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ANIMAL NUTRITION |
Department of Animal Science, University of Illinois, Urbana 61801
Abstract
Four trials investigated the effect of high levels of three phytase enzymes on P and protein utilization in chicks. The three phytases were derived from Aspergillus (Fungal Phytase 1), Peniophora (Fungal Phytase 2), and E. coli. Within each assay, 8-d-old male chicks were given ad libitum access to their experimental diet for 10 to 14 d. For Trials 1, 2, and 3, the basal diet was a corn-soybean meal diet deficient in P that was analyzed to contain 23% CP and 0.38% total P (0.10% estimated available P, as-fed basis). Phytase supplementation levels were based on the assessment of phytase premix activity (i.e., P release from Na phytate at pH 5.5 and 37°C). In Trial 1, supplementation of inorganic P from KH2PO4 (0 to 0.20%) resulted in a quadratic (P < 0.05) response in weight gain, gain:feed, and tibia ash concentration but a linear (P < 0.01) increase in tibia ash weight. Tibia ash was higher (P < 0.01) for chicks fed E. coli phytase than for those fed Fungal Phytase 1 at 500, 1,000, and 5,000 phytase units (FTU)/kg, but did not differ between these two phytases at 10,000 FTU/kg. In Trial 2, E. coli phytase supplementation at 1,000 FTU/kg maximized growth and bone responses, whereas addition of either of the two fungal phytases resulted in increasing responses up to 5,000 and 10,000 FTU/kg. Dietary addition of Fungal Phytase 2 resulted in the poorest (P < 0.01) responses among the three phytases. Escherichia coli phytase supplementation at 10,000 FTU/kg in Trial 3 resulted in tibia ash (millligrams) responses that were greater (P < 0.05) than those resulting from either 0.35% inorganic P supplementation or 10,000 FTU/kg of Fungal Phytase 1 or 2. Trial 4 showed that E. coli phytase supplementation at either 500 or 10,000 FTU/kg did not improve protein efficiency ratio (gain per unit of protein intake) of chicks fed low-protein soybean meal or corn gluten meal diets that were first-limiting in either methionine or lysine, respectively. These results demonstrate that high dietary levels of efficacious phytase enzymes can release most of the P from phytate, but they do not improve protein utilization.
Key Words: Chicks • Phosphorus • Phytase • Protein Utilization
Introduction
Through characterizing the P-releasing efficacy of a new Escherichia coli-derived phytase, namely, EcoPhos (ECP), our laboratory showed that the efficacy of two commercially available fungal phytases—Natuphos (FP1) and Ronozyme (FP2)—was unexpectedly low in the chick, but was higher in the young pig (Augspurger et al., 2003
). These were not the first data to show low efficacy for the fungal phytases in chicks, as Angel et al. (2001a,b) also showed low-efficacy values for FP1 in chicks but not in turkey poults. Recent work by Shirley and Edwards (2003) showed that supplementation of FP1 at a level of 12,000 phytase units (FTU)/kg resulted in almost complete digestion and release of the dietary phytate-P, which shows that FP1, at a high level, is capable of hydrolyzing phytate-P almost completely.
Previous work in our laboratory has shown no effect of phytase supplementation on protein utilization in chicks (Peter et al., 2000; Boling-Frankenbach et al., 2001; Peter and Baker, 2001). The effect of phytase supplementation on protein or amino acid digestibility in chickens and pigs has been inconsistent, with some finding a positive effect (Mroz et al., 1994; Ravindran et al., 1999; Zhang et al., 1999) but others finding no effect (Biehl and Baker, 1997a; Traylor et al., 2001; Snow et al., 2003). Even as positive digestibility responses have been found, they did not translate into positive effects on weight gain or protein efficiency ratio (PER; Zhang et al., 1999). Most of this work was carried out using standard phytase activity levels (i.e., 500 to 1,000 FTU/kg). Very high levels of phytase supplementation would test the concept of phytase-mediated responses in PER. Hence, the objectives of the research presented herein were to determine the effect of high levels of phytase activity on P and protein utilization and to compare those effects across three phytase sources: two commercially available fungal-derived phytases (FP1 and FP2) and one E. coli-derived phytase (ECP).
Materials and Methods
General Procedures
The University of Illinois Institutional Animal Care and Use Committee approved all housing, handling, and killing procedures. Four chick trials were carried out to determine the effect of high dietary phytase levels on P and protein utilization in young chicks. Trials 1, 2, and 4 were done using New Hampshire x Columbian Plymouth Rock male chicks, whereas Trial 3 was done using Ross x Ross male chicks. Chicks were housed in thermostatically controlled starter batteries with raised wire floors in an environmentally controlled building that provided 24 h of light. Both feed and water were provided for ad libitum consumption. After a period of overnight feed withdrawal, chicks were weighed, and chicks within a narrow weight range were selected. The selected chicks were then wing-banded and randomly assigned to pens, which were randomly assigned to dietary treatments. Five replicate pens of four chicks per pen were allowed to consume each experimental diet from d 8 to 18 (Trial 4), d 21 (Trial 1), or d 22 (Trials 2 and 3) after hatching.
The basal diet for Trials 1, 2, and 3 (Table 1) was a corn-soybean meal (SBM) diet, with no supplemental inorganic P (iP), designed to be deficient in P but super-adequate in cholecalciferol (25 µg/kg diet). It contained 0.38% total P and an estimated 0.10% bioavailable P (as-fed basis; NRC, 1994). Previous research in our laboratory had demonstrated that chicks fed this basal diet would respond linearly to supplemental iP levels (reagent-grade KH2PO4, 22.76% P) between 0 and 0.15% (Biehl et al., 1995; Biehl and Baker, 1997b; Augspurger et al., 2003).
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).
Phytase Sources
Two fungal phytases, Natuphos (FP1; BASF, Mt. Olive, NJ) and Ronozyme (FP2; Roche, Parsippany, NJ) and one bacterial phytase EcoPhos (ECP; Phytex LLC, Portland, ME), were used in these experiments. Fungal Phytase 1 (manufacturer’s guarantee of 5,000 FTU/g premix, analyzed activity of 5,000 FTU/g premix) is a recombinant enzyme from Aspergillus ficuum that is classified as a 3-phytase, with hydrolysis of the phosphate moiety being initiated at the 3-position on the phytate molecule. Fungal Phytase 1 exhibits optimal activity at pH 2.5 and 5.5. Fungal Phytase 2 (manufacturer’s guarantee of 2,500 FTU/g premix, analyzed activity of 2,850 FTU/g premix) is a recombinant phytase from Peniophora lycii that is classified as a 6-phytase and exhibits optimal phytase activity at pH 4.0 to 4.5 (Lassen et al., 2001). The phytase ECP (analyzed activity of 64,820 FTU/g premix) was cloned from E. coli and expressed in a yeast system as described by Rodriguez et al. (1999a,b; 2000). Classified as a 6-phytase, it is a recombinant enzyme produced from the appA2 gene isolated from E. coli obtained from pig intestine (Rodriguez et al., 1999a). The phytase ECP exhibits optimal activity at pH 2.5 to 3.5 (Rodriguez et al., 1999a). A similar E. coli-derived phytase was shown to be more resistant to the gastric enzyme pepsin than FP1 (Rodriguez et al., 1999b). Each phytase enzyme was assayed for phytase activity before inclusion in experimental diets as described previously by Han et al. (1999). One phytase unit (FTU) was defined as the amount of enzyme required to release 1 µmol of iP per minute from sodium phytate at 37°C and pH 5.5.
Trial 1
The objective of this trial was to compare the P-releasing efficacy of FP1 and ECP at a range of phytase activity levels. For this trial, calcium (Ca) was set at 0.75% in an effort to control Ca:P imbalance and thereby allow maximum responses to supplemental iP or phytase. The basal diet was supplemented with five graded levels of iP (0, 0.05, 0.10, 0.15, and 0.20%) from reagent-grade KH2PO4 to establish a standard curve. Additions of FP1 and ECP to the basal diet were made to accomplish dietary phytase activity levels of 500, 1,000, 5,000, and 10,000 FTU/kg. Phosphorus and phytase additions were made at the expense of cornstarch.
Trial 2
The objective of this trial was to clarify the results of Trial 1 that showed significantly higher bone ash values for the highest phytase activity levels compared to the diets supplemented with 0.20% iP. In this trial, Ca was increased to 1.0%, and FP2 was included in the comparison of the phytases. Experimental diets included five graded levels of supplemental iP (as in Trial 1) and the addition of FP1, FP2, and ECP at dietary phytase activity levels of 1,000, 5,000, and 10,000 FTU/kg.
Trial 3
The objective of this trial was to compare the effects on tibia ash of a high dietary phytase level to adequate P supplementation in commercial broiler chicks. Experimental diets included the P-deficient basal diet (0.75% Ca, as in Trial 1) unsupplemented or supplemented with 0.35% iP (KH2PO4); 5,000 FTU/kg from ECP; or 10,000 FTU/kg from either ECP, FP1, or FP2.
Trial 4
The objective of this trial was to determine the effect of high dietary phytase levels on protein utilization in chicks. Dehulled SBM, first-limiting in sulfur AA (Emmert and Baker, 1995; Emmert et al., 2000), and corn gluten meal (CGM), first-limiting in Lys (Peter et al., 2000), were added at the expense of cornstarch to a cornstarch-dextrose basal diet (Table 1
) to achieve 15% CP in each diet. The SBM was analyzed to contain 49.0% CP, and it provided 0.40% dietary digestible sulfur AA (0.20% dietary digestible Met; Emmert et al., 2000). This level of SAA represents approximately 50% of the digestible SAA requirement for 0- to 3-wk-old chicks (NRC, 1994). The CGM was analyzed to contain 64.6% CP, and it provided 0.18% dietary digestible Lys (Peter et al., 2000). This level of Lys represents only 17% of the digestible Lys requirement for 0- to 3-wk-old chicks (NRC, 1994). Each protein source was subjected to Kjeldahl N and total P analysis (AOAC, 1995) before diet formulation. The basal diet contained 0.38% available P and 0.89% Ca, and, as protein sources were added, final diets were made adequate and similar in Ca (1.0%) and available P (0.45%) through the addition of limestone and dicalcium phosphate. Phytase, that is, ECP, was added to each protein source at either 500 or 10,000 FTU/kg of diet to determine the effect of a normal or a high level of phytase on protein efficiency ratio (grams of gain per gram of CP consumed) of chicks.
Diet Analyses
Crude protein in all basal diets was determined in triplicate (AOAC, 1995), and amino acids were quantified in duplicate by chromatographic analysis (Model 6300, Beckman Instruments, Palo Alto, CA) following 24-h hydrolysis in HCl. Quadruplicate samples of basal diets from each of the trials were dry-ashed as described for the bones and then wet-ashed for quantification of total P (Augspurger et al., 2003).
Statistical Analyses
Within each trial, analysis of variance was performed on pen means data using the general linear models procedure of SAS (SAS Inst. Inc., Cary, NC) appropriate for a completely randomized design. Treatment means were compared using orthogonal and nonorthogonal single-df comparisons. For Trials 1 and 2, tibia ash (milligrams) per chick was regressed on supplemental iP intake (grams) to construct standard curves. Using bone ash responses to supplemental phytase, the regression equation was solved for bioavailable P intake (grams) and the solution was divided by feed intake and multiplied by 100 to yield bioavailable P release.
Results
Trial 1
Weight gain, gain:feed ratio, and tibia ash percentage increased quadratically (P < 0.05) with increasing levels of supplemental iP (Table 2). Tibia ash weight increased linearly (P < 0.01) as iP was supplemented, but regression of bone ash (milligrams) on supplemental iP intake was quadratic (P < 0.05) up to 0.20% iP supplementation. Omission of the highest level of supplemental iP resulted in a linear (P < 0.01) standard curve regression equation (r2 = 0.95). Weight gain and gain:feed ratio were higher for chicks fed ECP than for those fed FP1 at 500 and 1,000 FTU/kg, but were similar between the two phytases at the higher phytase activity levels (phytase source x activity level interaction, P < 0.01). Tibia ash (percentage and milligrams) was higher for chicks fed ECP than for those fed FP1 up to 5,000 FTU/kg but was similar for ECP and FP1 at 10,000 FTU/kg (phytase source x activity level interaction, P < 0.01). Phytase supplementation at 10,000 FTU/kg produced tibia ash (milligrams) responses that were greater (P < 0.05) than those achieved with supplementation of 0.20% iP.
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). Tibia ash weight increased linearly (P < 0.01) with increasing supplemental iP, whereas tibia ash percentage responded quadratically (P < 0.01) to supplemental iP levels. There was a phytase source (ECP vs. FP1 and FP2) x activity level (1,000 vs. higher) interaction (P < 0.01) for all response criteria, such that ECP maximized responses at 1,000 FTU/kg, whereas responses to the two fungal phytases increased with increasing activity levels but not to levels similar to those of ECP. Supplementation of ECP, regardless of activity level, produced tibia ash (milligrams) responses that were greater (P < 0.01) than those achieved with supplementation of 0.20% iP.
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). Dietary additions of ECP or FP1 produced greater (P < 0.05) weight gains than that from FP2. Tibia ash weights and concentrations were greater (P < 0.01) for ECP than for FP1 or FP2, with FP1 producing greater (P < 0.01) responses in those criteria than FP2. Supplemental ECP, but not FP1 or FP2, resulted in greater (P < 0.01) tibia ash weights than iP supplementation.
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). Regardless of level of supplementation, ECP supplementation did not affect (P > 0.10) any of the response criteria.
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These data show that phytase, either from ECP or FP1, was very efficacious for improving P utilization when supplemented at extremely high levels. In each of the three trials, supplementation of ECP or FP1 at 10,000 FTU/kg resulted in tibia ash (milligrams) values that were higher than those from 0.20% iP addition (Trials 1 and 2) or, for ECP, higher than those resulting from 0.35% iP supplementation (Trial 3). Extrapolation of the standard-curve regression equations generated in Trials 1 and 2 showed that ECP and FP1 supplemented at 10,000 FTU/kg released 0.196% and 0.191% P from diets containing 0.75% Ca in Trial 1, and 0.290% and 0.238% from diets containing 1.00% Ca in Trial 2, respectively (data not shown). These numbers equate to a release of approximately 70 (Trial 1) to 100% (Trial 2) of the phytate-P present in the diet. This is supported by data reported by Shirley and Edwards (2003) that showed that 12,000 FTU/kg of FP1 made approximately 95% of the phytate-P available for utilization by the chick.
We reported recently that the P-releasing efficacy of ECP was approximately threefold greater than FP1 or FP2 in the chick (Augspurger et al., 2003). The results herein support our earlier data, in the sense that, at lower levels of phytase activity (i.e., 500 and 1,000 FTU/kg), ECP maintained a greater than threefold advantage in P-releasing efficacy over FP1 and FP2. As phytase activity was increased up to 5,000 and 10,000 FTU/kg, however, the efficacy of FP1 became similar to that of ECP, but the efficacy of FP2, although increasing, still was only 50% of that of ECP. Whereas other researchers have shown a low efficacy of FP1 in chicks fed lower doses (Angel et al., 2001a), our work along with that of Shirley and Edwards (2003) showed that at a high level of activity, FP1 maximized P utilization, indicating that the proper dose of FP1 needed in a commercial broiler setting may need revision. The low efficacy of FP2, even at 10,000 FTU/kg, is particularly troubling and requires continued research into the reason behind its poor relative efficacy in chicks.
The basis herein for dietary addition of phytase premixes was activity determination (of premixes) at pH 5.5. As pointed out previously (Augspurger et al., 2003), however, ECP shows only about 70% of P-releasing activity at pH 5.5 relative to that occurring at a pH of 2.5 to 3.5 (Rodriguez et al., 1999a). Thus, adding all phytase premixes based on their activity at pH 5.5 (the standard and accepted assay procedure) may have resulted in some level of overfortification for the ECP-supplemented diets. This nonetheless cannot explain the marked P-releasing superiority of ECP over either FP1 or FP2. Thus, 500 FTU/kg of ECP in Trial 1 produced bone ash values that were markedly superior to those resulting from 1,000 FTU/kg of FP1. Also, in Trial 2, 1,000 FTU/kg of ECP resulted in higher bone ash values than those resulting from 5,000 FTU/kg of either FP1 or FP2. We believe the greater resistance of ECP to gastric pepsin and the lower pH optima ranging from 2.5 to 3.5 are more likely explanations for the greater efficacy of this enzyme relative to the fungal enzymes.
There has been great controversy in recent years about the protein-sparing effect of phytase in nonruminant nutrition. Phytate is able to bind proteins and amino acids at low to neutral pH values (Cosgrove, 1980; Anderson, 1985), theoretically rendering them less available for absorption from the gut of chickens and pigs. Digestibility studies have seemingly supported this, generally showing increased protein and amino acid digestibility, albeit small, in both chickens (Ravindran et al., 1999; Zhang et al., 1999) and pigs (Kemme et al., 1999). Other studies, however, have shown no beneficial effects on protein digestibility in chicks (Biehl and Baker, 1997a), pigs (Traylor et al., 2001), or molted laying hens (Snow et al., 2003). Growth studies, by contrast, have generally failed to show a positive response to supplemental phytase in chicks fed diets containing adequate P (Zhang et al., 1999; Boling-Frankenbach et al., 2001; Peter and Baker, 2001).
Any phytase-mediated growth response in animals fed protein or amino acid-deficient diets must be due to an increased amount or availability of the first-limiting amino acid. Supplementation of Met to low-CP SBM diets containing a similar deficient level of Met (% of requirement) produced dramatic improvements in weight gain (38%) of chicks (Emmert et al., 2000), whereas the addition of Lys to a low-CP CGM diet with a similar Lys deficiency also produced dramatic growth responses of chicks (Peter et al., 2000). Over the course of the past few years, our laboratory has tested the effect of phytase on many different phytate-containing ingredients that are first-limiting in different amino acids. Supplemental phytase failed to improve the PER values of any of these ingredients, regardless of whether Lys, sulfur AA, or Arg was first-limiting (Boling-Frankenbach et al., 2001; Peter and Baker, 2001). Results of the assay herein further argue that supplemental phytase, even at a very high dose level, does not improve the protein utilization of chicks fed diets based on ingredients first-limiting in different amino acids.
Implications
At dietary additions of 10 to 20 times normal usage levels (5,000 to 10,000 phytase units per kilogram of diet), a new E. coli-derived phytase can release up to 100% of the phytate-bound phosphorus in a corn-soybean meal broiler diet. At normal usage levels, the E. coli phytase releases more phosphorus than either of the two commercially available fungal-derived phytase products evaluated, which also differed from each other. With diets based on methionine-deficient soybean meal or lysine-deficient corn gluten meal, even a high dietary level of the E. coli phytase (10,000 phytase units per kilogram of diet) does not improve protein utilization.
Footnotes
1 Funding for this research was provided, in part, by the State of Illinois through the Illinois Council on Food and Agricultural Research (C-FAR). 
2 Correspondence: 290 Animal Science Laboratory, 1207 W. Gregory Dr. (phone: 217-333-0243; fax: 217-333-7861; e-mail: dhbaker{at}uiuc.edu).
Received for publication June 30, 2003. Accepted for publication December 2, 2003.
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