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Serum Protein Profile of Juvenile Pacu (Piaractus mesopotamicus) and Dourado (Salminus brasiliensis) Fed Bovine Colostrum as Partial Source of Protein in the Diet.

INTRODUCTION

Fish farming has increased mainly due to a greater demand for healthier meats for human consumption (1). However, the intensive production of these species presents a great challenge for the producer as a concentration of large populations increases the predisposition to bacterial and parasitic diseases (2). This problem is especially critical in the early stages of life of teleosts (3). Therefore, the formulation of diets that contribute to the health and well-being of juveniles are of great relevance.

Bovine colostrum is the first mammal lacteal secretion that is crucial for nutritional, metabolic and endocrine status of neonates (4,5). The effects of colostrum consumption include the protection of the enteric and respiratory tract and reduction in mortality and morbidity of the newborn (6-8). The high nutritional value and concentration of biological molecules, such as antioxidant and antimicrobial factors, designate colostrum as a nutraceutical food (9). This lacteal secretion from bovine has been widely used as an immunological and nutritional source for several species, including swine and rodents (10,11). In fish, the supply of lyophilized bovine colostrum is an innovative conception and the effects of this food on fish health has been explored by different approaches (12-14).

In Brazil, Piaractus mesopotamicus and Salminus brasiliensis, popularly known as pacu and dourado, are neotropical species with favorable features for commercial production. Besides being a species of interest for the sport of fishing, Piaractus mesopotamicus and Salminus brasiliensis present good performance and acceptance by the consumers (2,15,16). However, information about their physiology and the effects of nutraceutical foods on their health is still being gathered. The electrophoresis of proteins from blood plasma or serum can be used in humans and animals to provide information on acute and chronic inflammatory processes and consequently health (17,18). In recent decades, the study of blood protein fractions from different species has increased, including works involving fish, which focus on the relation between water pollution and fish health (19-22). The effects of diet on protein profile, especially gamma globulin fraction where antibodies are positioned, are of great relevance to evaluate the health and immunity of fish.

Since electrophoresis has been proposed to aid in the diagnosis of disease, normal reference ranges for serum protein levels still need to be established in different species offish. Considering colostrum as a nutraceutical food, there is the possibility of this food modulating immunity, and consequently, fish health. Thus, this study investigates the electrophoretic prolife of serum proteins of juvenile Piaractus mesopotamicus and Salminus brasilienesis fed diets with bovine colostrum, a nutraceutical food, in the lyophilized form (LBC).

MATERIAL AND METHODS

Diets

The first lacteal secretion from multiparous Holstein cows was frozen at-20[degrees]C and, thereafter, lyophilized. This powderwas homogenized to obtain a homogeneous sample, which was analyzed for the bromatological composition. Considering the nutritional composition of bovine colostrum, isonitrogenous and isoenergetic pelleted diets were formulated to attend to the requirements of juveniles Piaractus mesopotamicus and Salminus brasiliensis (Tables 1 and 2). After the homogenization of the ingredients, the diets were pelletized, dried (at a temperature of approximately 46 [degrees]C) and stored in a dry place until the time of supply. Chemical compositions of experimental pelleted diets were subsequently submitted to chemical analysis (23).

Experiment

Juvenile Piaractus mesopotamicus and Salminus brasiliensis (8.5[+ or -]0.7 and 13.3[+ or -]0.9 g; 7.8[+ or -]0.3 and 10.8[+ or -]0.3 cm, respectively) were randomly distributed in 36 tanks (324 pacu in 18 tanks and 270 dourado in 18 tanks) with controlled water quality parameters (26.8[+ or -]1.5[degrees]C,5.8[+ or -]1.0 mg [L.sup.-1] of dissolved oxygen and <0.05 mg [L.sup.-1] dissolved ammonia). After adaptation for 10 and seven days, respectively, diets containing 0%, 10% or 20% bovine colostrum in LBC were hand-fed to apparent satiety twice a day (08h30 and 16h30) for either 30 or 60 days (authorized by the ESALQ/USP ethics committee).

Seven fish were sampled on the 30th and 60th experimental day after 24 h fasting and anesthesia with benzocaine (0.1 g [L.sup.-1]). Blood samples obtained from the caudal vein were centrifuged and the serum was stored at -20[degrees]C.

Analyses

The total serum protein was determined (24) and an electrophoretic analysis was performed in an agarose gel (CELMGEL) for 30 min at 90 volts. After staining with 0.2% starch black for 5 min., a reading of the protein fractions in a densitometer (CELM DS35) with a wavelength of 520 nm was performed. The software CELM SE-250 was used to calculate the relative percentage of each protein fraction from the area under the curve created by the protein fraction. No attempt has been made to identify protein components of the sera studied as albumin or globulin. The electrophoretic fractions were numbered according to the increasing mobility.

Statistical Analysis

Serum variables were analyzed based on a 2x3 completely randomized factorial design using SAS software (SAS Institute Inc., 2004), taking into consideration the three diets and two feeding periods (30 and 60 experimental days). An analysis of variance was performed using the general linear model and comparisons between pairs of means were made using the Tukey test considering p<0.05.

RESULTS

Electrophoretic profile of serum proteins of juvenile pacu {Piaractus mesopotamicus)

Using the software SDS-60 (Celm), six fractions in the serum of juvenile Piaractus mesopotamicus were identified (Figures 1 and 2). These fractions were quantified by the software considering the value of serum total protein (Table 3). The effect of the period was observed for the 2nd fraction (p<0.05), with a higher value at 30 days compared to 60 days. The 6th fraction was affected by the diet and period (p<0.05), with higher values at 60 days and in the group 0% LBC.

Electrophoretic profile of serum proteins of juvenile dourado (Salminus brasiliensis)

Using the software SDS-60 (Celm), four fractions in the serum of juvenile Salminus brasiliensis were identified (Figures 3 and 4). These fractions were quantified by the software considering the value of serum total protein (Table 4). The effect of the period was observed for the 1st and 4th fractions (p<0.05), with higher values at 30 days compared to 60 days.

DISCUSSION

The serum protein profile of juvenile pacu, Piaractus mesopotamicus, showed six fractions. Approximately 28%, 19%, 14%, 8%, 25%, and 7% of proteins were observed in the 1st, 2nd, 3rd, 4th, 5th and 6th fraction, respectively. In the juvenile dourado, Salminus brasiliensis, four fractions were identified. The 1st to 4th fraction corresponded approximately to 32%, 41%, 5% and 22% of the serum total protein (25). Work with four species of Tilapia, seven serum fractions were observed in the T. nilotica, T. galilaea and T. aurea, while de T. zillii showed six serum fractions. The authors also observed differences in the protein concentration in each band and suggest that these results might be related to diet.

The 2nd fraction in the serum of pacu and the 1st fraction in the serum of dourado, Salminus brasiliensis, showed a higher protein concentration at 30 days compared to 60 days, indicating an inverse relationship with growth. As an additional investigation, bovine serum albumin (BSA, Sigma-Aldrich Co) was added to fish serum and samples were submitted again to electrophoresis analyses. The electrophoretic profile was not changed in both species; however, the 2nd fraction from Piaractus mesopotamicus serum and the 1st fraction from dourado serum showed a significant increase in its participation of total protein from 19% to 43% and 36% to 53%, respectively. These results indicated that these fractions are in the albumin migration zone and are probably the corresponding protein in fish. Thus, in juvenile pacu, the calculation of globulin by the difference of serum total protein and albumin is not adequate, since near 28% of serum proteins are in the 1st fraction, which corresponds to pre-albumin proteins and are not considered in this calculation.

According to Atamanalp et al. (26) and Maceda Veiga et al. (27), environmental changes can affect the physiological and biochemical characteristics offish blood, and the hematological and serum protein profiles are important indices in monitoring the effects of aquatic habitat changes suggests that the reduction of serum protein concentration is related to an adverse environment. The authors observed lower serum protein concentration in the Mugil cephalus exposed to different pHs. In the present work, Piaractus mesopotamicus and Salminus brasiliensis showed a reduction of protein concentration in the 2nd and 1st fractions, respectively, after 60 experimental days, suggesting a less favorable condition for fish. According to Fazio et al. (22), the reduction of protein concentration is due to protein catabolism, i.e. the process of converting blood and structural proteins to energy to produce higher energy, resulting in fish adaptation to a wide range of environmental conditions.

The 3rd and 4th fractions from Piaractus mesopotamicus serum and the 2nd and 3rd fractions from Salminus brasiliensis serum were positioned in an alpha-beta-globulin zone. Further studies should be conducted to better characterize each serum protein fraction since this information can be useful to fish health.

The 5th and 6th fraction from pacu serum and the 4th fraction from dourado, Salminus brasiliensis, serum were positioned in a gamma-globulin zone, where immunoglobulin are usually expected. In this study, the concentration of this protein fraction in pacu, Piaractus mesopotamicus, serum was higher at 60 days compared to 30 days while in dourado serum it was lower at 60 days compared to 30 days. According to Scapigliati et al. (28), the immunoglobulin levels increase consistently with age and size; however, other events like water oxygenation and season can also affect concentrations of this protein in serum. The authors observed that the hyperoxygenation of seawater resulted in a two-fold increase of immunoglobulins, from 3.9 mg [mL.sup.-1] in running seawater, to 7.1 mg [mL.sup.-1] at 12 ppm [O.sub.2] [L.sup.-1]. In juvenile Piaractus mesopotamicus, great concentrations of proteins were also observed in the 5th fraction in the group that was not fed lyophilized bovine colostrum, 0% LBC. This result suggests that the first lacteal bovine secretion, rich in immune and antimicrobial elements such as immunoglobulins, lactoferrin, lactoperoxidase and lysozyme (29), may have contributed to the protection of the juvenile. Consequently, the juveniles had less stimulus for their own synthesis of defense elements, probably immunoglobulin M. On the other hand, this result can indicate an immunosuppressive effect of colostrum. According to Mandalapu et al. (30) human colostrum contains a factor (colostrum inhibitory factor XX) that inhibits the induction of interleukin 2 in T lymphocyte cell lines. Aldridge et al. (31), in turn, observed that colostrum feeding reduces the number of immunoglobulin positive cells in the lymphoid tissues of newborn calves.

As found by other authors using SDS-PAGE, the presence, position and amount of protein in serum fractions can be affected by pollutants, water quality and phylogenetic distance (20, 32-36). Gicking et al. (37) states that plasma protein electrophoresis may be useful as a health assessment tool for evaluating injured sea turtles. The authors determined reference intervals for plasma protein fractions of wild Atlantic loggerhead sea turtles, Caretta caretta. In the present study, the values of protein concentration could be useful as reference ranges forthe health of juvenile Piaractus mesopotamicus and Salminus brasiliensis.

The two species studied, Piaractus mesopotamicus and Salminus brasiliensis, showed different electrophoretic profiles of serum proteins. The first species, an omnivorous fish, showed six fractions while the second, a carnivorous fish, showed four fractions. Fractions that were positioned in the albumin and gamma-globulin migration zone were affected by feeding period, 30 or 60 experimental days, in both species, pacu and dourado. Bovine colostrum influenced the serum protein profile of the juvenile Piaractus mesopotamicus with some indications of positive protective effects.

Ethics Committee Approval: Ethics committee approval was received for this study from the ethics committee of CEUA-ESALQ.

Peer-review: Externally peer-reviewed.

Author Contributions: Concept - R.M.N., DM; Design - R.M.N., D.M., W.N.; Supervision - R.M.N.; Resource - R.M.N., D.M.; Materials - R.M.N.; Data Collection and/or Processing - D.M., W.N.; Analysis and/or Interpretation - D.M.; Literature Search - D.M.; Writing - DM; Critical Reviews - R.M.N.

Conflict of Interest: The authors have no conflict of interest to declare.

Financial Disclosure: This study was supported by Sao Paulo Research Foundation (FAPESP), process 2012/50284-2 and 2011/51713-1 and National Council for Scientific and Technological Development (CNPq).

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Debora Moretti (1*) [iD], Wiolene Nordi (2) [iD], Raul Machado-Neto (1) [iD]

(1) University of Sao Paulo, Luiz de Queiroz College of Agriculture, Department of Animal Science, Piracicaba, Brazil

(2) Agriculture and Agri-Food Canada, Lethbridge Research and Development Centre, Government of Canada, Alberta, Canada

ORCID IDs of the authors: D.M. 0000-0003-0912-9989; W.N. 0000-0003-3666-6245; R.M.N. 0000-0002-5982-2776.

Please cite this article as: Moretti D, Nordi W, Machado-Neto R. Serum Protein Profile of Juvenile Pacu (Piaractus mesopotamicus) and Dourado (Salminus brasiliensis) Fed Bovine Colostrum as Partial Source of Protein in the Diet. Eur J Biol 2018; 77(2): 59-64.

This study was presented at the 39th CONBRAVET-Congresso Brasileiro de Medicina Veterinaria, December 4th-6th, 2012, Sao Paulo, Brazil.

Address for Correspondence: Debora Moretti

E-mail: dmoretti@usp.br

Received: 01.03.2018

Accepted: 19.06.2018

DOI: 10.26650/EurJBiol.2018.400108
Table 1. Chemical composition of experimental pelleted diets fed to
juvenile Piaractus mesopotamicus

                                                 Diets (1)
Ingredient (g [kg.sup.-1])                0%     10%    20%

Bovine colostrum (679 g [kg.sup.-1] CP)   -      100    200
Soybean meal (45 g [kg.sup.-1] CP)        265     76.7    -
Wheat meal                                238    311.8  311.8
Poultry by-product meal                   200    200    131
Broken rice                               188    198    200
Fish meal (55% CP)                         50     50     50
Fish oil                                   46.2   40     45.7
DL-methionine                               2.4    3.4    4.7
L-lysine HCI                                -      6     11.5
BHT                                         2      2      2
Cellulose                                   -      3.4    -
Calcareous                                  -      -     14.7
Corn grain                                  -      -      9.3
Premix (2)                                 10     10     10.5
Chemical composition (g [kg.sup.-1]) (3)
Dry matter                                940.6  933.4  936.4
Crude protein                             324.6  314.9  322
Crude fiber                                30     27.7   30.7
Fat                                        90.5   98.2  109.3
Ash                                       106.4  101.1   92.8
Gross energy (MJ [kg.sup.-1])              18     18.2   18.3

(1) 0% -diets containing 0% of lyophilized bovine colostrum; 10%-diets
containing 10% of lyophilized bovine colostrum; 20% - diets containing
20% of lyophilized bovine colostrum.
(2) Guabi Nutricao Animal, Campinas, Sao Paulo (ingredient per kg).
Vitamins: A, 2,500 Ul; D3,600.000 Ul; E, 37.500 Ul; K3,3,750 mg; C,
50,000 mg; Bl, 4.000 mg; B2,4,000 mg; B6,4,000 mg; B12,4,000 mg;
calcium pantothenate, 12,000 mg; biotin, 15 mg; acid folic, 1,250 mg;
niacin, 22,500 mg. Mineral: Cu, 2,500 mg; Zn, 12,500 mg; 1,375 mg; Se,
87.5 mg; Co, 125 mg; Mn, 12,500 mg; Fe, 15,000 mg; BHT, 15,000 mg.
(3) Original matter basis.

Table 2. Chemical composition of experimental pelleted diets fed to
juvenile Salminus brasiliensis

                                                 Diets (1)
Ingredient (g [kg.sup.-1])                0%     10%    20%

Bovine colostrum (679 g [kg.sup.-1] CP)   -      100    200
Soybean meal (45 g [kg.sup.-1] CP)        230    230    230
Poultry by-product meal                   204.8  119.8   24.5
Fish meal (55 g [kg.sup.-1] CP)           320    300    300
Fish oil                                   95     90     85.2
Premix (2)                                 10     10     10
BHT                                         0.2    0.2    0.2
Cellulose                                  20     30     30
Corn (whole grain)                        120    120    120
Chemical composition (g [kg.sup.-1]) (3)
Dry matter                                924.4  936.7  925.7
Crude protein                             422    425.1  444.7
Crude fiber                                18.9   29.2   37.3
Fat                                       140.7  140.6  133.7
Ash                                       121.9  114.5   91.1
Gross energy (MJ [kg.sup.-1])              20.8   21.1   20.8

(1) 0% -diets containing 0%of lyophilized bovine colostrum; 10%-diets
containing 10% of lyophilized bovine colostrum; 20% - diets containing
20% of lyophilized bovine colostrum.
(2) Guabi Nutricao Animal, Campinas, Sao Paulo (ingredient per kg).
Vitamins: A, 2,500 Ul; D3,600.000 Ul; E, 37.500 Ul; K3,3,750 mg; C,
50,000 mg; B1,4.000 mg; B2,4,000 mg; B6,4,000 mg; B12,4,000 mg; calcium
pantothenate, 12,000 mg; biotin, 15 mg; acid folic, 1,250 mg; niacin,
22,500 mg. Mineral: Cu, 2,500 mg; Zn, 12,500 mg; 1,375 mg; Se, 87.5 mg;
Co, 125 mg; Mn, 12,500 mg; Fe, 15,000 mg; BHT, 15,000 mg.
(3) Original matter basis.

Table 3. Serum protein fractions (in order from fastest to slowest) and
total protein (g [dL.sup.-1]) in juvenile Piaractus mesopotamicus (mean
[+ or -] standard error) fed lyophilized bovine colostrum

                               Diet (1)
         0% LBC                10% LBC

Total
protein  4.00[+ or -]0.23      4.14[+ or -]0.16
Band 1   1.07[+ or -]0.09      1.18[+ or -]0.06
Band 2   0.80[+ or -]0.04      0.79[+ or -]0.05
Band 3   0.54[+ or -]0.03      0.56[+ or -]0.02
Band 4   0.29[+ or -]0.02      0.32[+ or -]0.01
Band 5   0.97[+ or -]0.05      1.00[+ or -]0.04
Band 6   0.32[+ or -]0.03 (a)  0.27[+ or -]0.01 (b)

         Diet (1)             Feeding period (days)
         20% LBC               30                60

Total
protein  3.95[+ or -]0.11      4.04[+ or -]0.14  4.03[+ or -]0.12
Band 1   1.11[+ or -]0.02      1.09[+ or -]0.05  1.16[+ or -]0.03
Band 2   0.76[+ or -]0.06      0.86[+ or -]0.03  0.69[+ or -]0.03
Band 3   0.54[+ or -]0.02      0.53[+ or -]0.02  0.56[+ or -]0.01
Band 4   0.29[+ or -]0.01      0.29[+ or -]0.01  0.32[+ or -]0.01
Band 5   1.00[+ or -]0.05      1.02[+ or -]0.04  0.97[+ or -]0.03
Band 6   0.25[+ or -]0.02 (b)  0.24[+ or -]0.01  0.31 [+ or -]0.02

         Effect (2)
          D   P   DXP

Total
protein   NS  NS  NS
Band 1    NS  NS  NS
Band 2    NS  *   NS
Band 3    NS  NS  NS
Band 4    NS  NS  NS
Band 5    NS  NS  NS
Band 6    *   *   NS

(*) p<0.05; NS-p>0.05; means followed by the same letter (a,b) differ
(p<0.05); 10% LBC-juveniles fed 0% of lyophilized bovine colostrum; LBC
10%-juveniles fed 10% of lyophilized bovine colostrum; 20%
CBL-juveniles fed 20% of lyophilized bovine colostrum; 2D-diet effect
P-period effect; DxP-interaction between diet and period.

Table 4. Serum protein fractions (in order from fastest to slowest) and
total protein (g dL-1) in juvenile Salminus brasiliensis (mean [+ or -]
standard error) fed lyophilized bovine colostrum

                                 Diet (1)
               0% LBC            10% LBC           20% LBC

Total protein  3.37[+ or -]0.08  3.42[+ or -]0.07  3.38[+ or -]0.12
Band 1         1.01[+ or -]0.03  1.13[+ or -]0.04  1.11[+ or -]0.07
Band 2         1.45[+ or -]0.05  1.37[+ or -]0.06  1.37[+ or -]0.05
Band 3         0.12[+ or -]0.01  0.13[+ or -]0.01  0.13[+ or -]0.01
Band 4         0.79[+ or -]0.03  0.79[+ or -]0.01  0.76[+ or -]0.03

               Feeding period (days)               Effect (2)
               30                60                D   P   DXP

Total protein  3.46[+ or -]0.05  3.33[+ or -]0.08  NS  NS  NS
Band 1         1.16[+ or -]0.03  1.01[+ or -]0.03  NS  *   NS
Band 2         1.35[+ or -]0.04  1.44[+ or -]0.04  NS  NS  NS
Band 3         0.13[+ or -]0.01  0.13[+ or -]0.01  NS  NS  NS
Band 4         0.81[+ or -]0.02  0.75[+ or -]0.01  NS  *   NS

(*) p<0.05; NS-p>0.05; 10% LBC-juveniles fed 0% of lyophilized bovine
colostrum; LBC 10%-juveniles fed 10% of lyophilized bovine colostrum;
20% CBL-juveniles fed 20% of lyophilized bovine colostrum; 2D-diet
effect P-period effect; DxP-interaction between diet and period.
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Author:Moretti, Debora; Nordi, Wiolene; Machado-Neto, Raul
Publication:IUFS Journal of Biology
Date:Dec 1, 2018
Words:4459
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