulted in a significant weight gain and feed intake. The survival was 100% in normal fish fed without or with any ABPs diet; the challenged fish fed with 1.0 mg kg−1 ABPs diet had 98.6% survival. The RBC and WBC counts, Hb, and Hct levels were significant in both normal and challenged groups fed with 1.0 and 1.5 mg kg−1 ABPs diets. A significant increase in total protein and albumin level was observed in both groups fed with 1.0 and 1.5 mg kg−1 ABPs diets. Significant increase in GPx, ROS, GR, GSH, PC, and MnSOD activity was observed in HK of both groups fed with 1.0 and 1.5 mg kg−1 ABPs diets; similarly both groups when fed with the same ABPs diets showed significant Lz, C3, and C4 activity. However, both groups fed with 1.0 mg kg−1 ABPs diet showed significant β-defensin, LEAP-2A, IL-6, and NF-κB P65 mRNA expression. Similarly, IFN-γ2, IL-10, and TNFα mRNA expressions were significant in both groups fed with 1.0 mg kg−1 ABPs diet. The results indicate that both normal and challenged C. idella fed with a 1.0 mg kg−1 ABPs diet had better growth, antioxidant status, immune response, and pro-anti-inflammatory gene modulation against A. hydrophila.

Introduction

More than 70% of the world population (15 million people) depends upon agriculture or allied sub-sectors for their livelihood. Among these, fisheries constitute one of the main economic sources of income; the global agricultural production registered a 14-fold increase (i.e.) 10.8 million metric tons (mmt) when compared to 0.75 mmt in 1950–51, this includes about 6.4% of world's total fish production in 2015–16. Now, India ranks as the 2nd largest aquaculture producer in the world and earns about US$ 5 billion during 2015–16 via exports. Of the total 5.3% Indian Agriculture GDP, fish contributes about 1.1% [1]. In India, Chinese grass carp, Ctenopharyngodon idella is one of the most favored culture species in polycuture; grass carp was first introduced from Hong Kong in 1959 at Cuttack fisheries research station for aquatic weed control in rivers and lakes. It belongs to the genus Ctenopharyngodon that comes under the family Cyprinidae; it is highly amenable for culture; its exclusive herbivorous feeding habit helps control a wide variety of weeds without causing chemical pollution. It has a good market value due to its delicious and high quality protein. The annual global production of grass carp was 5,537,794 tons in 2014 [2]. Simultaneously, bacterial, viral, and parasitic diseases adversely affect fish production. The most common bacterial pathogens include Aeromonas sp., Vibrio sp. Myxococcus sp., Pseudomonas sp., and Flavobacterium sp., which slice down the harvest size in carp farming leading to severe economic loss [3].

The rapid development of intensive aquaculture practice also has contributed to the increased incidence and severity of various fish diseases in recent years. Under intensive aquaculture practice, enteritis is a major cause of high mortality in farmed fish leading to substantial annual economic losses [4,5]. The grass carp is the most important productive species in Asia; it is also frequently infected with many bacterial, viral, and parasitic diseases under intensive culture conditions. Among these, bacterial enteritis is possibly a major common intestinal disease that infects freshwater fishes including grass carp [[6], [7], [8]]. Among these, Aeromonas hydrophila is mostly considered a major bacterial pathogen in fish, causing intestinal inflammation [8,9].

Fish farmers try to control disease outbreaks using traditional antibiotics and chemotherapy. However, the residues settle down; these pollutant sediments leads to the emergence of drug-resistant strains of pathogens. Vaccines are effective preventive measures against bacterial disease in aquaculture, but it is difficult to develop polyvalent vaccines. In this regard, many bioresearches from plant and animal origin are considered effective preventive measures against fish disease since they are biodegradable and are without any side effect and pollution.

Globally more than 5 million fungal species have been documented recently via modern sequencing [10]. Among these, 3 million species have been recommended for general medical purpose; out of this literature is available only for about 1.5 million species [11]. Around, 2000 species are reported as edible and nearly 650 species are used for pharmaceutical purposes currently [12,13]. A number of scientific clinical studies report that mushrooms are rich in bioactive metabolites and other phytochemicals with anti-cancer, anti-inflammatory, anti-microbial, anti-allergic, anti-diabetic immune-modulatory properties [12,13]. Among these, polysaccharides like chitin and β-glucans from cell walls of plants, fungi or mushrooms are considered the most important active compounds [14]. The fungi or mushrooms contain a large amount of polysaccharides such as β-D-glucans in various forms; among these 1–3,1-6 branching [(1–3)(1–6)beta-d-glucans] are its primary forms. The β-glucans or homopolysaccharides are known to be the most important bioactive polysaccharides in most mushroom species. Each β-D-glucan molecular forms range in size from 1 × 104 to 1 × 106 kDa, which provide various immunomodulatory functions that influence their molecular structures or weight, water solubility, and degree of branching and conformation [15]. It possesses a wide variety of biological activity like anti-obesity, anti-diabetic, anti-carcinogenic, anti-microbial, and anti-viral properties. These demonstrate the polysaccharides act as multiple health-promoting potential which are associated with anti-oxidative, anti-inflammatory, and immunomodulating activities [16]. Few reports are available on the mushrooms or their products on growth performance, physiological function, antioxidant activity, disease resistance, innate-adaptive immune response, and different gene expression in various fishes challenged with different fish pathogens [[17], [18], [19], [20], [21], [22], [23], [24], [25], [26], [27], [28], [29], [30], [31], [32], [33], [34], [35], [36], [37], [38], [39]].

Several reports showed that mushroom and their products possess significant medicinal properties such as immuno-modulation, anti-cancer, anti-oxidant, blood pressure lowering, cholesterol lowering, liner protective, antifibrotic, anti-inflatiory, anti-diabetic, and anti-microbial activities. Mushroom contain rich amount of β-D-glucan that exert an incredible host-mediated immune stimulatory effect in T-cells, which release many cytokines including interleukin (IL)-1β, IL-2, IL-6, interferon-γ (IFN-γ), and tumor necrosis factor-α (TNF-α) [40,41]. Apart from β-D-glucan, a polysaccharide-protein complex (PSPC) extracted from Trametes versicolor is known to augment the immunostimulatory function in T-cells and antigen-presenting cells (APCs) such as macrophages [42] which are effectively inducing T-helper cells to modulate and increase T-helper cell/T-killer cell (CD4+/CD8+) ratio [43]; this result in an enlargement of the spleen [44] which indicates its role in augmenting adaptive immunity. Several works report on the cytotoxic effects of CD8+ and non-cytotoxic CD4+ cells; they are responsible for releasing pro-inflammatory cytokines which recruit effector cells, like macrophages, neutrophils, and eosinophils [45]. TNF-α and IFN-γ are cytokines produced by macrophage and Th cell in response to antigen infections; among these TNF-α is one of the important pro-inflammatory cytokines [46]. Th-1 cells also produce a high level of TNF-α and IFN-γ. Numerous bioactive polysaccharides or polysaccharide protein complexes have been described from medicinal mushrooms. They are known to enhance innate and cell-mediated immune responses, besides exhibiting antitumour activities in animals and humans. For example, mushrooms polysaccharides provide efficient immuno-modulatory expression in various cytokine genes including IL-1α and IL-1β [47].

Recent evidences suggest that mushroom polymers (β-glucans) may trigger many kinds of immune cells in fish, animals, and humans. However, the mechanism of action on growth performance, physiological function, antioxidant, disease resistance, innate-adaptive immune response, and different gene expression in fishes and animals is still not completely understood. The growth of fish is associated with disease resistance and partly related to the status of the immune system. Agaricus bisporus known as the white button mushroom, is the most common edible fungus well documented for its nutritional and bio-medicinal properties. In this backdrop, the present study hypothesizes that an optimal level of A. bisporus polysaccharides (ABPs) may increase growth performance, physiological activity, antioxidant activity, and innate-adaptive immune response such as disease resistance and different gene expression in C. idella against A. hydrophila.

Section snippets

Feed preparation

The basal diet includes fish meal, casein, and gelatin as protein sources, fish oil and soybean oil as lipid sources. A. bisporus polysaccharides (ABPs) powder (10%–50%) was obtained from Xi'an Contri Biological Technology Co. Ltd., Xian, China and used in the feed preparation. The choline chloride was used to provide graded concentrations of 0 g (control diet), 0.5 g, 1.0 g, and 1.5 g kg−1 diets according to Chithra et al. [33]. All ingredients were finely powdered separately in an electric

Growth

The PWG did not vary significantly in the normal fish or challenged fish. However, PWG was high in both normal and normal challenged fish fed with 1.0 and 1.5 g kg−1 ABPs diets as compared with 0.5 g kg−1 ABPs diet. The PI was in normal and challenged fish fed with 1.0 and 1.5 g kg−1 ABPs diets did not vary as compared to fish fed with a 0.5 g kg−1 ABPs diet. The FE did not significantly vary among the experimental groups. The survival rate was 100% in normal fish fed without and with graded

Discussion

Fish growth is very closely associated with disease resistance related to immune function [[60], [61], [62]]. Ganoderma lucidum polysaccharides (GLPs) increased growth rate in grass carp growth [33]. This study reports for the time on the effects of dietary ABPs levels on disease resistance in grass carp. A significant weight gain was recorded in both normal and challenged fish fed with 1.0 and 1.5 g kg−1 ABPs diets than with 0.5 g kg−1 ABPs diet. Normal and challenged fish fed with 1.0 and

Conclusion

Dietary supplementation of ABPs at 1.0 g kg−1 significantly improved fish health, survival rate, disease resistance, and survival by enhancing of antioxidant status, immune response and gene regulation in the immune organs such as HK. It further increased the production of antibacterial compounds such as Lz, IgM, C3, C4, antimicrobial peptides, pro-inflammatory cytokines such as IFN-γ2, IL-1β, IL-10, and TNFα and anti-inflammatory cytokines including IL-10 and IL-11 mRNA expression, as well

Authorship contributions

Ramasamy Harikrishnan: Conception, design, and conduct experiment, Gunapathy Devi: Contribution of data preparation, Hien Van Doan: Contribution to manuscript preparation, Chellam Balasundaram: Contribution to the revision of the manuscript Subramanian Thamizharasan: Contribution for sample collection and reference collection Seyed Hossein Hoseinifar: Contribution to analyse of the data, Mohsen Abdel-Tawwab: Supporting of manuscript revision.

Declaration of competing interest

All authors declare that there are no conflicts of interest in the present study.

Acknowledgements

This research work was partially supported by Chiang Mai University.

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