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Growth performance and meat quality of broiler chickens supplemented with Rhodopseudomonas palustris in drinking water a
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Q.Q. Xu , H. Yan , X.L. Liu , L. Lv , C.H. Yin & P. Wang a
School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Beijing 100083, China Accepted author version posted online: 14 Mar 2014.Published online: 23 Apr 2014.
To cite this article: Q.Q. Xu, H. Yan, X.L. Liu, L. Lv, C.H. Yin & P. Wang (2014) Growth performance and meat quality of broiler chickens supplemented with Rhodopseudomonas palustris in drinking water, British Poultry Science, 55:3, 360-366, DOI: 10.1080/00071668.2014.903326 To link to this article: http://dx.doi.org/10.1080/00071668.2014.903326
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British Poultry Science, 2014 Vol. 55, No. 3, 360–366, http://dx.doi.org/10.1080/00071668.2014.903326
Growth performance and meat quality of broiler chickens supplemented with Rhodopseudomonas palustris in drinking water Q.Q. XU, H. YAN, X.L. LIU, L. LV, C.H. YIN,
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P. WANG
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School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Beijing 100083, China
Abstract 1. The effect of the bacterium, Rhodopseudomonas palustris, on the growth performance and meat quality of broiler chickens was investigated. 2. A total of 900-d-old Arbor Acres broilers were allocated to three experimental treatments for 6 weeks. Chicks were administered with R. palustris in drinking water as follows: (i) control group without R. palustris; (ii) treatment 1 (R1) with R. palustris of 8 × 109 cells per chick per day in drinking water; (iii) treatment 2 (R2) with R. palustris of 1.6 × 1010 cells per chick per day in drinking water. 3. The results showed that, compared with that of control, both groups of R. palustris treatment increased daily weight gain and improved feed conversion ratio of broiler chickens significantly during the whole growing period of 6 weeks. 4. Both total and glutamic acid contents of chicken breast fillet in R. palustris treatment R2 were higher, while the fat content was lower, than those of the control group. Furthermore, R. palustris treatments also improved sensory attributes of chicken breast fillet. 5. As a probiotic providing rich nutrients and biological active substances, R. palustris administration in drinking water displayed a growth promoting effect and improved meat quality of broiler chickens.
INTRODUCTION In the poultry industry, antibiotics have been widely used for therapeutic, prophylactic and growth promotion purposes. However, improper use of antibiotics could cause bacterial resistance and antibiotic residues in poultry products, which could produce potential threats to humans, including allergic reactions and imbalances in intestinal microflora (Teuber, 2001; Dibner and Richards, 2005). Since 2006, the use of antibiotics as growth promoters in animal feed has been banned in the European Union (Castanon, 2007). Current research highlights the role of probiotics as an effective alternative to subtherapeutic antibiotics. Probiotics have been defined as “live microorganisms which, when administered in adequate amounts, confer a health benefit on the host” by improving its intestinal microbial balance, increasing digestive capacity, stimulating the
immune system and enhancing production performance (Patterson and Burkholder, 2003; Mountzouris et al., 2009). Previous studies on probiotic utilisation in poultry dominantly focus on various strains of Lactobacillus, Bifidobacterium, Enterococcus, Bacillus, Aspergillus and yeasts (Lee et al., 2007; Mountzouris et al., 2007; Samli et al., 2010; Molnár et al., 2011; Amirdahri et al., 2012). The photosynthetic bacterium R. palustris has generally been evaluated as a probiotic in aquaculture to enhance the growth performance of fish, improve water quality and maintain fish health (Zhou et al., 2010; Wang, 2011; Peirong and Wei, 2013). R. palustris supplemented diet also reduced the risk of atherosclerosis in rats (Lee et al., 1990; Tsujii et al., 2007). However, less information has been provided on the effect of R. palustris treatment, especially via drinking water, on poultry performance. In addition to
Correspondence to: Hai Yan, School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Beijing 100083, China. E-mail: [email protected] Accepted for publication 14 January 2014.
© 2014 British Poultry Science Ltd
RHODOPSEUDOMONAS AND BROILER PERFORMANCE
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its functions as a probiotic, R. palustris also provides rich nutrients (Kim and Lee, 2000) and many bioactive ingredients including lycopene and coenzyme Q10 as a nutritional feed additive (Bao et al., 2010). Here, the effect of R. palustris on growth performance and meat quality of Arbor Acres broiler chickens was studied. Broiler performance parameters such as daily weight gain (DWG), feed conversion ratio (FCR) and chicken mortality were determined. Protein, fat, moisture, amino acid contents and sensory attributes of chicken breast meat were also measured to evaluate meat quality.
MATERIALS AND METHODS Probiotic strain and culture A bacteria strain of R. palustris (No. 1.2180) was bought from the China General Microbiological Culture Collection Center. It was cultured at 30°C and a light intensity of 3000 lx for 6 d using the medium previously reported (Chen et al., 2007). The cells were harvested using centrifugation at 18500 g for 20 min, then resuspended and washed twice with the drinking water of chicks. R. palustris suspension with the concentration of viable bacterial cells 8 × 1010 cells/ml was prepared and diluted daily with the drinking water of chicks.
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per day in drinking water. After receiving the required amount of R. palustris, water without R. palustris was supplied for further consumption ad libitum. Growth performance Body weight of birds was measured individually on a weekly basis. Dead birds were removed daily and weighed. The amounts of added feed to each pen and the residual feed remaining at the end of each week were accurately weighed and recorded. Feed consumption divided by body weight gain per day per chick was taken as FCR. The DWG of each weak and FCR in starter period (0–3 weeks), grower period (3–6 weeks) and overall (0–6 weeks) were calculated. Sample collection and analytical determinations At 6 weeks of age, 10 male chickens from each pen were selected randomly and killed by the conventional method at a slaughtering plant. Breast muscles from the right side of each carcass were excised and individually divided into two sections. One section was used for chemical composition analysis, whereas the other for sensory analyses. All the samples were stored in plastic bags at −20°C before analyses. For chemical composition and free amino acid analyses, 10 breast fillets from each pen were homogenised and mixed together as one sample. Protein, moisture
Birds and experimental treatments A total of 900 one-d-old Arbor Acres (AA) broiler chicks were randomly assigned to three experimental groups and raised for 6 weeks. Each treatment had 300 broilers arranged in three replicates of 100 chicks (50 male and 50 female) per replication. The chicks of each replicate were raised in floor pens (0.90 m2/bird) equipped with self-feed feeders and drinkers. Chicks were vaccinated at hatch for Marek’s disease, infectious bronchitis and Newcastle disease. The ambient temperature was 32°C on the first day, followed by a gradual decline in temperature to 24°C on d 21, and maintained at this temperature until termination of the experiment. All birds had access to feed ad libitum under continuous light conditions. The basal diet without any antibiotics or growth promoters was formulated for starter (0–3 weeks) and grower (3–6 weeks) periods (Table 1), and met or exceeded the nutrient requirements of broilers. The drinking water was untreated well water with pH 7.5 with free residual chlorine of 0 mg/l. The birds in control group received water without R. palustris. R. palustris treatment 1 (R1) had 8 × 109 R. palustris cells per chick per day in drinking water, while R. palustris treatment 2 (R2) had R. palustris of 1.6 × 1010 cells per chick
Table 1. Ingredients and composition of the basal diet
Ingredients (g/kg)
Starter
Grower
(0–3 weeks)
(3–6 weeks)
Maize 535.3 Soybean meal 355.2 Fish meal 39.9 Vegetable oil 35.2 Limestone 15.2 Sodium chloride 3.0 Monocalcium phosphate 9.2 2.0 Vitamin premixa 2.0 Mineral premixb DL-methionine 1.5 L-lysine 1.0 Choline chloride 0.5 Analysed and calculated chemical composition (g/kg) ME (MJ/kg) 12.9 Crude protein 221.6 Lysine 11.2 Methionine + cystine 8.5 Calcium 10.2 Total phosphorus 6.9
588.6 315.3 36.3 30.2 12.7 3.0 7.8 2.0 2.0 1.0 0.6 0.5 12.8 206.3 9.5 7.6 8.7 6.3
a Vitamin premix provided per kg of diet: retinol acetate 3.37 mg, cholecalciferol 0.05 mg, DL-α-tocopherol 40 mg, menadione 2 mg, thiamine 1 mg, riboflavin 7 mg, pyridoxine 6 mg, cyanocobalamine 0.035 mg, nicotine 50 mg, pantothenic acid 15 mg, folic acid 1.5 mg and biotin 0.15 mg. b Mineral premix provided per kg of diet: iron 70 mg, copper 9 mg, manganese 90 mg, zinc 60 mg, selenium 0.16 mg and iodine 0.5 mg.
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and fat contents in chicken breast fillet were determined by the AOAC Official Method.
RESULTS Growth performance
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Free amino acid analysis About 200 mg homogenate sample was extracted with 1.5 ml of methanol–water solution (1:1, v/v) for 30 min and then centrifuged at 10 000 g for 5 min. The supernatant was diluted with methanol–water solution at a 1:25 ratio. The dilute supernatant (40 μl) were labelled with iTRAQTM reagents (AA 45/32 kit, Applied Biosystems) and analysed on an Applied Biosystems SCIEX 3200 QTRAP® LC/MS/MS system equipped with Amino Acid Analyser (AAA) C18 Column (5 µm particle size, 4.6 mm diameter, 150 mm length). The contents of total amino acids, essential amino acids and glutamic acid, which is one important taste-active component for developing meat taste, were measured.
The effect of R. palustris treatment on DWG of male birds is shown in Table 2. No significant differences between the three treatment groups were seen for DWG in the starter period of 0–3 weeks. However, R. palustris treatments R1 and R2 showed higher DWG than that of control during the growing period of 3–6 weeks and the whole growing period of 0–6 weeks, suggesting R. palustris had a beneficial effect on the growth performance in the latter and whole periods. A similar effect was found in female birds (Table 3). Table 4 clearly shows how R. palustris treatment significantly reduced the FCR of the chicks. Overall for the entire experiment, there was significant difference (P < 0.05) in FCR of R1 and R2 (1.66 ± 0.021 and 1.71 ± 0.021, Table 2.
Sensory analyses Sensory characteristics of chicken breast fillet were evaluated by three groups of semi-trained students. Each group consisted of 15 students (20–28 years of age) with 8 males and 7 females. Before tasting, panellists were well instructed on the assessment criteria, meat attributes to be rated and how to properly complete the questionnaire. Chicken breast fillet samples were sliced into 1-cm-thick pieces and grilled until internal temperature reached 71–75°C. The samples were provided to the sensory panel using random threedigit numbers. The presentation order of samples and the first-order and carry-over effect were blocked. Each treated sample was tasted by at least three different panellists. Room temperature water was used to neutralise sensory perception between samples. The trial consisted of 6 sessions, and the traits assessed were meat colour, aroma strength, juiciness, flavour, texture and overall acceptability. A 9-point scale was used, 1 referring to extremely light, very weak, extremely dry, extremely unpleasant, extremely gooey and disagreeable, 9 referring to extremely dark, very strong, extremely juicy, extremely enjoyable, extremely smooth and enjoyable.
Statistical analysis The results were subjected to one-way analysis of variance using the general linear models (GLM) procedure of SPSS 19.0.0 software (2010, SPSS Inc., USA). Significance of differences (P < 0.05) was evaluated by Duncan’s test.
Effect of R. palustris treatment on daily weight gain of male birds (mean ± SEM) Daily weight gain of treatment groups (g)
Age in weeks 0–1 1–2 2–3 3–4 4–5 5–6 0–3 3–6 0–6
Control 20.26 30.81 73.41 94.87 93.76 82.38 41.49 90.34 65.91
± ± ± ± ± ± ± ± ±
0.25a 0.59a 0.80a 0.90a 1.54a 1.93a 0.52a 1.32a 0.89a
R1 22.28 32.45 74.98 88.20 93.40 112.49 43.24 98.03 70.63
± ± ± ± ± ± ± ± ±
R2 0.25b 0.60ab 0.82a 0.90b 1.53a 1.94b 0.51a 1.30b 0.90b
20.65 33.96 71.58 83.48 103.00 109.15 42.06 98.54 70.30
± ± ± ± ± ± ± ± ±
0.25a 0.59b 0.81a 0.88c 1.50b 1.77b 0.52a 1.28b 0.89b
a,b,c Mean values within the same row sharing a common superscript letter are not statistically different at P < 0.05. Control: without R. palustris. R1: R. palustris treatment with 8 × 109 R. palustris cells per chick per day in drinking water. R2: R. palustris treatment with 1.6 × 1010 R. palustris cells per chick per day in drinking water.
Table 3.
Effect of R. palustris treatment on daily weight gain of female birds (mean ± SEM) Daily weight gain of treatment groups (g)
Age in weeks 0–1 1–2 2–3 3–4 4–5 5–6 0–3 3–6 0–6
Control 21.42 28.49 58.07 68.41 74.89 75.00 36.00 72.77 54.38
± ± ± ± ± ± ± ± ±
0.25a 0.49a 0.69a 0.84a 1.29a 1.98a 0.46a 0.98a 0.71a
R1 21.87 30.44 57.27 75.77 92.74 98.73 36.53 89.08 62.80
± ± ± ± ± ± ± ± ±
R2 0.25a 0.50b 0.69a 0.84b 1.30b 1.95b 0.46a 0.97b 0.71b
21.84 28.08 62.68 74.97 90.71 80.47 37.54 82.05 59.79
± ± ± ± ± ± ± ± ±
0.25a 0.50a 0.69b 0.83b 1.29b 1.96a 0.46a 1.00c 0.72c
a,b,c Mean values within the same row sharing a common superscript letter are not statistically different at P < 0.05. Control: without R. palustris. R1: R. palustris treatment with 8 × 109 R. palustris cells per chick per day in drinking water. R2: R. palustris treatment with 1.6 × 1010 R. palustris cells per chick per day in drinking water.
RHODOPSEUDOMONAS AND BROILER PERFORMANCE
Table 4. Broiler feed conversion (feed/gain) ratio during the starter, grower and the entire experimental period (mean ± SEM)
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significantly different in essential amino acid content (Figure 1(e)) with respect to the control.
Feed conversion ratio of treatment groups (g) Age in week 0–3 3–6 0–6
Sensory attributes
Control
R1
R2
1.61 ± 0.02a 1.91 ± 0.02a 1.81 ± 0.02a
1.60 ± 0.02a 1.68 ± 0.02b 1.66 ± 0.02b
1.58 ± 0.02a 1.76 ± 0.02c 1.71 ± 0.02b
respectively) compared with the control (1.81 ± 0.021), while R1 and R2 did not differ. There were no treatment effects on bird mortality, which is consistent with that reported by O’Dea et al. (2006). Chemical composition and free amino acid analyses
DISCUSSION
90
b
b a
85 80 75 70
4 b
3 a
c
2
100
1
R2 b
a
Control
a
R1
Control
(e)
R2
Essential Amino Acid Content (mg/g)
R1
R1
a
a
a
Control
R1
R2
60 40 20
R2 (f)
20 15
80
0
0 Control
(d) 80 70 60 50 40 30 20 10 0
(c)
(b) 5
Moisture Content (%)
95
In this work, administration of R. palustris in drinking water significantly increased DWG of broilers, especially during the late growth period. These findings are in agreement with those of Alkhalf et al. (2010), concluding that a commercial probiotic Pediococcus acidilactici improved DWG of broilers compared with control treatment after 3 weeks of age. Gao et al. (2008) also showed that DWG of broilers fed on a diet supplemented with 2.5 g/kg of yeast culture was significantly better than that of control during grower and overall periods. Probiotic treatment is known to benefit the host animals by improving their intestinal microflora balance, which could increase the
a
a b
10 5
Glutamic Acid Content (mg/g)
100
Fat Content (%)
(a) Protein Content (g/100 g dry weight)
The protein content, fat content, moisture content and amino acid contents of chicken breast fillet are presented in Figure 1(a–f). Figure 1(a) shows that the protein contents of the breast meat in two R. palustris treatments were significantly higher than that of control group, while the moisture content had no changes (Figure 1(c)). Figure 1(b) shows that the chicken breast fillet of R. palustris treatment R2 had a lower fat percentage (6.5%) than that of the control group (7.9%) and R. palustris treatment R1 (10.6%). Both total amino acid content (65.2 mg/g) and glutamic acid content (4.2 mg/g) (Figure 1(d, f)) of chicken breast fillet in R. palustris treatment R2 were higher than those of control, but not
Total Amino Acid Content (mg/g)
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a,b,c Mean values within the same row sharing a common superscript letter are not statistically different at P < 0.05. Control: without R. palustris. R1: R. palustris treatment with 8 × 109 R. palustris cells per chick per day in drinking water. R2: R. palustris treatment with 1.6 × 1010 R. palustris cells per chick per day in drinking water.
To assess meat quality, sensory attributes such as meat colour, aroma strength, juiciness, flavour, texture and overall acceptability of chicken breast fillet were determined in our study (Figure 2). Statistically significant effects of the probiotic treatments on the improvement of meat colour and juiciness were found (P < 0.05), as well as lower values of flavour and texture for control than the two R. palustris treatments (P < 0.05, Figure 2). However, no differences were noticed between the two R. palustris treatments. The remaining sensory attribute aroma strength was not affected by R. palustris treatments. Finally, for overall acceptability, two R. palustris treatments were significant higher than control (P < 0.05).
6 5 4
b a
a
3 2 1 0
0 Control
R1
R2
Control
R1
R2
Figure 1. Effect of R. palustris treatment on meat quality of broiler chickens. Error bars represent standard deviations (n = 3). Control: without R. palustris, R1: R. palustris treatment with 8 × 109 R. palustris cells per chick per day in drinking water and R2: R. palustris treatment with 1.6 × 1010 R. palustris cells per chick per day in drinking water.
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Figure 2. Comparison of meat colour, aroma strength, juiciness, flavour, texture and overall acceptability of chicken breast fillet between the control group and R. palustris treated groups. A 9-point scale was used where the meat colour ranged from extremely light to extremely dark, aroma strength from very weak to very strong, juiciness from extremely dry to extremely juicy, flavour from extremely unpleasant to extremely enjoyable, texture from extremely gooey to extremely smooth and overall acceptability from disagreeable to enjoyable. Error bars represent standard deviations (n = 15).
efficiency of digestion and nutrient absorption processes and enhance growth and improve feed efficiency, as found in poultry (Lu et al., 2003; Djouvinov, 2005), mammals (Guerra et al., 2007; Scharek et al., 2007) and aquatic animals (Yanbo and Zirong, 2006; Wang, 2011). Intestinal microflora balance is always dynamic (Sonnenburg et al., 2006; El-Shibiny et al., 2007), and early intestinal bacterial community of broiler chickens is relatively transient and is replaced by a stable one with increasing complexity as the chicks age (Lu et al., 2003). So the beneficial effect occurred after the stable intestinal bacterial community had been established, which is about the third week found in our study. As shown in Table 4, R. palustris treatment significantly reduced the FCR of the chicks. An improvement in FCR of broilers by feeding probiotic has been evidenced in many studies (Karimi Torshizi et al., 2010; Molnár et al., 2011; Lv et al., 2012). FCR is not a simple index of feed intake, but it reflects the relationship between feed utilisation and actual body weight gain. Although probiotic supplement to the chicks may lead to more appetitive foraging, an improvement in the intestinal environment which includes gut microflora, gut maintenance, mucus production and host immune function could improve the digestibility of feed, promote the absorption of nutrients and thus promote growth, decrease FCR and reduce the production cost (Mountzouris et al., 2007). However, some studies reported that probiotic supplementation did not affect FCR of chickens (Huang et al., 2004; Biernasiak and Slizewska, 2009; Navidshad et al., 2010). These varying results may be due to differences in the bacterial strains, dosages and broiler growth stages. In our study, treatment R1 with R. palustris of 8 × 109 cells per chick per day in drinking water could supply
adequate amounts of probiotics to get beneficial effects on growth performance and FCR of broilers. In addition to a probiotic effect, R. palustris itself can also be a nutritious feed additive, containing high contents of protein and many bioactive ingredients such as lycopene and coenzyme Q10, which is widely used in aquaculture for feeding fish and shrimp (Kim and Lee, 2000). Studies showed that lycopene supplementation increased the final live weight of broilers (Sevcikova et al., 2008) and decreased the cholesterol content of chicken leg meat (Englmaierova et al., 2011). Coenzyme Q10 is a component of the electron transport chain, generating energy in the form of ATP. Karadas et al. (2011) found that coenzyme Q10 also plays an important role in chick viability as an antioxidant, but in most of the tissues its concentrations decreased substantially between 18 h and 36 h post-hatch. In this study, R. palustris treatment could supply lycopene and exogenous coenzyme Q10 for the chickens to improve energy generation, resistance to oxidative stress and to benefit to growth performance. Protein, fat and water are the basic components of poultry meat. In meat products, proteins and carbohydrates are used in combination with water to produce gels to get the elastic, soft and juicy texture (Chizzolini et al., 1999). Protein contents of the breast meat in two R. palustris treatments were significantly higher than the control group, suggesting that R. palustris treatment could maintain the texture quality of meat, which also coincided with the sensory attributes (Figure 2). Excess fat deposition is supposed to be the main negative effect of nutrition (Jiménez-Colmenero et al., 2001). In our study, fat content (Figure 1 (b)) of breast meat was significantly decreased by
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RHODOPSEUDOMONAS AND BROILER PERFORMANCE
the R2 treatment, which could provide low-fat meat as healthy food materials. Flavour is one of the most significant factors influencing the quality of meat products. As we know, most of the meat flavour develops during cooking. The main reactions are the Maillard reaction between reducing sugars and amino acids, the thermal degradation of lipid and Maillard–lipid interactions (Mottram, 1998; Jayasena et al., 2013). Some amino acids such as serine, glutamic acid, glycine, isoleucine, leucine, alanine and proline contribute to the rich full flavour of meat (Imanari et al., 2007; Liu et al., 2007, 2012). As one important taste-active component, glutamic acid could enhance meat taste including delicious, umami and brothy tastes. Among chicken, pork and beef, chicken contained the most free glutamic acid (Imanari et al., 2008; Jayasena et al., 2013). In our study, the concentration of glutamic acid in chicken breast fillet exceeded the threshold concentration for umami taste (Chen and Zhang, 2007). The amino acid contents of chicken breast fillet in R. palustris treatment R2 were higher in both total amino acids and glutamic acid. In sensory analyses, statistically significant effects of R. palustris treatment on the improvement of flavour and overall acceptability were also found, which suggested that R. palustris treatment induced an increase in amino acid content of meat and improved meat taste. Our study showed that the supplement of R. palustris, especially in high levels, made a great contribution to nutritional and sensorial quality improvements of meat. These results could be due to rich nutrients and biological active substances provided by R. palustris. In conclusion, administration of R. palustris in drinking water significantly improved DWG and FCR of broilers, but no effect on mortality was found. The breast meat of chickens in the R. palustris treatments, especially in high levels of R. palustris supplement, had increased contents of total and glutamic acid and decreased fat content. Furthermore, improvement in sensory attributes was observed in broilers fed with R. palustris. As a potential probiotic which also provides rich nutrients and biological active substances, R. palustris can be recommended to be used for increasing growth performance and meat quality of broiler chickens.
ACKNOWLEDGEMENTS The authors wish to acknowledge the Fundamental Research Funds for the Central Universities [grant number FRF-AS-10-001B] and Beijing Municipal Science and Technology Commission [grant number z131102002813058] for financial support of this research.
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REFERENCES ALKHALF, A., ALHAJ, M. & AL-HOMIDAN, I. (2010) Influence of probiotic supplementation on blood parameters and growth performance in broiler chickens. Saudi Journal of Biological Sciences, 17: 219–225. doi:10.1016/j. sjbs.2010.04.005. AMIRDAHRI, S., JANMOHAMMADI, H., TAGHIZADEH, A. & RAFAT, A. (2012) Effect of dietary Aspergillus meal prebiotic on growth performance, carcass characteristics, nutrient digestibility, and serum lipid profile in broiler chick lowprotein diets. Turkish Journal of Veterinary & Animal Sciences, 36: 602–610. BAO, Y.X., YAN, H., LIU, L.Q. & XU, Q.Q. (2010) Efficient extraction of lycopene from Rhodopseudomonas palustris with n-hexane and methanol after alkaline wash. Chemical Engineering & Technology, 33: 1665–1671. doi:10.1002/ ceat.201000033. BIERNASIAK, J. & SLIZEWSKA, K. (2009) The effect of a new probiotic preparation on the performance and faecal microflora of broiler chickens. Veterinarni Medicina, 54: 525–531. CASTANON, J.I.R. (2007) History of the use of antibiotic as growth promoters in European poultry feeds. Poultry Science, 86: 2466–2471. doi:10.3382/ps.2007-00249. CHEN, C.Y., LU, W.B., WU, J.F. & CHANG, J.S. (2007) Enhancing phototrophic hydrogen production of Rhodopseudomonas palustris via statistical experimental design. International Journal of Hydrogen Energy, 32: 940–949. doi:10.1016/j. ijhydene.2006.09.021. CHEN, D.-W. & ZHANG, M. (2007) Non-volatile taste active compounds in the meat of Chinese mitten crab (Eriocheir sinensis). Food Chemistry, 104: 1200–1205. doi:10.1016/j. foodchem.2007.01.042. CHIZZOLINI, R., ZANARDI, E., DORIGONI, V. & GHIDINI, S. (1999) Calorific value and cholesterol content of normal and low-fat meat and meat products. Trends in Food Science & Technology, 10: 119–128. doi:10.1016/S0924-2244(99) 00034-5. DIBNER, J.J. & RICHARDS, J.D. (2005) Antibiotic growth promoters in agriculture: history and mode of action. Poultry Science, 84: 634–643. doi:10.1093/ps/84.4.634. DJOUVINOV, D. (2005) Effect of feeding Lactina probiotic on performance, some blood parameters and caecalmicroflora of mule duckings. Trakia Journal of Sciences, 3: 22–28. EL-SHIBINY, A., CONNERTON, P.L. & CONNERTON, I.F. (2007) Campylobacter succession in broiler chickens. Veterinary Microbiology, 125: 323–332. doi:10.1016/j. vetmic.2007.05.023. ENGLMAIEROVA, M., BUBANCOVA, I., VIT, T. & SKRIVAN, M. (2011) The effect of lycopene and vitamin E on growth performance, quality and oxidative stability of chicken leg meat. Czech Journal of Animal Science, 56: 536–543. GAO, J., ZHANG, H.J., YU, S.H., WU, S.G., YOON, I., QUIGLEY, J., GAO, Y.P. & QI, G.H. (2008) Effects of yeast culture in broiler diets on performance and immunomodulatory functions. Poultry Science, 87: 1377–1384. doi:10.3382/ps.2007-00418. GUERRA, N.P., BERNÁRDEZ, P.F., MÉNDEZ, J., CACHALDORA, P. & PASTRANA CASTRO, L. (2007) Production of four potentially probiotic lactic acid bacteria and their evaluation as feed additives for weaned piglets. Animal Feed Science and Technology, 134: 89–107. doi:10.1016/j. anifeedsci.2006.05.010. HUANG, M., CHOI, Y., HOUDE, R., LEE, J., LEE, B. & ZHAO, X. (2004) Effects of Lactobacilli and an acidophilic fungus on the production performance and immune responses in broiler chickens. Poultry Science, 83: 788–795. doi:10.1093/ ps/83.5.788. IMANARI, M., KADOWAKI, M. & FUJIMURA, S. (2007) Regulation of taste-active components of meat by dietary leucine. British Poultry Science, 48: 167–176. doi:10.1080/ 00071660701244738.
Downloaded by [Memorial University of Newfoundland] at 09:56 01 August 2014
366
Q.Q. XU ET AL.
IMANARI, M., KADOWAKI, M. & FUJIMURA, S. (2008) Regulation of taste-active components of meat by dietary branched-chain amino acids; effects of branched-chain amino acid antagonism. British Poultry Science, 49: 299–307. doi:10.1080/ 00071660802155080. JAYASENA, D.D., AHN, D.U., NAM, K.C. & JO, C. (2013) Flavour chemistry of chicken meat: a review. Asian-Australasian Journal of Animal Sciences, 26: 732–742. doi:10.5713/ ajas.2012.12619. JIMÉNEZ-COLMENERO, F., CARBALLO, J. & COFRADES, S. (2001) Healthier meat and meat products: their role as functional foods. Meat Science, 59: 5–13. doi:10.1016/S0309-1740(01) 00053-5. KARADAS, F., SURAI, P.F. & SPARKS, N.H.C. (2011) Changes in broiler chick tissue concentrations of lipid-soluble antioxidants immediately post-hatch. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 160: 68–71. doi:10.1016/j.cbpa.2011.05.006. KARIMI TORSHIZI, M.A., MOGHADDAM, A.R., RAHIMI, S. & MOJGANI, N. (2010) Assessing the effect of administering probiotics in water or as a feed supplement on broiler performance and immune response. British Poultry Science, 51: 178–184. doi:10.1080/00071661003753756. KIM, J.K. & LEE, B.-K. (2000) Mass production of Rhodopseudomonas palustris as diet for aquaculture. Aquacultural Engineering, 23: 281–293. doi:10.1016/S01448609(00)00057-1. LEE, M.G., KOBAYASHI, M. & YASUMOTO, K. (1990) Hypocholesterolemic effect of phototrophic bacterial cells in rats. Journal of Nutritional Science and Vitaminology, 36: 475–483. doi:10.3177/jnsv.36.475. LEE, S., LILLEHOJ, H.S., PARK, D.W., HONG, Y.H. & LIN, J.J. (2007) Effects of Pediococcus- and Saccharomyces-based probiotic (MitoMax®) on coccidiosis in broiler chickens. Comparative Immunology Microbiology and Infectious Diseases, 30: 261–268. doi:10.1016/j.cimid.2007.02.002. LIU, X.L., YAN, H., LV, L., XU, Q.Q., YIN, C.H., ZHANG, K.Y., WANG, P. & HU, J.Y. (2012) Growth performance and meat quality of broiler chickens supplemented with Bacillus licheniformis in drinking water. Asian-Australasian Journal of Animal Sciences, 25: 682–689. doi:10.5713/ ajas.2011.11334. LIU, Y., XU, X.-L. & ZHOU, G.-H. (2007) Changes in taste compounds of duck during processing. Food Chemistry, 102: 22–26. doi:10.1016/j.foodchem.2006.03.034. LU, J., IDRIS, U., HARMON, B., HOFACRE, C., MAURER, J.J. & LEE, M. D. (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Applied and Environmental Microbiology, 69: 6816–6824. doi:10.1128/ AEM.69.11.6816-6824.2003. LV, L., YAN, H., LIU, X.L., XU, Q.Q. & YIN, C.H. (2012) Growth performance and meat quality of broiler chickens supplemented with chicken-specific Lactobacillus CSL-13 in drinking water. Indian Journal of Animal Sciences, 82: 1415–1422. MOLNÁR, A.K., PODMANICZKY, B., KÜRTI, P., TENK, I., GLÁVITS, R., VIRÁG, G.Y. & SZABÓ, Z.S. (2011) Effect of different concentrations of Bacillus subtilis on growth performance, carcase quality, gut microflora and immune response of broiler chickens. British Poultry Science, 52: 658–665. doi:10.1080/ 00071668.2011.636029. MOTTRAM, D.S. (1998) Flavour formation in meat and meat products: a review. Food Chemistry, 62: 415–424. doi:10.1016/ S0308-8146(98)00076-4. MOUNTZOURIS, K.C., TSIRTSIKOS, P., KALAMARA, E., NITSCH, S., SCHATZMAYR, G. & FEGEROS, K. (2007) Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler
performance and modulating cecal microflora composition and metabolic activities. Poultry Science, 86: 309–317. doi:10.1093/ps/86.2.309. MOUNTZOURIS, K.C., BALASKAS, C., XANTHAKOS, I., TZIVINIKOU, A. & FEGEROS, K. (2009) Effects of a multi-species probiotic on biomarkers of competitive exclusion efficacy in broilers challenged with Salmonella enteritidis. British Poultry Science, 50: 467–478. doi:10.1080/00071660903110935. NAVIDSHAD, B., ADIBMORADI, M. & ANSARI PIRSARAEI, Z. (2010) Effects of dietary supplementation of Aspergillus originated prebiotic (Fermacto) on performance and small intestinal morphology of broiler chickens fed diluted diets. Italian Journal of Animal Science, 9: 55–60. doi:10.4081/ijas.2010.e12. O’DEA, E.E., FASENKO, G.M., ALLISON, G.E., KORVER, D.R., TANNOCK, G.W. & GUAN, L.L. (2006) Investigating the effects of commercial probiotics on broiler chick quality and production efficiency. Poultry Science, 85: 1855–1863. PATTERSON, J.A. & BURKHOLDER, K.M. (2003) Application of prebiotics and probiotics in poultry production. Poultry Science, 82: 627–631. doi:10.1093/ps/82.4.627. PEIRONG, Z. & WEI, L. (2013) Use of fluidized bed biofilter and immobilized Rhodopseudomonas palustris for ammonia removal and fish health maintenance in a recirculation aquaculture system. Aquaculture Research, 44: 327–334. doi:10.1111/j.1365-2109.2011.03038.x. SAMLI, H.E., DEZCAN, S., KOC, F., OZDUVEN, M.L., OKUR, A.A. & SENKOYLU, N. (2010) Effects of Enterococcus faecium supplementation and floor type on performance, morphology of erythrocytes and intestinal microbiota in broiler chickens. British Poultry Science, 51: 564–568. doi:10.1080/ 00071668.2010.507241. SCHAREK, L., ALTHERR, B.J., TÖLKE, C. & SCHMIDT, M.F.G. (2007) Influence of the probiotic Bacillus cereus var. toyoi on the intestinal immunity of piglets. Veterinary Immunology and Immunopathology, 120: 136–147. doi:10.1016/j. vetimm.2007.07.015. SEVCIKOVA, S., SKRIVAN, M. & DLOUHA, G. (2008) The effect of lycopene supplementation on lipid profile and meat quality of broiler chickens. Czech Journal of Animal Science, 53: 431–440. SONNENBURG, J.L., CHEN, C.T.L. & GORDON, J.I. (2006) Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLOS Biology, 4: e413. doi:10.1371/journal.pbio.0040413. TEUBER, M. (2001) Veterinary use and antibiotic resistance. Current Opinion in Microbiology, 4: 493–499. doi:10.1016/ S1369-5274(00)00241-1. TSUJII, H., NISHIOKA, M., SALMA, U., MIAH, A.G., MAKI, T. & LEE, M.G. (2007) Comparative study on hypocholesterolemic effect of Rhodopseudomonas palustris and Rhodobacter capsulatus on rats fed a high cholesterol diet. Animal Science Journal, 78: 535–540. doi:10.1111/j.1740-0929.2007.00473.x. WANG, Y. (2011) Use of probiotics Bacillus coagulans, Rhodopseudomonas palustris and Lactobacillus acidophilus as growth promoters in grass carp (Ctenopharyngodon idella) fingerlings. Aquaculture Nutrition, 17: e372–e378. doi:10.1111/j.1365-2095.2010.00771.x. YANBO, W. & ZIRONG, X.U. (2006) Effect of probiotics for common carp (Cyprinus carpio) based on growth performance and digestive enzyme activities. Animal Feed Science and Technology, 127: 283–292. doi:10.1016/j. anifeedsci.2005.09.003. ZHOU, X.X., TIAN, Z.Q., WANG, Y.B. & LI, W.F. (2010) Effect of treatment with probiotics as water additives on tilapia (Oreochromis niloticus) growth performance and immune response. Fish Physiology and Biochemistry, 36: 501–509. doi:10.1007/s10695-009-9320-z.
British Poultry Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/cbps20
Growth performance and meat quality of broiler chickens supplemented with Rhodopseudomonas palustris in drinking water a
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Q.Q. Xu , H. Yan , X.L. Liu , L. Lv , C.H. Yin & P. Wang a
School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Beijing 100083, China Accepted author version posted online: 14 Mar 2014.Published online: 23 Apr 2014.
To cite this article: Q.Q. Xu, H. Yan, X.L. Liu, L. Lv, C.H. Yin & P. Wang (2014) Growth performance and meat quality of broiler chickens supplemented with Rhodopseudomonas palustris in drinking water, British Poultry Science, 55:3, 360-366, DOI: 10.1080/00071668.2014.903326 To link to this article: http://dx.doi.org/10.1080/00071668.2014.903326
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British Poultry Science, 2014 Vol. 55, No. 3, 360–366, http://dx.doi.org/10.1080/00071668.2014.903326
Growth performance and meat quality of broiler chickens supplemented with Rhodopseudomonas palustris in drinking water Q.Q. XU, H. YAN, X.L. LIU, L. LV, C.H. YIN,
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P. WANG
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School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Beijing 100083, China
Abstract 1. The effect of the bacterium, Rhodopseudomonas palustris, on the growth performance and meat quality of broiler chickens was investigated. 2. A total of 900-d-old Arbor Acres broilers were allocated to three experimental treatments for 6 weeks. Chicks were administered with R. palustris in drinking water as follows: (i) control group without R. palustris; (ii) treatment 1 (R1) with R. palustris of 8 × 109 cells per chick per day in drinking water; (iii) treatment 2 (R2) with R. palustris of 1.6 × 1010 cells per chick per day in drinking water. 3. The results showed that, compared with that of control, both groups of R. palustris treatment increased daily weight gain and improved feed conversion ratio of broiler chickens significantly during the whole growing period of 6 weeks. 4. Both total and glutamic acid contents of chicken breast fillet in R. palustris treatment R2 were higher, while the fat content was lower, than those of the control group. Furthermore, R. palustris treatments also improved sensory attributes of chicken breast fillet. 5. As a probiotic providing rich nutrients and biological active substances, R. palustris administration in drinking water displayed a growth promoting effect and improved meat quality of broiler chickens.
INTRODUCTION In the poultry industry, antibiotics have been widely used for therapeutic, prophylactic and growth promotion purposes. However, improper use of antibiotics could cause bacterial resistance and antibiotic residues in poultry products, which could produce potential threats to humans, including allergic reactions and imbalances in intestinal microflora (Teuber, 2001; Dibner and Richards, 2005). Since 2006, the use of antibiotics as growth promoters in animal feed has been banned in the European Union (Castanon, 2007). Current research highlights the role of probiotics as an effective alternative to subtherapeutic antibiotics. Probiotics have been defined as “live microorganisms which, when administered in adequate amounts, confer a health benefit on the host” by improving its intestinal microbial balance, increasing digestive capacity, stimulating the
immune system and enhancing production performance (Patterson and Burkholder, 2003; Mountzouris et al., 2009). Previous studies on probiotic utilisation in poultry dominantly focus on various strains of Lactobacillus, Bifidobacterium, Enterococcus, Bacillus, Aspergillus and yeasts (Lee et al., 2007; Mountzouris et al., 2007; Samli et al., 2010; Molnár et al., 2011; Amirdahri et al., 2012). The photosynthetic bacterium R. palustris has generally been evaluated as a probiotic in aquaculture to enhance the growth performance of fish, improve water quality and maintain fish health (Zhou et al., 2010; Wang, 2011; Peirong and Wei, 2013). R. palustris supplemented diet also reduced the risk of atherosclerosis in rats (Lee et al., 1990; Tsujii et al., 2007). However, less information has been provided on the effect of R. palustris treatment, especially via drinking water, on poultry performance. In addition to
Correspondence to: Hai Yan, School of Chemistry and Biological Engineering, University of Science and Technology Beijing, Beijing 100083, China. E-mail: [email protected] Accepted for publication 14 January 2014.
© 2014 British Poultry Science Ltd
RHODOPSEUDOMONAS AND BROILER PERFORMANCE
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its functions as a probiotic, R. palustris also provides rich nutrients (Kim and Lee, 2000) and many bioactive ingredients including lycopene and coenzyme Q10 as a nutritional feed additive (Bao et al., 2010). Here, the effect of R. palustris on growth performance and meat quality of Arbor Acres broiler chickens was studied. Broiler performance parameters such as daily weight gain (DWG), feed conversion ratio (FCR) and chicken mortality were determined. Protein, fat, moisture, amino acid contents and sensory attributes of chicken breast meat were also measured to evaluate meat quality.
MATERIALS AND METHODS Probiotic strain and culture A bacteria strain of R. palustris (No. 1.2180) was bought from the China General Microbiological Culture Collection Center. It was cultured at 30°C and a light intensity of 3000 lx for 6 d using the medium previously reported (Chen et al., 2007). The cells were harvested using centrifugation at 18500 g for 20 min, then resuspended and washed twice with the drinking water of chicks. R. palustris suspension with the concentration of viable bacterial cells 8 × 1010 cells/ml was prepared and diluted daily with the drinking water of chicks.
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per day in drinking water. After receiving the required amount of R. palustris, water without R. palustris was supplied for further consumption ad libitum. Growth performance Body weight of birds was measured individually on a weekly basis. Dead birds were removed daily and weighed. The amounts of added feed to each pen and the residual feed remaining at the end of each week were accurately weighed and recorded. Feed consumption divided by body weight gain per day per chick was taken as FCR. The DWG of each weak and FCR in starter period (0–3 weeks), grower period (3–6 weeks) and overall (0–6 weeks) were calculated. Sample collection and analytical determinations At 6 weeks of age, 10 male chickens from each pen were selected randomly and killed by the conventional method at a slaughtering plant. Breast muscles from the right side of each carcass were excised and individually divided into two sections. One section was used for chemical composition analysis, whereas the other for sensory analyses. All the samples were stored in plastic bags at −20°C before analyses. For chemical composition and free amino acid analyses, 10 breast fillets from each pen were homogenised and mixed together as one sample. Protein, moisture
Birds and experimental treatments A total of 900 one-d-old Arbor Acres (AA) broiler chicks were randomly assigned to three experimental groups and raised for 6 weeks. Each treatment had 300 broilers arranged in three replicates of 100 chicks (50 male and 50 female) per replication. The chicks of each replicate were raised in floor pens (0.90 m2/bird) equipped with self-feed feeders and drinkers. Chicks were vaccinated at hatch for Marek’s disease, infectious bronchitis and Newcastle disease. The ambient temperature was 32°C on the first day, followed by a gradual decline in temperature to 24°C on d 21, and maintained at this temperature until termination of the experiment. All birds had access to feed ad libitum under continuous light conditions. The basal diet without any antibiotics or growth promoters was formulated for starter (0–3 weeks) and grower (3–6 weeks) periods (Table 1), and met or exceeded the nutrient requirements of broilers. The drinking water was untreated well water with pH 7.5 with free residual chlorine of 0 mg/l. The birds in control group received water without R. palustris. R. palustris treatment 1 (R1) had 8 × 109 R. palustris cells per chick per day in drinking water, while R. palustris treatment 2 (R2) had R. palustris of 1.6 × 1010 cells per chick
Table 1. Ingredients and composition of the basal diet
Ingredients (g/kg)
Starter
Grower
(0–3 weeks)
(3–6 weeks)
Maize 535.3 Soybean meal 355.2 Fish meal 39.9 Vegetable oil 35.2 Limestone 15.2 Sodium chloride 3.0 Monocalcium phosphate 9.2 2.0 Vitamin premixa 2.0 Mineral premixb DL-methionine 1.5 L-lysine 1.0 Choline chloride 0.5 Analysed and calculated chemical composition (g/kg) ME (MJ/kg) 12.9 Crude protein 221.6 Lysine 11.2 Methionine + cystine 8.5 Calcium 10.2 Total phosphorus 6.9
588.6 315.3 36.3 30.2 12.7 3.0 7.8 2.0 2.0 1.0 0.6 0.5 12.8 206.3 9.5 7.6 8.7 6.3
a Vitamin premix provided per kg of diet: retinol acetate 3.37 mg, cholecalciferol 0.05 mg, DL-α-tocopherol 40 mg, menadione 2 mg, thiamine 1 mg, riboflavin 7 mg, pyridoxine 6 mg, cyanocobalamine 0.035 mg, nicotine 50 mg, pantothenic acid 15 mg, folic acid 1.5 mg and biotin 0.15 mg. b Mineral premix provided per kg of diet: iron 70 mg, copper 9 mg, manganese 90 mg, zinc 60 mg, selenium 0.16 mg and iodine 0.5 mg.
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and fat contents in chicken breast fillet were determined by the AOAC Official Method.
RESULTS Growth performance
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Free amino acid analysis About 200 mg homogenate sample was extracted with 1.5 ml of methanol–water solution (1:1, v/v) for 30 min and then centrifuged at 10 000 g for 5 min. The supernatant was diluted with methanol–water solution at a 1:25 ratio. The dilute supernatant (40 μl) were labelled with iTRAQTM reagents (AA 45/32 kit, Applied Biosystems) and analysed on an Applied Biosystems SCIEX 3200 QTRAP® LC/MS/MS system equipped with Amino Acid Analyser (AAA) C18 Column (5 µm particle size, 4.6 mm diameter, 150 mm length). The contents of total amino acids, essential amino acids and glutamic acid, which is one important taste-active component for developing meat taste, were measured.
The effect of R. palustris treatment on DWG of male birds is shown in Table 2. No significant differences between the three treatment groups were seen for DWG in the starter period of 0–3 weeks. However, R. palustris treatments R1 and R2 showed higher DWG than that of control during the growing period of 3–6 weeks and the whole growing period of 0–6 weeks, suggesting R. palustris had a beneficial effect on the growth performance in the latter and whole periods. A similar effect was found in female birds (Table 3). Table 4 clearly shows how R. palustris treatment significantly reduced the FCR of the chicks. Overall for the entire experiment, there was significant difference (P < 0.05) in FCR of R1 and R2 (1.66 ± 0.021 and 1.71 ± 0.021, Table 2.
Sensory analyses Sensory characteristics of chicken breast fillet were evaluated by three groups of semi-trained students. Each group consisted of 15 students (20–28 years of age) with 8 males and 7 females. Before tasting, panellists were well instructed on the assessment criteria, meat attributes to be rated and how to properly complete the questionnaire. Chicken breast fillet samples were sliced into 1-cm-thick pieces and grilled until internal temperature reached 71–75°C. The samples were provided to the sensory panel using random threedigit numbers. The presentation order of samples and the first-order and carry-over effect were blocked. Each treated sample was tasted by at least three different panellists. Room temperature water was used to neutralise sensory perception between samples. The trial consisted of 6 sessions, and the traits assessed were meat colour, aroma strength, juiciness, flavour, texture and overall acceptability. A 9-point scale was used, 1 referring to extremely light, very weak, extremely dry, extremely unpleasant, extremely gooey and disagreeable, 9 referring to extremely dark, very strong, extremely juicy, extremely enjoyable, extremely smooth and enjoyable.
Statistical analysis The results were subjected to one-way analysis of variance using the general linear models (GLM) procedure of SPSS 19.0.0 software (2010, SPSS Inc., USA). Significance of differences (P < 0.05) was evaluated by Duncan’s test.
Effect of R. palustris treatment on daily weight gain of male birds (mean ± SEM) Daily weight gain of treatment groups (g)
Age in weeks 0–1 1–2 2–3 3–4 4–5 5–6 0–3 3–6 0–6
Control 20.26 30.81 73.41 94.87 93.76 82.38 41.49 90.34 65.91
± ± ± ± ± ± ± ± ±
0.25a 0.59a 0.80a 0.90a 1.54a 1.93a 0.52a 1.32a 0.89a
R1 22.28 32.45 74.98 88.20 93.40 112.49 43.24 98.03 70.63
± ± ± ± ± ± ± ± ±
R2 0.25b 0.60ab 0.82a 0.90b 1.53a 1.94b 0.51a 1.30b 0.90b
20.65 33.96 71.58 83.48 103.00 109.15 42.06 98.54 70.30
± ± ± ± ± ± ± ± ±
0.25a 0.59b 0.81a 0.88c 1.50b 1.77b 0.52a 1.28b 0.89b
a,b,c Mean values within the same row sharing a common superscript letter are not statistically different at P < 0.05. Control: without R. palustris. R1: R. palustris treatment with 8 × 109 R. palustris cells per chick per day in drinking water. R2: R. palustris treatment with 1.6 × 1010 R. palustris cells per chick per day in drinking water.
Table 3.
Effect of R. palustris treatment on daily weight gain of female birds (mean ± SEM) Daily weight gain of treatment groups (g)
Age in weeks 0–1 1–2 2–3 3–4 4–5 5–6 0–3 3–6 0–6
Control 21.42 28.49 58.07 68.41 74.89 75.00 36.00 72.77 54.38
± ± ± ± ± ± ± ± ±
0.25a 0.49a 0.69a 0.84a 1.29a 1.98a 0.46a 0.98a 0.71a
R1 21.87 30.44 57.27 75.77 92.74 98.73 36.53 89.08 62.80
± ± ± ± ± ± ± ± ±
R2 0.25a 0.50b 0.69a 0.84b 1.30b 1.95b 0.46a 0.97b 0.71b
21.84 28.08 62.68 74.97 90.71 80.47 37.54 82.05 59.79
± ± ± ± ± ± ± ± ±
0.25a 0.50a 0.69b 0.83b 1.29b 1.96a 0.46a 1.00c 0.72c
a,b,c Mean values within the same row sharing a common superscript letter are not statistically different at P < 0.05. Control: without R. palustris. R1: R. palustris treatment with 8 × 109 R. palustris cells per chick per day in drinking water. R2: R. palustris treatment with 1.6 × 1010 R. palustris cells per chick per day in drinking water.
RHODOPSEUDOMONAS AND BROILER PERFORMANCE
Table 4. Broiler feed conversion (feed/gain) ratio during the starter, grower and the entire experimental period (mean ± SEM)
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significantly different in essential amino acid content (Figure 1(e)) with respect to the control.
Feed conversion ratio of treatment groups (g) Age in week 0–3 3–6 0–6
Sensory attributes
Control
R1
R2
1.61 ± 0.02a 1.91 ± 0.02a 1.81 ± 0.02a
1.60 ± 0.02a 1.68 ± 0.02b 1.66 ± 0.02b
1.58 ± 0.02a 1.76 ± 0.02c 1.71 ± 0.02b
respectively) compared with the control (1.81 ± 0.021), while R1 and R2 did not differ. There were no treatment effects on bird mortality, which is consistent with that reported by O’Dea et al. (2006). Chemical composition and free amino acid analyses
DISCUSSION
90
b
b a
85 80 75 70
4 b
3 a
c
2
100
1
R2 b
a
Control
a
R1
Control
(e)
R2
Essential Amino Acid Content (mg/g)
R1
R1
a
a
a
Control
R1
R2
60 40 20
R2 (f)
20 15
80
0
0 Control
(d) 80 70 60 50 40 30 20 10 0
(c)
(b) 5
Moisture Content (%)
95
In this work, administration of R. palustris in drinking water significantly increased DWG of broilers, especially during the late growth period. These findings are in agreement with those of Alkhalf et al. (2010), concluding that a commercial probiotic Pediococcus acidilactici improved DWG of broilers compared with control treatment after 3 weeks of age. Gao et al. (2008) also showed that DWG of broilers fed on a diet supplemented with 2.5 g/kg of yeast culture was significantly better than that of control during grower and overall periods. Probiotic treatment is known to benefit the host animals by improving their intestinal microflora balance, which could increase the
a
a b
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Glutamic Acid Content (mg/g)
100
Fat Content (%)
(a) Protein Content (g/100 g dry weight)
The protein content, fat content, moisture content and amino acid contents of chicken breast fillet are presented in Figure 1(a–f). Figure 1(a) shows that the protein contents of the breast meat in two R. palustris treatments were significantly higher than that of control group, while the moisture content had no changes (Figure 1(c)). Figure 1(b) shows that the chicken breast fillet of R. palustris treatment R2 had a lower fat percentage (6.5%) than that of the control group (7.9%) and R. palustris treatment R1 (10.6%). Both total amino acid content (65.2 mg/g) and glutamic acid content (4.2 mg/g) (Figure 1(d, f)) of chicken breast fillet in R. palustris treatment R2 were higher than those of control, but not
Total Amino Acid Content (mg/g)
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a,b,c Mean values within the same row sharing a common superscript letter are not statistically different at P < 0.05. Control: without R. palustris. R1: R. palustris treatment with 8 × 109 R. palustris cells per chick per day in drinking water. R2: R. palustris treatment with 1.6 × 1010 R. palustris cells per chick per day in drinking water.
To assess meat quality, sensory attributes such as meat colour, aroma strength, juiciness, flavour, texture and overall acceptability of chicken breast fillet were determined in our study (Figure 2). Statistically significant effects of the probiotic treatments on the improvement of meat colour and juiciness were found (P < 0.05), as well as lower values of flavour and texture for control than the two R. palustris treatments (P < 0.05, Figure 2). However, no differences were noticed between the two R. palustris treatments. The remaining sensory attribute aroma strength was not affected by R. palustris treatments. Finally, for overall acceptability, two R. palustris treatments were significant higher than control (P < 0.05).
6 5 4
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a
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0 Control
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Figure 1. Effect of R. palustris treatment on meat quality of broiler chickens. Error bars represent standard deviations (n = 3). Control: without R. palustris, R1: R. palustris treatment with 8 × 109 R. palustris cells per chick per day in drinking water and R2: R. palustris treatment with 1.6 × 1010 R. palustris cells per chick per day in drinking water.
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Figure 2. Comparison of meat colour, aroma strength, juiciness, flavour, texture and overall acceptability of chicken breast fillet between the control group and R. palustris treated groups. A 9-point scale was used where the meat colour ranged from extremely light to extremely dark, aroma strength from very weak to very strong, juiciness from extremely dry to extremely juicy, flavour from extremely unpleasant to extremely enjoyable, texture from extremely gooey to extremely smooth and overall acceptability from disagreeable to enjoyable. Error bars represent standard deviations (n = 15).
efficiency of digestion and nutrient absorption processes and enhance growth and improve feed efficiency, as found in poultry (Lu et al., 2003; Djouvinov, 2005), mammals (Guerra et al., 2007; Scharek et al., 2007) and aquatic animals (Yanbo and Zirong, 2006; Wang, 2011). Intestinal microflora balance is always dynamic (Sonnenburg et al., 2006; El-Shibiny et al., 2007), and early intestinal bacterial community of broiler chickens is relatively transient and is replaced by a stable one with increasing complexity as the chicks age (Lu et al., 2003). So the beneficial effect occurred after the stable intestinal bacterial community had been established, which is about the third week found in our study. As shown in Table 4, R. palustris treatment significantly reduced the FCR of the chicks. An improvement in FCR of broilers by feeding probiotic has been evidenced in many studies (Karimi Torshizi et al., 2010; Molnár et al., 2011; Lv et al., 2012). FCR is not a simple index of feed intake, but it reflects the relationship between feed utilisation and actual body weight gain. Although probiotic supplement to the chicks may lead to more appetitive foraging, an improvement in the intestinal environment which includes gut microflora, gut maintenance, mucus production and host immune function could improve the digestibility of feed, promote the absorption of nutrients and thus promote growth, decrease FCR and reduce the production cost (Mountzouris et al., 2007). However, some studies reported that probiotic supplementation did not affect FCR of chickens (Huang et al., 2004; Biernasiak and Slizewska, 2009; Navidshad et al., 2010). These varying results may be due to differences in the bacterial strains, dosages and broiler growth stages. In our study, treatment R1 with R. palustris of 8 × 109 cells per chick per day in drinking water could supply
adequate amounts of probiotics to get beneficial effects on growth performance and FCR of broilers. In addition to a probiotic effect, R. palustris itself can also be a nutritious feed additive, containing high contents of protein and many bioactive ingredients such as lycopene and coenzyme Q10, which is widely used in aquaculture for feeding fish and shrimp (Kim and Lee, 2000). Studies showed that lycopene supplementation increased the final live weight of broilers (Sevcikova et al., 2008) and decreased the cholesterol content of chicken leg meat (Englmaierova et al., 2011). Coenzyme Q10 is a component of the electron transport chain, generating energy in the form of ATP. Karadas et al. (2011) found that coenzyme Q10 also plays an important role in chick viability as an antioxidant, but in most of the tissues its concentrations decreased substantially between 18 h and 36 h post-hatch. In this study, R. palustris treatment could supply lycopene and exogenous coenzyme Q10 for the chickens to improve energy generation, resistance to oxidative stress and to benefit to growth performance. Protein, fat and water are the basic components of poultry meat. In meat products, proteins and carbohydrates are used in combination with water to produce gels to get the elastic, soft and juicy texture (Chizzolini et al., 1999). Protein contents of the breast meat in two R. palustris treatments were significantly higher than the control group, suggesting that R. palustris treatment could maintain the texture quality of meat, which also coincided with the sensory attributes (Figure 2). Excess fat deposition is supposed to be the main negative effect of nutrition (Jiménez-Colmenero et al., 2001). In our study, fat content (Figure 1 (b)) of breast meat was significantly decreased by
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RHODOPSEUDOMONAS AND BROILER PERFORMANCE
the R2 treatment, which could provide low-fat meat as healthy food materials. Flavour is one of the most significant factors influencing the quality of meat products. As we know, most of the meat flavour develops during cooking. The main reactions are the Maillard reaction between reducing sugars and amino acids, the thermal degradation of lipid and Maillard–lipid interactions (Mottram, 1998; Jayasena et al., 2013). Some amino acids such as serine, glutamic acid, glycine, isoleucine, leucine, alanine and proline contribute to the rich full flavour of meat (Imanari et al., 2007; Liu et al., 2007, 2012). As one important taste-active component, glutamic acid could enhance meat taste including delicious, umami and brothy tastes. Among chicken, pork and beef, chicken contained the most free glutamic acid (Imanari et al., 2008; Jayasena et al., 2013). In our study, the concentration of glutamic acid in chicken breast fillet exceeded the threshold concentration for umami taste (Chen and Zhang, 2007). The amino acid contents of chicken breast fillet in R. palustris treatment R2 were higher in both total amino acids and glutamic acid. In sensory analyses, statistically significant effects of R. palustris treatment on the improvement of flavour and overall acceptability were also found, which suggested that R. palustris treatment induced an increase in amino acid content of meat and improved meat taste. Our study showed that the supplement of R. palustris, especially in high levels, made a great contribution to nutritional and sensorial quality improvements of meat. These results could be due to rich nutrients and biological active substances provided by R. palustris. In conclusion, administration of R. palustris in drinking water significantly improved DWG and FCR of broilers, but no effect on mortality was found. The breast meat of chickens in the R. palustris treatments, especially in high levels of R. palustris supplement, had increased contents of total and glutamic acid and decreased fat content. Furthermore, improvement in sensory attributes was observed in broilers fed with R. palustris. As a potential probiotic which also provides rich nutrients and biological active substances, R. palustris can be recommended to be used for increasing growth performance and meat quality of broiler chickens.
ACKNOWLEDGEMENTS The authors wish to acknowledge the Fundamental Research Funds for the Central Universities [grant number FRF-AS-10-001B] and Beijing Municipal Science and Technology Commission [grant number z131102002813058] for financial support of this research.
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REFERENCES ALKHALF, A., ALHAJ, M. & AL-HOMIDAN, I. (2010) Influence of probiotic supplementation on blood parameters and growth performance in broiler chickens. Saudi Journal of Biological Sciences, 17: 219–225. doi:10.1016/j. sjbs.2010.04.005. AMIRDAHRI, S., JANMOHAMMADI, H., TAGHIZADEH, A. & RAFAT, A. (2012) Effect of dietary Aspergillus meal prebiotic on growth performance, carcass characteristics, nutrient digestibility, and serum lipid profile in broiler chick lowprotein diets. Turkish Journal of Veterinary & Animal Sciences, 36: 602–610. BAO, Y.X., YAN, H., LIU, L.Q. & XU, Q.Q. (2010) Efficient extraction of lycopene from Rhodopseudomonas palustris with n-hexane and methanol after alkaline wash. Chemical Engineering & Technology, 33: 1665–1671. doi:10.1002/ ceat.201000033. BIERNASIAK, J. & SLIZEWSKA, K. (2009) The effect of a new probiotic preparation on the performance and faecal microflora of broiler chickens. Veterinarni Medicina, 54: 525–531. CASTANON, J.I.R. (2007) History of the use of antibiotic as growth promoters in European poultry feeds. Poultry Science, 86: 2466–2471. doi:10.3382/ps.2007-00249. CHEN, C.Y., LU, W.B., WU, J.F. & CHANG, J.S. (2007) Enhancing phototrophic hydrogen production of Rhodopseudomonas palustris via statistical experimental design. International Journal of Hydrogen Energy, 32: 940–949. doi:10.1016/j. ijhydene.2006.09.021. CHEN, D.-W. & ZHANG, M. (2007) Non-volatile taste active compounds in the meat of Chinese mitten crab (Eriocheir sinensis). Food Chemistry, 104: 1200–1205. doi:10.1016/j. foodchem.2007.01.042. CHIZZOLINI, R., ZANARDI, E., DORIGONI, V. & GHIDINI, S. (1999) Calorific value and cholesterol content of normal and low-fat meat and meat products. Trends in Food Science & Technology, 10: 119–128. doi:10.1016/S0924-2244(99) 00034-5. DIBNER, J.J. & RICHARDS, J.D. (2005) Antibiotic growth promoters in agriculture: history and mode of action. Poultry Science, 84: 634–643. doi:10.1093/ps/84.4.634. DJOUVINOV, D. (2005) Effect of feeding Lactina probiotic on performance, some blood parameters and caecalmicroflora of mule duckings. Trakia Journal of Sciences, 3: 22–28. EL-SHIBINY, A., CONNERTON, P.L. & CONNERTON, I.F. (2007) Campylobacter succession in broiler chickens. Veterinary Microbiology, 125: 323–332. doi:10.1016/j. vetmic.2007.05.023. ENGLMAIEROVA, M., BUBANCOVA, I., VIT, T. & SKRIVAN, M. (2011) The effect of lycopene and vitamin E on growth performance, quality and oxidative stability of chicken leg meat. Czech Journal of Animal Science, 56: 536–543. GAO, J., ZHANG, H.J., YU, S.H., WU, S.G., YOON, I., QUIGLEY, J., GAO, Y.P. & QI, G.H. (2008) Effects of yeast culture in broiler diets on performance and immunomodulatory functions. Poultry Science, 87: 1377–1384. doi:10.3382/ps.2007-00418. GUERRA, N.P., BERNÁRDEZ, P.F., MÉNDEZ, J., CACHALDORA, P. & PASTRANA CASTRO, L. (2007) Production of four potentially probiotic lactic acid bacteria and their evaluation as feed additives for weaned piglets. Animal Feed Science and Technology, 134: 89–107. doi:10.1016/j. anifeedsci.2006.05.010. HUANG, M., CHOI, Y., HOUDE, R., LEE, J., LEE, B. & ZHAO, X. (2004) Effects of Lactobacilli and an acidophilic fungus on the production performance and immune responses in broiler chickens. Poultry Science, 83: 788–795. doi:10.1093/ ps/83.5.788. IMANARI, M., KADOWAKI, M. & FUJIMURA, S. (2007) Regulation of taste-active components of meat by dietary leucine. British Poultry Science, 48: 167–176. doi:10.1080/ 00071660701244738.
Downloaded by [Memorial University of Newfoundland] at 09:56 01 August 2014
366
Q.Q. XU ET AL.
IMANARI, M., KADOWAKI, M. & FUJIMURA, S. (2008) Regulation of taste-active components of meat by dietary branched-chain amino acids; effects of branched-chain amino acid antagonism. British Poultry Science, 49: 299–307. doi:10.1080/ 00071660802155080. JAYASENA, D.D., AHN, D.U., NAM, K.C. & JO, C. (2013) Flavour chemistry of chicken meat: a review. Asian-Australasian Journal of Animal Sciences, 26: 732–742. doi:10.5713/ ajas.2012.12619. JIMÉNEZ-COLMENERO, F., CARBALLO, J. & COFRADES, S. (2001) Healthier meat and meat products: their role as functional foods. Meat Science, 59: 5–13. doi:10.1016/S0309-1740(01) 00053-5. KARADAS, F., SURAI, P.F. & SPARKS, N.H.C. (2011) Changes in broiler chick tissue concentrations of lipid-soluble antioxidants immediately post-hatch. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 160: 68–71. doi:10.1016/j.cbpa.2011.05.006. KARIMI TORSHIZI, M.A., MOGHADDAM, A.R., RAHIMI, S. & MOJGANI, N. (2010) Assessing the effect of administering probiotics in water or as a feed supplement on broiler performance and immune response. British Poultry Science, 51: 178–184. doi:10.1080/00071661003753756. KIM, J.K. & LEE, B.-K. (2000) Mass production of Rhodopseudomonas palustris as diet for aquaculture. Aquacultural Engineering, 23: 281–293. doi:10.1016/S01448609(00)00057-1. LEE, M.G., KOBAYASHI, M. & YASUMOTO, K. (1990) Hypocholesterolemic effect of phototrophic bacterial cells in rats. Journal of Nutritional Science and Vitaminology, 36: 475–483. doi:10.3177/jnsv.36.475. LEE, S., LILLEHOJ, H.S., PARK, D.W., HONG, Y.H. & LIN, J.J. (2007) Effects of Pediococcus- and Saccharomyces-based probiotic (MitoMax®) on coccidiosis in broiler chickens. Comparative Immunology Microbiology and Infectious Diseases, 30: 261–268. doi:10.1016/j.cimid.2007.02.002. LIU, X.L., YAN, H., LV, L., XU, Q.Q., YIN, C.H., ZHANG, K.Y., WANG, P. & HU, J.Y. (2012) Growth performance and meat quality of broiler chickens supplemented with Bacillus licheniformis in drinking water. Asian-Australasian Journal of Animal Sciences, 25: 682–689. doi:10.5713/ ajas.2011.11334. LIU, Y., XU, X.-L. & ZHOU, G.-H. (2007) Changes in taste compounds of duck during processing. Food Chemistry, 102: 22–26. doi:10.1016/j.foodchem.2006.03.034. LU, J., IDRIS, U., HARMON, B., HOFACRE, C., MAURER, J.J. & LEE, M. D. (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Applied and Environmental Microbiology, 69: 6816–6824. doi:10.1128/ AEM.69.11.6816-6824.2003. LV, L., YAN, H., LIU, X.L., XU, Q.Q. & YIN, C.H. (2012) Growth performance and meat quality of broiler chickens supplemented with chicken-specific Lactobacillus CSL-13 in drinking water. Indian Journal of Animal Sciences, 82: 1415–1422. MOLNÁR, A.K., PODMANICZKY, B., KÜRTI, P., TENK, I., GLÁVITS, R., VIRÁG, G.Y. & SZABÓ, Z.S. (2011) Effect of different concentrations of Bacillus subtilis on growth performance, carcase quality, gut microflora and immune response of broiler chickens. British Poultry Science, 52: 658–665. doi:10.1080/ 00071668.2011.636029. MOTTRAM, D.S. (1998) Flavour formation in meat and meat products: a review. Food Chemistry, 62: 415–424. doi:10.1016/ S0308-8146(98)00076-4. MOUNTZOURIS, K.C., TSIRTSIKOS, P., KALAMARA, E., NITSCH, S., SCHATZMAYR, G. & FEGEROS, K. (2007) Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler
performance and modulating cecal microflora composition and metabolic activities. Poultry Science, 86: 309–317. doi:10.1093/ps/86.2.309. MOUNTZOURIS, K.C., BALASKAS, C., XANTHAKOS, I., TZIVINIKOU, A. & FEGEROS, K. (2009) Effects of a multi-species probiotic on biomarkers of competitive exclusion efficacy in broilers challenged with Salmonella enteritidis. British Poultry Science, 50: 467–478. doi:10.1080/00071660903110935. NAVIDSHAD, B., ADIBMORADI, M. & ANSARI PIRSARAEI, Z. (2010) Effects of dietary supplementation of Aspergillus originated prebiotic (Fermacto) on performance and small intestinal morphology of broiler chickens fed diluted diets. Italian Journal of Animal Science, 9: 55–60. doi:10.4081/ijas.2010.e12. O’DEA, E.E., FASENKO, G.M., ALLISON, G.E., KORVER, D.R., TANNOCK, G.W. & GUAN, L.L. (2006) Investigating the effects of commercial probiotics on broiler chick quality and production efficiency. Poultry Science, 85: 1855–1863. PATTERSON, J.A. & BURKHOLDER, K.M. (2003) Application of prebiotics and probiotics in poultry production. Poultry Science, 82: 627–631. doi:10.1093/ps/82.4.627. PEIRONG, Z. & WEI, L. (2013) Use of fluidized bed biofilter and immobilized Rhodopseudomonas palustris for ammonia removal and fish health maintenance in a recirculation aquaculture system. Aquaculture Research, 44: 327–334. doi:10.1111/j.1365-2109.2011.03038.x. SAMLI, H.E., DEZCAN, S., KOC, F., OZDUVEN, M.L., OKUR, A.A. & SENKOYLU, N. (2010) Effects of Enterococcus faecium supplementation and floor type on performance, morphology of erythrocytes and intestinal microbiota in broiler chickens. British Poultry Science, 51: 564–568. doi:10.1080/ 00071668.2010.507241. SCHAREK, L., ALTHERR, B.J., TÖLKE, C. & SCHMIDT, M.F.G. (2007) Influence of the probiotic Bacillus cereus var. toyoi on the intestinal immunity of piglets. Veterinary Immunology and Immunopathology, 120: 136–147. doi:10.1016/j. vetimm.2007.07.015. SEVCIKOVA, S., SKRIVAN, M. & DLOUHA, G. (2008) The effect of lycopene supplementation on lipid profile and meat quality of broiler chickens. Czech Journal of Animal Science, 53: 431–440. SONNENBURG, J.L., CHEN, C.T.L. & GORDON, J.I. (2006) Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLOS Biology, 4: e413. doi:10.1371/journal.pbio.0040413. TEUBER, M. (2001) Veterinary use and antibiotic resistance. Current Opinion in Microbiology, 4: 493–499. doi:10.1016/ S1369-5274(00)00241-1. TSUJII, H., NISHIOKA, M., SALMA, U., MIAH, A.G., MAKI, T. & LEE, M.G. (2007) Comparative study on hypocholesterolemic effect of Rhodopseudomonas palustris and Rhodobacter capsulatus on rats fed a high cholesterol diet. Animal Science Journal, 78: 535–540. doi:10.1111/j.1740-0929.2007.00473.x. WANG, Y. (2011) Use of probiotics Bacillus coagulans, Rhodopseudomonas palustris and Lactobacillus acidophilus as growth promoters in grass carp (Ctenopharyngodon idella) fingerlings. Aquaculture Nutrition, 17: e372–e378. doi:10.1111/j.1365-2095.2010.00771.x. YANBO, W. & ZIRONG, X.U. (2006) Effect of probiotics for common carp (Cyprinus carpio) based on growth performance and digestive enzyme activities. Animal Feed Science and Technology, 127: 283–292. doi:10.1016/j. anifeedsci.2005.09.003. ZHOU, X.X., TIAN, Z.Q., WANG, Y.B. & LI, W.F. (2010) Effect of treatment with probiotics as water additives on tilapia (Oreochromis niloticus) growth performance and immune response. Fish Physiology and Biochemistry, 36: 501–509. doi:10.1007/s10695-009-9320-z.
