Aquaculture 495 (2018) 786–793

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Aquaculture

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Effects of corncob derived xylooligosaccharide on innate immune response, disease resistance, and growth performance in Nile tilapia (Oreochromis T niloticus) fingerlings

Hien Van Doana, Seyed Hossein Hoseinifarb, Caterina Faggioc, Chanagun Chitmanatd, ⁎ Nguyen Thi Maie, Sanchai Jaturasithaa, Einar Ringøf, a Department of Animal and Aquatic Sciences, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand b Department of Fisheries Gorgan, University of Agricultural Sciences and Natural Resources, Gorgan, Iran c Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina Viale Ferdinando Stagno d'Alcontres, 31 98166, S. Agata, Messina, Italy d Faculty of Fisheries Technology and Aquatic Resources, Maejo University, Chiang Mai 50290, Thailand e Department of Aquaculture, Faculty of Fisheries, Vietnam National University of Agriculture, Hanoi, Viet Nam f Norwegian College of Fishery Science, Faculty of Bioscience, Fisheries and Economics, UiT The Arctic University of Norway, Tromsø, Norway.

ARTICLE INFO ABSTRACT

Keywords: An-eight week experiment was conducted to test efficacy of corncob derived xylooligosaccharides (CDXOS) on Corncob mucosal and serum immune, disease resistance, and growth performance of Nile tilapia (Oreochromis niloticus). Xylooligosaccharide Three hundred and twenty tilapia fingerlings (20.72 ± 0.02 g) were fed the following diets; 0 (Diet 1- control), − Nile tilapia added 5 – (Diet 2), 10 – (Diet 3), and 20 g kg 1 CDXOS (Diet 4). After 4 and 8 weeks feeding were mucosal, Growth performance serum immune responses, and growth performance measured. A challenge test (15 days) against Streptococcus Mucosal immune parameters agalactiae was conducted after 8 weeks post-feeding. A significant (P < 0.05) stimulation of skin mucus lyso- Serum immunology zyme and peroxidase activities, as well as serum immune parameters (serum lysozyme, serum peroxidase, al- ternative complement activities, phagocytosis index, and respiratory burst activity) was noticed by feeding the fish CDXOS supplemented diets compared to the control group. Highest (P < 0.05) innate immune parameters − were observed by feeding the fish 10 g kg 1 CDXOS vs. the other treatments. With regard to the challenge test, relative percent survival (RSP) of Nile tilapia fingerlings fed Diet 2, Diet 3, and Diet 4 was 34.78%, 60.87%, and − 30.43%, respectively. Among the supplemented groups, dietary inclusion of 10 g kg 1 CDXOS revealed sig- nificant (P < 0.05) higher RPS and resistance towards S. agalactiae than the other groups. Regarding growth performance, final weight, weight gain, specific growth rate, and feed conversion ratio were remarkably − (P < 0.05) improved in the CDXOS groups; highest improvement was observed in the 10 g kg 1 CDXOS − treatment. In conclusion, inclusion of 10 g kg 1 CDXOS derived from corncob improved growth performance and health status of Nile tilapia fingerlings.

1. Introduction delivery methods, and side effects to human and the environment (Done et al., 2015; Murray and Peeler, 2005). Thus, it was necessary to Global aquaculture has dramatically expended during the last develop cost-effective alternatives to sustain environmentally friendly decade, and contributed for > 50% of the total fisheries production in aquaculture (Turcios and Papenbrock, 2014), and in this respect has 2014 (Makled et al., 2017). Expansion and intensification of tilapias, prebiotics received considerable attention as a promising alternative one of the most important farmed fish species in the world are nega- dietary feed additive (e.g Akhter et al., 2015; Carbone and Faggio, tively affected by stressful conditions and diseases, which cause serious 2016; Nawaz et al., 2018; Ringø et al., 2014; Song et al., 2014). economic losses (Dhar et al., 2014). Previously, were antibiotics and Prebiotics are indigestible substances that allow specific changes in chemotherapeutics used as treatment strategies towards traditional the composition and/or activity of gastrointestinal microbiota, which diseases. However, these treatments have showed several obstacles and has a positive effect on the nutrition and health status of the host (Ringø restrictions, which include regulatory constraints, inconvenient et al., 2014). Prebiotics play a paramount role in host health when by-

⁎ Corresponding author. E-mail address: [email protected] (E. Ringø). https://doi.org/10.1016/j.aquaculture.2018.06.068 Received 5 May 2018; Received in revised form 23 June 2018; Accepted 23 June 2018 Available online 25 June 2018 0044-8486/ © 2018 Elsevier B.V. All rights reserved. H. Van Doan et al. Aquaculture 495 (2018) 786–793 products in the intestine are fermented by the favorable gut microbiota Table 1 (Choque Delgado et al., 2011; Hoseinifar et al., 2015; Song et al., 2014). The formulation and proximate composition of experimental diet (g kg-1).

fi − In this sense, agricultural by-products, rich sources of dietary bre, Ingredients Diets (g kg 1) have been considered as functional food ingredients which can prevent diseases related to modulation of gut the microbiota (Buruiana et al., Diet 1 Diet 2 Diet 3 Diet 4 2017; Li and Komarek, 2017). Since by-products are not often used or Fish meal 270 270 270 270 they are burned, their use as industrial purpose may overcome the Corn meal 200 200 200 200 proper disposal of the wastes, provide value-added income to the Soybean meal 270 270 270 270 farmers, and generate employment (Chapla et al., 2012). Wheat flour 60 60 60 60 Maize is the staple crop with the largest production worldwide, with Rice bran 150 150 150 150 Cellulose 30 25 20 10 an estimate of 1.026 million tons (López-Castillo et al., 2018). Corn- CDXOSa 051020 cobs, which account for 27% to 30% of maize agro-wastes, are potential Soybean oil 2222 feedstuffs for animal feed and feed substrate (Kanengoni et al., 2015; Premixb 10 10 10 10 Melekwe et al., 2016; Wachirapakorn et al., 2016). They have been Vitamin Cc 8888 − used as substrate for growth of numerous bacteria and fungi, for Proximate composition of the experimental diets (g kg 1 dry matter basis) pharmaceutical production, as well as nutraceutically important en- Crude protein 319.36 319.36 319.35 319.33 zymes (Chapla et al., 2012). Xylooligosaccharides, xylitol, and xylose Crude lipid 71.75 71.75 71.75 71.75 Fibre 52.48 52.48 52.48 52.48 are the main components in the corncob waste (Aachary and Prapulla, Ash 106.68 106.97 107.27 107.88 2009; Sun et al., 2015). They are sugar oligomers made up of xylose Dry matter 817.80 817.40 816.90 816.10 units, and according to Chapla et al. (2013) and (Samanta et al., 2015a) GE (cal/g)d 4066 4065 4064 4061 they are considered as important prebiotics. Additionally, xylooligo- a saccharides (XOS) possess wide ranges of biological - and physiological CDXOS = Corn cob derived xylooligosaccharides. b −1 −1 activities, which include; antioxidant activity, blood and skin related Vitamin and trace mineral mix supplemented as follows (IU kg or g kg effects, antimicrobial, antiallergy, antiinfection, antiinflammatory diet): retinyl acetate 1,085,000 IU; cholecalciferol 217,000 IU; D, L-a-toco- properties, selective cytotoxic activity, and immunomodulatory activity pherol acetate 0.5 g; thiamin nitrate 0.5 g; pyridoxine hydrochloride 0.5 g; −1 (Akpinar et al., 2009; Moure et al., 2006; Parajó et al., 2004; Vazquez niacin 3 g; folic 0.05 g; cyanocobalamin 10 g; Ca pantothenate 1 g kg ; inositol 0.5 g; zinc 1 g; copper 0.25 g; manganese 1.32 g; iodine 0.05 g; sodium 7.85 g. et al., 2000). However, to our knowledge, no information is available c Vitamin C 98% 8 g. about the effects of CDXOS on Nile tilapia (Oreochromis niloticus). d GE = Gross energy. Therefore, the present study addressed to evaluate possible effects of CDXOS on skin mucus - and serum immune responses, Streptococcus use. agalactiae resistance, as well as growth performance of Nile tilapia fingerlings.

2.2. Diets preparation 2. Materials and methods

The basal diet was formulated according to the known requirements 2.1. Xylooligosaccharide preparation of Nile tilapia (Tiengtam et al., 2015). Four diets were prepared by − incorporating CDXOS: 0 (Diet 1 - control), 5 g kg 1 CDXOS (Diet 2), 2.1.1. Preparation of raw materials − − 10 g kg 1 CDXOS (Diet 3), and 20 g kg 1 CDXOS for Diet 4 (Table 1). Corncob obtained from an experimental farm, Faculty of The selection of CDXOS levels was based on the study of Abdelmalek Agriculture, Chiang Mai University, Thailand. Upon arrival, was et al. (2015). For pellets preparation, fine ingredients were completely corncob dried in oven at 60 °C for 48 h, then ground by using hammer mixed together, and soybean-oil and water were added to produce stiff mill, and filtered with the use of 100-mesh size sieve, and stored at 4 °C dough. The dough was thereafter passed through pellet maker machine until further use. to form pellets, and the wet pellets were collected dried in an oven at 50 °C to obtain moisture content around 10% and stored in plastic bags 2.1.2. Isolation of xylan at 4 °C until further use. Isolation of xylan was carried out as described by Chapla et al. (2012) with some modifications. Briefly, 5 g of corncob powder were thoroughly mixed with 80 mL of 1.25 M NaOH. This mixture was in- 2.3. Fish preparation and experimental design cubated at 37 °C for 24 h in automated shaker (Orbital Shaker In- cubator) at a speed of 150 rpm. Then, it was centrifuged at 10.000 g for Tilapia fry were brought from Chiang Mai Patana Farm, Chiang Mai, 5 min, and the supernatant was gathered and acidified to pH 5.0 with Thailand stocked in a cage (5x5x2 m), and fed commercial diet (CP 37% HCl. Next, the obtained supernatant was precipitated by using tilapia feed 9951). After transport from the farm, were the fish trans- 95% ethanol (1.5 volumes), and xylan was collected and dried in hot air ferred to a 1.000-litre tank, and fed the control diet for two weeks to oven at 60 °C for 48 h, and the recovered pellet was used as substrate for acclimatize to experimental conditions. Before experimental start, were enzymatic hydrolysis as described elsewhere (Yoon et al., 2006). 10 randomly caught fish used for health status check, observation of gills and internal organs by light microscopy. Three hundred and 2.1.3. Enzymatic hydrolysis twenty healthy fish with an average weight of 20.72 ± 0.02 were Xylan was used as substrate for xylooligosaccharide production. The − − randomly distributed to 16 glass tanks (150 l tank 1), 20 fish tank 1, substrate was subjected to enzymatic hydrolysis by mixing with 0.01 M and fed experimental diets for eight weeks. Completely Randomized potassium phosphate buffer at pH 6.5 (15% w/v). Thereafter, 100 U/g Design with four replications was applied. Fish were hand-fed to ad of substrate of crude xylanase from Aspergillus niger (support by ASIA libitum with different diets twice per day (9:00 a.m. and 5:00 p.m.). STAR CO., LTD.) was added and the reaction was carried out at 55 °C Water temperature was in a range from 25 to 29 °C, and pH from for 24 h (Boonchuay et al., 2014). The incubated samples were col- − 7.5–8.2. The dissolved oxygen level was not < 5 mg litre 1. lected, and centrifuged at 10.000 rpm for 10 min. The supernatant was gathered and freeze-dried at −40 °C in freeze dryer (FreezeZone Plus Labconco, USA). The obtained powder was kept at −20 °C until further

787 H. Van Doan et al. Aquaculture 495 (2018) 786–793

2.4. Samples preparation and immunological analysis ) Diet 1 Diet 2 Diet 3 Diet 4 -1 9 A 2.4.1. Samples preparation 8 At week four and eight of the feeding trial, were four randomly 7 B caught fish used for the innate immune response analysis. 6 B Collection of skin mucus was sampled according to the protocol of 5 4 C Ross et al. (2000) and Khodadadian Zou et al. (2016). Briefly, four fish a − from each replication were anaesthetized by clove oil (5 mL litre 1), 3 b b and each fish was placed in polyethylene bag containing 10 mL of 2 c 50 mM NaCl (Merck, Germany) for approximately 1 min. Fish were 1 0 gently rubbed inside the plastic in a downward motion for collection of (µg ml activity lysozyme Skin mucus skin mucus. Thereafter, fish were placed in their respective tanks. Skin skeew4 skeew8 mucus samples were immediately transferred to 15 mL sterile cen- Time elapsed trifuge tubes, centrifuged 1.500 × g for 10 min at 4 °C and stored in Fig. 1. Skin mucus lysozyme activity of O. niloticus after 4 and 8 weeks post 1.5 mL tubes at −80 °C until further use. feeding fed different concentrations of dietary CDXOS (mean ± S.E., n = 4): − − Collection and separation of serum were carried out as described Diet1 (0 – control), Diet 2 (5 g kg 1 CDXOS), Diet 3 (10 g kg 1 CDXOS), and − elsewhere (Van Doan et al., 2016b; Van Doan et al., 2016a). Briefly, Diet 5 (20 g kg 1 CDXOS). Columns sharing the same superscript letter are not blood samples were collected through the caudal vein from five fish significantly different (P < 0.05) (by Duncan's Multiple Range Test). − tank 1 using a 1 mL syringe at the end of the feeding trial. The samples were immediately withdrawn into the Eppendorf tubes without antic- the control - and experimental groups as described by (Van Doan et al., oagulant, allowed to clot (1 h at room temperature and 4 h at 4 °C) and 2018). centrifuged at 1500 × g, 5 min, at 4 °C. Serums were stored at −20 °C until analysis. Leukocytes were isolated from peripheral blood by the method of 2.7. Statistical analysis Chung and Secombes (1988) with some modifications; described by Van Doan et al. (2016a) and Van Doan et al. (2016b). The obtained data were analyzed using a SAS Computer Program (SAS, 2003) for least significant differences among the treatments 2.4.2. Immunological measurements where the Duncan's Multiple Range Test was used. Mean values were 2.4.2.1. Lysozyme activity. Serum and skin mucus lysozyme activity considered significantly different when P < 0.05. Data are presented was measured followed the method of Parry et al. (Parry Jr. et al., as means ± standard error (SE). 1965). The equivalent unit of the activity of the sample (compared with − the standard) was determined and expressed in μgmL 1 serum. 3. Results 2.4.2.2. Peroxidase activity. Peroxidase activity was measured according to Quade and Roth (1997) and Cordero et al. (2016). 3.1. Skin mucus immune responses

2.4.2.3. Phagocytosis activity. The phagocytosis activity was Data on skin mucus lysozyme and peroxidase activities of Nile ti- determined as described by Yoshida and Kitao (1991). A detailed lapia fed different concentrations of CDXOS are presented in Figs. 1 & 2. description is presented in the studies of (Van Doan et al., 2016b; Van The results revealed that regardless of inclusion levels, Nile tilapia fed Doan et al., 2016a). diets supplemented with CDXOS; significantly (P < 0.05) increased skin mucus lysozyme and peroxidase activities after 4 and 8 weeks 2.4.2.4. Respiratory burst activity. Measurement of respiratory burst feeding (Figs. 1 & 2). The highest levels of the skin mucus immune − activity was determined by following the method described by parameters were noticed by feeding fish 10 g kg 1 of CDXOS compared Secombes and Fletcher (1992). to the other groups (Figs. 1 & 2). No significant (P>0.05) differences were noticed on lysozyme and peroxidase activities among dietary − 2.4.2.5. Alternative complement pathway activity. Alternative treatments supplemented 5 and 20 g kg 1 of CDXOS (Figs. 1 & 2). complement pathway activity (ACH50) was determined as described by Yanno (1992). )

-1 Diet 1 Diet 2 Diet 3 Diet 4 0.35 A 2.5. Challenge study 0.3 A detailed description of S. agalactiae used in the present study, 0.25 B preparation, and injection dose are presented by (Van Doan et al., 0.2 B 2018). After eight weeks post-feeding, were eight randomly caught fish from each tank injected intraperitoneal with 0.1 mL of 0.85% saline 0.15 a − b b C solution (NSS) containing 107 CFU mL 1 of S. agalactiae. Dead fish from 0.1 each replication were removed daily and recorded. After 15 days post 0.05 c challenge, was mortality (%) of tilapia in each treatment calculated, 0 and the relative percentage of survival (RPS) determined according to (µg ml activity peroxidase Skin mucus skeew4 skeew8 the following equation: Time elapsed RPS=∗ 100–(test mortality/control mortality) 100 Fig. 2. Skin mucus peroxidase activity of O. niloticus after 4 and 8 weeks post feeding fed different concentrations of dietary CDXOS (mean ± S.E., n = 4): − − 2.6. Growth performance Diet1 (0 – control), Diet 2 (5 g kg 1 CDXOS), Diet 3 (10 g kg 1 CDXOS), and − Diet 5 (20 g kg 1 CDXOS). Columns sharing the same superscript letter are not fi ff After eight weeks of feeding, was growth performance calculated in signi cantly di erent (P < 0.05) (by Duncan's Multiple Range Test).

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Diet 1 Diet 2 Diet 3 Diet 4 20 A 450

) A -1 18 400 B 16 a 350 a B 14 300 b B B 12 b 250 b b C 10 C 200 8 c 150 6 c 4 100 50 Serum lysozyme activity (µg ml (µg activity lysozyme Serum 2 0 0 skeew4 skeew8 skeew4 skeew8 Time elapsed Time elapsed

Fig. 3. Serum lysozyme activity of O. niloticus after 4 and 8 weeks post feeding Fig. 5. Alternative complement activity of O. niloticus after 4 and 8 weeks post fed different concentrations of dietary CDXOS (mean ± S.E., n = 4): Diet1 (0 – feeding fed different concentrations of dietary CDXOS (mean ± S.E., n = 4): − − − − control), Diet 2 (5 g kg 1 CDXOS), Diet 3 (10 g kg 1 CDXOS), and Diet 5 Diet1 (0 – control), Diet 2 (5 g kg 1 CDXOS), Diet 3 (10 g kg 1 CDXOS), and − − (20 g kg 1 CDXOS). Columns sharing the same superscript letter are not sig- Diet 5 (20 g kg 1 CDXOS). Columns sharing the same superscript letter are not nificantly different (P < 0.05) (by Duncan's Multiple Range Test). significantly different (P < 0.05) (by Duncan's Multiple Range Test).

3.2. Serum immunological response Diet 1 Diet 2 Diet 3 Diet 4 4

) A ff -1 3.5 The e ects of feeding CDXOS on serum lysozyme activity are shown A A − in Fig. 3. The findings indicated that inclusion level of 10 g kg 1 of 3 a a CDXOS resulted in higher serum lysozyme activity, control vs. the other 2.5 a − treatment groups; 5 and 20 g kg 1 of CDXOS (Fig. 3). However, no 2 B b statistical significant (P>0.05) variation was observed on lysozyme 1.5 −1 activity among the CDXOS inclusion groups; 5 and 20 g kg CDXOS 1 − (Fig. 3). Likewise, inclusion of 10 g kg 1 CDXOS significantly

Phagocytic index (bead cell 0.5 (P < 0.05) increased alternative complement activity of fish compared 0 to the control and other supplemented groups) Fig. 5(. The effects of skeew4 skeew8 dietary administration of CDXOS on phagocytic and respiratory burst Time elapsed activities revealed that fish fed CDXOS, significantly (P < .05) in- creased phagocytosis and respiratory burst activities after 8 weeks post Fig. 6. Phagocytosis activity of O. niloticus after 4 and 8 weeks post feeding fed different concentrations of dietary CDXOS (mean ± S.E., n = 4): Diet1 (0 – feeding. However, no significant (P>0.05) difference among the − − control), Diet 2 (5 g kg 1 CDXOS), Diet 3 (10 g kg 1 CDXOS), and Diet 5 treatment groups was observed (Figs. 6 & 7). Similarly, dietary ad- −1 (20 g kg CDXOS). Columns sharing the same superscript letter are not sig- fi ministration of CDXOS signi cantly (P < 0.05) elevated serum per- nificantly different (P < 0.05) (by Duncan's Multiple Range Test). oxidase activity of Nile tilapia compared to the control group (Fig. 4).

Diet 1 Diet 2 Diet 3 Diet 4 3.3. Challenge test 0.35 A 0.3 A A The survival rates in all CDXOS supplemented groups were sig- 0.25 nificantly (P<0.05) higher, 53.13% (Diet 2), 71.88% (Diet 3), and 0.2 50% (Diet 4) vs. control fed fish (28.13%) (Fig. 8). Dead fish were B noticed in the control group at day 4 after bacterial injection; while in 0.15 a a fi 0.1 the CDXOS treated groups, dead sh were noticed at day 5 and 7. The b fi fi b appearance of dead sh was darkness, exophthalmia, pair- ns basal 0.05

Respiratory burst activity (OD655) 0 Diet 1 Diet 2 Diet 3 Diet 4 skeew4 skeew8 0.4 Time elapsed a A ) 0.35 -1 a A A 0.3 a Fig. 7. Respiratory burst activity of O. niloticus after 4 and 8 weeks post feeding fed different concentrations of dietary CDXOS (mean ± S.E., n = 4): Diet1 (0 – 0.25 − − B control), Diet 2 (5 g kg 1 CDXOS), Diet 3 (10 g kg 1 CDXOS), and Diet 5 − 0.2 b (20 g kg 1 CDXOS). Columns sharing the same superscript letter are not sig- 0.15 nificantly different (P < 0.05) (by Duncan's Multiple Range Test). 0.1 Serum peroxidase (µg ml (µg peroxidase Serum 0.05 haemorrhage and pale liver, typical symptoms of Streptococcus infec- tion. The relative percent survival (RSP) of tilapia was 34.78%, 60.87%, 0 skeew4 skeew8 and 30.43% by feeding Diet 2, Diet 3, and Diet 5, respectively (Fig. 8). −1 Time elapsed Among the supplemented groups, fish fed 10 g kg CDXOS showed significantly (P<0.05) higher RPS and highest resistance towards S. Fig. 4. Serum peroxidase activity of O. niloticus after 4 and 8 weeks post feeding agalactiae compared with other groups (Fig. 8). fed different concentrations of dietary CDXOS (mean ± S.E., n = 4): Diet1 (0 – − − control), Diet 2 (5 g kg 1 CDXOS), Diet 3 (10 g kg 1 CDXOS), and Diet 5 − (20 g kg 1 CDXOS). Columns sharing the same superscript letter are not sig- nificantly different (P < 0.05) (by Duncan's Multiple Range Test).

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Diet 1 Diet 2 Diet 3 Diet 4 researchers, the pharmaceutical - and food industries, as well as nu- 100 traceutical manufacturers following discovery of their multi- 90 dimensional beneficial roles on human and livestock (Samanta et al., 80 2015a). Among the prebiotic compounds, are xylooligosaccharides 70 (XOS) promising, since they occur in agricultural crop residues; are inexpensive, abundant and renewable in nature (Aachary and Prapulla, 60 2011; Samanta et al., 2015b). 50 Skin mucus is released from goblet cells located in fish skin (Pérez- 40 Sánchez et al., 2017). They play important roles as physical -, biological Survival rate (%) 30 -, and immunological barrier against foreign particles, external stressors 20 and pathogens present in the environment (Cordero et al., 2017; 10 Esteban, 2012; Shephard, 1994), and therefore has skin mucus undergo 0 intense studies as a mirror of the immune status of fish (Brinchmann, 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 2016; Carda-Diéguez et al., 2017; Cordero et al., 2017). Several innate Day post challenge immune response parameters, such as proteases, antiproteases, perox- Fig. 8. Survival rate of tilapia, O. niloticus fed different concentrations of idases, esterases, alkaline phosphatase, lysozyme or immunoglobulins − dietary CDXOS (n = 8): Diet1 (0 – control), Diet 2 (5 g kg 1 CDXOS), Diet 3 have been assessed in skin mucus (Cordero et al., 2016; Cordero et al., − − (10 g kg 1 CDXOS), and Diet 5 (20 g kg 1 CDXOS) during 15 days post chal- 2017; Guardiola et al., 2014; Neil et al., 2000). In agreement with our lenge with Streptococcus agalactiae. results, revealing that CDXOS supplemented diets significantly stimu- lated mucus lysozyme and peroxidase activities of Nile tilapia; sig- 3.4. Growth performance nificant increase in mucosal immunity has been reported in other fish species. For example by β-glucan in common carp (Cyprinus carpio) Table 2 shows the effects of CDXOS on growth, nutrition utilization, (Przybylska-Diaz et al., 2013); XOS in Caspian white fish (Rutilus frisii and survival of Nile tilapia. Feeding the fish diets supplemented CDXOS kutum)(Hoseinifar et al., 2014); galactooligosaccharide in common for 8 weeks resulted in significantly (P<0.05) improved FW, WG, and carp, goldfish (Carassius auratus gibelio) and rainbow trout (Oncor- SGR compared to control fed fish (Table 2), and the highest growth hynchus mykiss)(Modanloo et al., 2017); Cordyceps militaris spent − performances were revealed in the diet group of 10 g kg 1 CDXOS mushroom substrate in Nile tilapia (Van Doan et al., 2017), and Agar- compared to the other treatment groups. However, the values did not icus bisporus powder in common carp, (Khodadadian Zou et al., 2016). − significantly (P > 0.05)differ by feeding tilapia 5 and 20 g kg 1 The significant elevation of skin mucus lysozyme and peroxidase ac- CDXOS. No statistical significant (P > 0.05) variations were observed tivities revealed in present study is due to xylooligosaccharide. Im- on survival by dietary administration. Nile tilapia fed CDXOS showed munostimulants, such as prebiotics, probiotics, and medical plants are significantly (P<0.05) lower FCR than the control (Table 2), and the well known to display positive effects on the mucosal immune system of − lowest FCR was revealed in treatment group fed 10 g kg 1 CDXOS; fish, including gut-associated skin-associated lymphoid tissues, and gill- however, no difference was revealed among other supplemented groups associated lymphoid tissues (Caipang, 2015; Martin and Król, 2017; (Table 2). Vallejos-Vidal et al., 2016). However, the mode of action of how CDXOS modulates fish mucosal immune response is unknown and merit investigations. 4. Discussion Regarding the serum immune responses, the present study displayed that dietary administration of CDXOS significantly stimulated serum Prebiotics seem to be promising as they possess various biological immunology of Nile tilapia. To our knowledge, no information is activities functions, which include modulation towards more favorable available about the effect of CDXOS on tilapia innate immune response. intestinal microbiota, improvement of mineral absorption, pathogen However, in accordance with the results of the present study, sig- exclusion, and immune stimulation (Sánchez and Vázquez, 2017; nificantly improved serum immune response through dietary adminis- Slavin, 2013). Commercialization of oligosaccharides as low calorie tration of XOS has been observed in turbot (Scophthalmus maximus)(Li bulking agents increased during 1980s, due to attention among

Table 2 − − Growth performances and feed utilization of the Nile tilapia fed different levels of dietary CDXOS: Diet 1 (control), Diet 2 (5 g kg 1 CDXOS), Diet 3 (10 g kg 1 − CDXOS), and Diet 4 (20 g kg 1 CDXOS). Values are presented as the mean ± SE.

Diet 1 Diet 2 Diet 3 Diet 4

Initial weight (g) 20.74 ± 0.03 20.73 ± 0.04 20.66 ± 0.01 20.76 ± 0.03

Final weight (g) 4 weeks 91.59 ± 2.04c 99.82 ± 0.83b 105.95 ± 2.37a 98.16 ± 1.24b 8 weeks 181.21 ± 6.25c 203.16 ± 2.90b 217.98 ± 2.34a 197.17 ± 1.29b

Weight gain (g) 4 weeks 70.85 ± 2.05c 79.10 ± 0.85b 85.28 ± 2.38a 77.40 ± 1.25b 8 weeks 160.47 ± 6.26c 182.43 ± 2.92b 197.31 ± 2.34a 176.40 ± 1.29b

SGR 4 weeks 2.77 ± 0.04c 2.91 ± 0.02b 3.03 ± 0.04a 2.88 ± 0.02b 8 weeks 2.43 ± 0.04c 2.56 ± 0.02b 2.65 ± 0.01a 2.53 ± 0.01b

FCR 4 weeks 1.49 ± 0.01a 1.45 ± 0.004b 1.43 ± 0.005c 1.46 ± 0.003b 8 weeks 1.56 ± 0.003a 1.51 ± 0.004b 1.49 ± 0.003c 1.52 ± 0.001b

Survival rate (%) 98 99 99 98

Data assigned with different letter denote significant difference in a row (P < 0.05).

790 H. Van Doan et al. Aquaculture 495 (2018) 786–793 et al., 2008), Caspian white fish (Hoseinifar et al., 2014), white sea have similar effect on tilapia gut cells, resulting in a decrease of fish bream (Diplodus sargus)(Guerreiro et al., 2016) and European seabass innate immune response. To confirm this hypothesis, gut morphology (Dicentrarchus labrax)(Abdelmalek et al., 2015; Azeredo et al., 2017). merits investigations in future studies. Although, the exact mechanism Although dietary prebiotics stimulate fish immune response, the mode how XOS significantly improve growth performance of fish has not yet of action has not clearly been demonstrated. In an early study, (Brown been clarified, it may be due to that XOS acts as prebiotic and im- et al., 2002) put forward the hypothesis that immunosaccharides di- munostimulant. Moreover, dietary XOS has revealed beneficial effects rectly activate the non-specific immune system by contacting with PRRs on gut lactic acid bacteria (LAB) and an increase in digestive enzyme expressed on microphages receptors, such as β-glucan or dentin-1. The activities; amylase and protease (Hoseinifar et al., 2014; Xu et al., interaction between these ligand-receptors will stimulate signal trans- 2009). The importance of LAB is well known as they participate by duction molecules, such as NF-kB and finally activate immune cells improving growth performance, regulate pathogens through competi- (Yadav and Schorey, 2006). Moreover, the pathogen-associated mole- tive exclusion for adhesion sites, production of SCFA, hydrogen per- cular patterns of bacteria, such as teichoic acid, peptidoglycan, glyco- oxide, antibiotics, bacteriocins, siderophores, and lysozyme (Hoseinifar sylated protein, and the capsular polysaccharide can be detected and et al., 2015; Li et al., 2018; Xia et al., 2018). LAB also influence the fish thus enhancing the immune response (Matozzo et al., 2016; Pagano physiological - and immunological responses (Hoseinifar et al., 2015; et al., 2016; Song et al., 2014). Therefore, it seems likely that prebiotics Merrifield et al., 2014; Nayak, 2010; Ringø et al., 2010). Moreover, activate the non-specific immune system in two different ways; stimu- prebiotics supplementation increase microbiota metabolite products; late the non-specific immune system, or enhance population level of acetic -, lactic -, propionic - and butyric acid (Hoseinifar et al., 2016; beneficial intestinal bacteria (Hoseinifar et al., 2015; Song et al., 2014; Ríos-Covián et al., 2016), a topic that merits investigations in further Wang An et al., 2017). A recent study revealed that CDXOS displayed studies on tilapia and CDXOS, as in vertebrate, these SCFAs may be prebiotic properties; antimicrobial effects, production of short chain useful for the immune cells of the gut associated lymphoid tissue (Bach fatty acids (SCFS), modulate the intestinal microbiota, and stimulated Knudsen et al., 2003; Hoseinifar et al., 2015). Furthermore, SCFAs are growth of Lactobacillus plantarum (Yu et al., 2015). absorbed by the host and utilized as energy source, with butyrate acting S. agalactiae significantly affects the global aquaculture industry and as the main fuel for the colonic wall (Topping and Clifton, 2001; Sleeth causes huge economic-losses (Li et al., 2015). Therefore, success against et al. 2010). Streptococcus infection is one of the most important goals in aquaculture In conclusion, the present study clearly showed that CDXOS could as well as for the tilapia culture industry. Successful improvement of be a functional feed additive for tilapia, by promoting growth perfor- survival rate by immunostimulants administration has been demon- mance, immune response, and improved protection against S. aga- strated in many fish species, such as Nile tilapia (Laith et al., 2017; Van lactiae. These findings encourage further research on application of Doan et al., 2018), rainbow trout (Baba et al., 2018), and tambaqui CDXOS isolated from agricultural by-products as feed additive to other (Colossoma macropomum)(Ribeiro et al., 2018). It is well known that fish species. immunostimulatory compounds improve natural resistance of fishes (Raa, 1996; Sakai, 1999; Wang et al., 2017). The ability of im- Acknowledgements munostimulants in case of bacteria inhibition is normally linked to the improvement of immune responses (Kheti et al., 2017). In agreement The authors wish to thank Thai Research Fund (Grant No. with our results, revealing improved survival of Nile tilapia by feeding MRG5980127) and Functional Food Research Center for Well-being, CDXOS in a challenge experiment with S. agalactiae; dietary adminis- Chiang Mai University, Thailand for their fi nancial assistance. Thanks tration of CDXOS showed significantly increased survival rate of Eur- to Dr. Wanaporn Tapingkae for her kind assistance in preparation of opean seabass and narrow-clawed crayfish (Astacus leptodactylus) xylooligosaccharide. Finally, the authors would like to thank for the against Aeromonas hydrophila (Abdelmalek et al., 2015; Safari et al., staffs at Central and Biotechnology Laboratories as well as Post Harvest 2017). These findings infer that CDXOS can enhance humoral and Technology Research Center, Faculty of Agriculture, Chiang Mai cellular factors, serum lysozyme, alternative complement, peroxidase, University for their kind supports during data analysis. respiratory burst, and phagocytosis activities of the host during pa- thogen invasion. The protective effect of CDXOS supplemented diet References may be attributable to the sugar contents, which enhance disease re- sistance of host via stimulation of the innate immune system Aachary, A.A., Prapulla, S.G., 2009. Value addition to corncob: production and char- (Abdelmalek et al., 2015; Burgents et al., 2004). acterization of xylooligosaccharides from alkali pretreated lignin-saccharide complex using Aspergillus oryzae MTCC 5154. Bioresour. Technol. 100, 991–995. The ultimate goal of aquaculture is to obtain fast growth and low Aachary, A.A., Prapulla, S.G., 2011. Xylooligosaccharides (XOS) as an emerging prebiotic: feed conversion ratio (FCR). The present study, showed significant microbial synthesis, utilization, structural characterization, bioactive properties, and improvement of growth and FCR by feeding tilapia CDXOS. Similarly, applications. Compr. Rev. Food Sci. Food Saf. 10, 2–16. fi Abdelmalek, B.E., Driss, D., Kallel, F., Guargouri, M., Missaoui, H., Chaabouni, S.E., signi cant improved growth performance and FCR have been displayed Ayadi, M.A., Bougatef, A., 2015. Effect of xylan oligosaccharides generated from in turbot (Li et al., 2008); crucian carp (Carassius auratus gibelio) (Xu corncobs on food acceptability, growth performance, haematology and im- et al., 2009), and European seabass (Abdelmalek et al., 2015) fed diets munological parameters of Dicentrarchus labrax fingerlings. Fish Physiol. Biochem. – supplemented with XOS. However, in contrast to our results, Hoseinifar 41, 1587 1596. Akhter, N., Wu, B., Memon, A.M., Mohsin, M., 2015. Probiotics and prebiotics associated et al. (2014) reported that although higher FW, WG, SGR and lower with aquaculture: a review. Fish Shellfish Immunol. 45, 733–741. FCR was noticed in Caspian white fish fed 3% XOS, no significant dif- Akpinar, O., Erdogan, K., Bostanci, S., 2009. Production of xylooligosaccharides by – ferences were observed vs. the other groups. Different aspects, types of controlled acid hydrolysis of lignocellulosic materials. Carbohydr. Res. 344, 660 666. Azeredo, R., Machado, M., Kreuz, E., Wuertz, S., Oliva-Teles, A., Enes, P., Costas, B., 2017. prebiotic, administration routes, dosage, fermentability, the gut mi- The European seabass (Dicentrarchus labrax) innate immunity and gut health are crobiota communities, fish species, and developmental stages must be modulated by dietary plant-protein inclusion and prebiotic supplementation. Fish ff fi Shellfish Immunol. 60, 78–87. considered when discussing e ects on sh growth and feed digestibility ı fi Baba, E., Acar, Ü., Y lmaz, S., Zemheri, F., Ergün, S., 2018. Dietary olive leaf (Olea europea (Hoseinifar et al., 2010). Interestingly, signi cant lower growth per- L.) extract alters some immune gene expression levels and disease resistance to formance and innate immune responses were revealed in Nile tilapia Yersinia ruckeri infection in rainbow trout Oncorhynchus mykiss. Fish Shellfish − − fed 20 g kg 1 CDXOS compared with fish fed 10 g kg 1 CDXOS. This Immunol. 79, 28–33 (August). Bach Knudsen, K.E., Serena, A., Canibe, N., Juntunen, K.S., 2003. New insight into bu- may be attributed to the inclusion level of CDXOS in the diet, as pre- tyrate metabolism. Proc. Nutr. Soc. 62, 81–86. vious investigations have reported that high dietary level of prebiotics Boonchuay, P., Techapun, C., Seesuriyachan, P., Chaiyaso, T., 2014. Production of xy- exert damaging effect on intestinal enterocytes (Cerezuela et al., 2013; looligosaccharides from corncob using a crude thermostable endo-xylanase from Streptomyces thermovulgaris TISTR1948 and prebiotic properties. Food Sci. Olsen et al., 2001). The highest CDXOS dose used in present study may

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