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© 2005 The American Society for Nutritional Sciences J. Nutr. 135:1712-1717, July 2005

Nutrient Metabolism

Dietary S-Methylmethionine, a Component of Foods, Has Choline-Sparing Activity in Chickens1

Nathan R. Augspurger2, Colleen S. Scherer, Timothy A. Garrow and David H. Baker3

Departments of Animal Sciences and Food Science and Human Nutrition, and Division of Nutritional Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801

3To whom correspondence should be addressed. E-mail: dhbaker{at}uiuc.edu.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Acid hydrolysis of dehulled soybean meal (SBM) and corn gluten meal (CGM) followed by chromatographic amino acid analysis (ninhydrin detection) revealed substantial quantities of S-methylmethionine (SMM) in both ingredients (1.65 g SMM/kg SBM; 0.5 g SMM/kg CGM). Young chicks were used to quantify the methionine- (Met) and choline-sparing bioactivity of crystalline L-SMM, relative to L-Met and choline chloride standards in 3 assays. A soy isolate basal diet was developed that could be made markedly deficient in Met, choline, or both. When singly deficient in choline or in both choline and Met, dietary SMM addition produced a significant (P < 0.01) growth response. In Assay 2, dietary SMM did not affect (P > 0.10) growth of chicks fed a Met-deficient, choline-adequate diet. A standard-curve growth assay revealed choline bioactivity values (wt:wt) of 14.2 ± 0.8 and 25.9 ± 5.1 g/100 g SMM based on weight gain and gain:food responses, respectively. A fourth assay, using standard-curve procedures, showed choline bioactivity values of 20.1 ± 1.1 and 22.9 ± 1.7 g/100 g SMM based on weight gain and gain:food responses, respectively. It is apparent that SMM in foods and feeds has methylation bioactivity, and this has implications for proper assessment of dietary Met and choline requirements as well as their bioavailability in foods and feeds.

KEY WORDS: • choline • methionine • S-methylmethionine • betaine • chick

S-Methylmethionine (SMM)4 is an analog of S-adenosylmethionine (SAM; Fig. 1), with a methyl group substituted for the adenosyl group. This compound is unique to plants and is found in measurable-to-high concentrations in corn, cabbage, tomatoes, celery, spinach, and garlic (1–3). SMM is an active component of the methionine (Met) cycle in plants, formed from Met accepting a methyl group from SAM, and utilized through the donation of a methyl group to homocysteine (Hcy) to produce Met. The operation of this short-term cycle serves to attenuate the depletion of the free Met pool by an overshoot in SAM synthesis (4–6).



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  		FIGURE 1 Structure of SMM and SAM.

 
Previous research elucidated the mechanism for synthetic synthesis and the in vitro and in vivo metabolism of SMM (7–12). SMM promoted the growth of Escherichia coli heterotrophs only in the presence of Cys or Hcy (9). Radiolabeling experiments suggested that the methyl group of SMM is available for choline or creatine synthesis, but not for Met synthesis (13). In vivo experiments with rats were equivocal, with SMM supporting growth of rats fed sulfur amino acid (SAA)-deficient diets (14,15), but not in rats fed SAA-free diets (13). Additionally, there is anecdotal evidence for SMM exhibiting choline bioactivity as a result of ameliorating choline deficiency–induced fatty liver in rats (16).

The objective of this research was to qualitatively and quantitatively determine the efficacy of L-SMM for sparing dietary choline or Met. Avians, unlike mammals, have a requirement for preformed choline that cannot be replaced by excess Met (17,18), making them an excellent animal model for studying choline bioavailability. Limited supplies of L-SMM had to be considered in setting the length of the bioassays as well as the number of chicks used for each dietary treatment employed herein.


   MATERIALS AND METHODS
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 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    General procedures. All procedures were approved by the University of Illinois Laboratory Animal Care and Use Committee. Four assays were done using New Hampshire x Columbian Plymouth Rock male chicks obtained from the University of Illinois Poultry Farm. Chicks were fed a nutritionally adequate 23% crude protein (CP) corn-soybean meal starter diet from hatching to d 7 posthatch. On d 8, after an overnight period of feed withdrawal, chicks were weighed, wing-banded, and randomly allotted to form 3 or 7 replicates of 3 chicks per pen within each assay. Chicks were housed in thermostatically controlled starter batteries (Petersime Incubator) with raised wire floors in an environmentally controlled building with 24-h continuous light. Experimental diets (Table 1) were fed from d 8 to 17 posthatch. At the end of each bioassay, individual chicks and feeders were weighed for calculation of weight gain and gain:food ratio.


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  		TABLE 1 Composition of the experimental diets

 
The SMM (Degussa AG Feed Additives Division) compound, an analog of SAM, contained 2 methyl groups bound to the sulfur (S) atom of Hcy (Fig. 1). The pure L-SMM compound was synthesized as either the iodide (I, Assay 1) or bromide (Br, Assays 2–4) salt. Thus, I (KI) or Br (NaBr) was added to appropriate experimental diets at a concentration equal to that provided by L-SMM. Earlier work with chicks (19) revealed that 2700 mg/kg of the I salt of L-SMM (isosulfurous to 1400 mg/kg L-Met) provided 1200 mg I/kg. This level was found to be toxic, but subsequent work revealed that 100 mg/kg Br reversed the toxicity of I and restored weight gain in chicks consuming diets containing high levels of I (19,20). Additionally, Br per se at concentrations up to 100 mg/kg was not found to be toxic for chicks (19,20).

A soy-protein isolate (SPI) basal diet formulated to be deficient in both Met and choline was used for Expts. 1, 3, and 4 (Table 1). This diet was used previously in our laboratory to study the utilization of several nutrients (21–24). The SPI was a functional alcohol-extracted product analyzed to contain 824 g/kg CP, 21.8 g/kg SAA (i.e., Met plus Cys), 31.7 g/kg threonine, and 51.7 g/kg lysine (24). The basal diet contained 200.2 g/kg CP and 5.3 g/kg SAA, and was essentially devoid of bioavailable choline (23). Supplementation of Met or choline to this diet produced dramatic increases in the weight gain of chicks (22,23). The basal diet used for Assay 2 (Table 1) was a corn-peanut meal diet formulated to be deficient in Met but superadequate in choline (22).

    SMM analysis of foodstuffs. The SMM content of SPI, dehulled soybean meal (SBM), corn gluten meal (CGM), and ground corn was quantified in duplicate by chromatographic analysis (Beckman model 6300, Beckman Instruments) following 24-h hydrolysis in HCl at 105°C.

    Assay 1. The objective of this bioassay was to determine the efficacy of SMM for promoting weight gain in chicks fed diets that were deficient in Met, choline, or both. Dietary additions of L-Met, choline chloride, or L-SMM were made at the expense of cornstarch. The basal diet was supplemented with 0.8 g/kg of either L-Met or choline or the combination of the two, in the absence and presence of 1.3 g/kg L-SMM, a concentration isosulfurous to 1.2 g/kg L-Met.

    Assay 2. The objective of this bioassay was to determine the Met-sparing activity of SMM when added to a Met-deficient diet containing excess choline. The corn-peanut meal basal diet was supplemented with 0.5 g/kg L-Met or 1.1 g/kg L-SMM. The 1.1 g/kg concentration of L-SMM was isosulfurous to 1 g/kg L-Met.

    Assay 3. This bioassay was done to determine the choline-sparing activity of L-SMM for chicks fed diets containing deficient amounts of choline but adequate amounts of Met. The SPI diet was supplemented with 1 g/kg DL-Met to serve as a basal diet. This concentration of supplemental Met maximizes the growth rate of chicks fed the SPI diet (Table 1) made adequate to superadequate in choline (25). Three levels of choline from choline chloride (150, 300, and 450 mg/kg) were supplemented to the basal diet, as well as one level of L-SMM (948 mg/kg) that was isomethyl to 400 mg/kg choline.

    Assay 4. This bioassay was carried out to confirm the efficacy of L-SMM for promoting growth of chicks fed diets deficient in choline or both choline and Met. The SPI basal diet (deficient in both choline and Met) was supplemented with 1 g/kg L-Met or 1 g/kg choline, or both. To the Met-adequate but choline-deficient diet, choline was added at 150 and 300 mg/kg to construct a standard curve. L-SMM (1.4 g/kg) was added to the diet deficient in both choline and Met, and also to the diet singly deficient in choline.

    Statistical analysis. All 4 assays were analyzed using pen means data according to completely randomized designs (26). Where appropriate, orthogonal single df comparisons were used to evaluate treatment differences; in other cases, the least-significant differences test was used to compare treatments (27). In Assays 3 and 4, standard-curve methodology was used to determine a choline bioactivity value for SMM. Weight gain (g, Y) or gain:food ratio (g/kg, Y) was regressed against choline intake (mg, X), using pen means data, to establish a standard curve (Y = aX + b). Performance responses to L-SMM supplementation were substituted into the resulting equation for Y and solved for X, i.e., an equivalent intake of choline. This result was divided by the intake (mg) of L-SMM and multiplied by 100 to produce a choline bioactivity value.


   RESULTS
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 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
    SMM content of foodstuffs. Analyzed concentrations of SMM in foodstuffs are presented in Table 2. Dehulled SBM contained the highest concentration of those ingredients analyzed, 1.65 g/kg, whereas SPI was devoid of SMM. CGM and corn contained 0.50 and 0.10 g SMM/kg, respectively. Analyzed values represent acid hydrolysates, even though, presumably, the SMM contained in foodstuffs exists in a free unbound state (1).


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  		TABLE 2 SMM in feed ingredients1

 
    Assay 1. Weight gain was increased (P < 0.01) by supplementation of L-Met, choline, or L-SMM (Table 3), with choline and SMM producing greater improvements than Met. There was a choline x SMM interaction (P < 0.05) for gain:food ratio, such that SMM improved gain:food to a greater extent in choline-deficient chicks than in choline-adequate chicks. Supplemental Met also improved (P < 0.01) gain:food ratio.


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  		TABLE 3 Growth responses of chicks to SMM when added to diets deficient in choline, methionine, or both (Assay 1)1

 
    Assay 2. Supplementation of L-Met increased (P < 0.05) weight gain, food intake, and gain:food ratio of chicks fed Met-deficient, choline-adequate diets (Table 4). Growth performance was not affected (P > 0.05) by dietary supplementation of L-SMM.


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  		TABLE 4 SMM has no methionine-sparing activity when added to a methionine-deficient diet containing excess choline (Assay 2)1

 
    Assay 3. Dietary addition of graded levels of choline to a choline-deficient, Met-adequate diet resulted in linear (P < 0.01) increases in weight gain, food intake, and gain:food ratio (Table 5). L-SMM supplementation increased (P < 0.05) weight gain and gain:food ratio of chicks above that occurring in chicks fed the basal diet. Standard-curve methodology predicted choline bioactivity values for L-SMM of 14.2 ± 0.8 and 25.9 ± 5.1 g/100 g based on weight gain and gain:food ratio responses, respectively.


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  		TABLE 5 Choline-sparing activity of SMM for chicks fed diets deficient in choline (Assay 3)1

 
    Assay 4. The addition of both L-Met (1 g/kg) and choline (1 g/kg) increased (P < 0.05) growth performance of chicks fed the Met- and choline-deficient basal diet (Table 6). Weight gain, food intake, and gain:food ratio increased linearly (P < 0.05) when graded levels of choline were added to the Met-adequate diet (Diets 2, 5, and 6). Dietary supplementation of L-SMM to both the basal diet and the Met-adequate diet increased (P < 0.05) growth performance over that observed for the respective controls. Standard-curve methodology predicted choline-sparing bioactivity values for L-SMM (i.e., Diet 8) of 20.1 ± 1.1 and 22.9 ± 1.7 g/100 g based on weight gain and gain:food responses, respectively.


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  		TABLE 6 Efficacy of SMM for chicks fed diets deficient in choline alone or in both choline and methionine (Assay 4)1

 

   DISCUSSION
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The objective of these experiments was to determine the bioavailability of SMM as either a Met or choline source, using a Met- and choline-deficient semipurified diet previously shown to respond markedly to dietary additions of either nutrient (23). The marked responses in growth performance when SMM was added to choline-deficient, Met-adequate diets in Assays 1, 3, and 4 showed that SMM exhibited choline-sparing bioactivity; indeed, SMM exhibited ~20% bioequivalence (wt:wt) to choline per se. Conversely, scrutiny of the data in Assays 1 and 2 suggested that SMM probably did not exhibit Met activity in chicks.

The choline-sparing bioactivity of SMM may manifest through the methyl-transfer reactions that produce phosphatidylcholine (PC) from phosphatidylethanolamine (PE) by PE methyltransferase (PEMT; Fig. 2). The biosynthesis of PC requires 3 sequential methylations of PE by PEMT; the first of these is performed very inefficiently in avians (28–30). The methyl group of SMM is readily available for choline biosynthesis (13); thus, it is plausible that SMM serves as a methyl donor for PEMT. In vivo evidence of the choline bioactivity of SMM was seen in mammals (16) in that SMM supplementation in rats prevented fatty livers induced by choline deficiency.



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  		FIGURE 2 Involvement of SMM in choline biosynthesis.

 
Assay 2 (Table 4) showed unequivocally that SMM does not exhibit Met-sparing bioactivity when a surfeit amount of choline is contained in the diet. The data of Assay 1, however, are not so clear-cut. The growth response to SMM in chicks fed a choline-supplemented, Met-deficient diet (diet 7 vs. diet 3), on the surface, appeared to be a Met response, but we hypothesize that it is actually a choline response. In previous work with the same SPI diet, Emmert et al. (21) reported that weight gain responses of chicks to graded levels of choline per se followed a 2-slope pattern, with weight gains increasing more rapidly at choline levels < 350 mg/kg than at levels between 350 and 825 mg choline/kg. Our choline concentration of 800 mg/kg used in Assay 1 lies within the second slope, possibly below the dietary concentration necessary to maximize performance, and thus leaving room in that response range for a small response to choline rather than Met.

The lack of Met activity from SMM is perplexing, especially in light of the in vitro evidence to the contrary (7,8). Indeed, Shapiro (7,8) reported that Met was produced via SMM methylation of Hcy, and also via the demethylation of SMM, thereby producing 2 mol of Met from 1 mol of SMM (7). SMM promoted 3 times greater growth of E. coli cells than Met, indicating roles in both Met- and non-Met-methyl transfer reactions (9,10). In rats, SMM supplementation produced growth rates that were similar (14) or even greater (15) than those produced by Met supplementation. Rats in both experiments were fed diets containing deficient levels of Met and adequate levels of Cys. An experiment done by Stekol (13), however, contradicted these results because supplementation of SMM as the sole source of dietary SAA resulted in weight gains of rats that were very poor compared with those obtained with Met. The addition of Cys to the SAA-containing diets produced growth rates of rats that were similar to or better than those of rats fed diets containing Met (13). Taken together, these data suggest that SMM has the ability to serve not only as a methyl donor for choline and creatine biosynthesis, but also, under some conditions, as a putative precursor for Met biosynthesis. How coprophagy may have influenced the results with rats is problematic.

The lack of response to SMM (Table 4) when used as a Met precursor may be a function of dietary choline adequacy. In chicks, after meeting the requirement for acetylcholine and PC (31), choline is rapidly oxidized by choline dehydrogenase to betaine (17,32), which then can donate a methyl group to Hcy to produce Met and dimethylglycine through the action of betaine-Hcy methyltransferase (BHMT; Fig. 2). Deficient concentrations of Met and surfeit concentrations of choline (such as those used in Assay 2) or betaine, significantly increased BHMT activity in chicks compared with those fed adequate levels of Met (33,34). Hence, when dietary choline (and betaine) concentrations are adequate or surfeit, betaine may be preferentially used to remethylate Hcy, effectively preventing biosynthesis of Met from SMM. This seems logical if chick hepatic BHMT, like pig hepatic BHMT (35), can use SMM as an alternate methyl donor under conditions of low dietary choline and betaine ingestion.

The presence of SMM in foods and feeds adds one more complicating factor to the proper assessment of the requirement and bioavailability of choline. In mammalian species, but not avians, excess dietary Met can eliminate the dietary need for preformed choline (17,18,36,37), and betaine, which is also present in many foods and feeds (38), can replace the methylation function of choline (31). Thus, previous attempts to obtain clear-cut animal responses to choline supplementation of corn-soybean meal diets have often met with failure (18,39), probably due not only to significant concentrations of choline per se in soybean meal but also to the presence of both betaine and SMM in this ingredient. Moreover, previous research in which the bioavailability of choline per se in soybean meal was found to be as high as 80 (22) to ~100% (40) probably represents overestimates. It is apparent that when considering a dietary need for bioavailable choline, choline itself as well as betaine and SMM levels in foods and feeds must be taken into account. For mammalian species, including humans, excess dietary Met is also capable of sparing choline.


   FOOTNOTES
 
1 Presented in part at Experimental Biology 04, April 2004, Washington, DC [Augspurger, N. R., Scherer, C., Garrow, T. A. & Baker, D. H. (2004) S-Methylmethionine, a component of foods, has methionine and choline-sparing bioactivity. FASEB J. 18: A545 (abs.)]. Back

2 Present address: United Feeds, Incorporated, Sheridan, IN 46069. Back

4 Abbreviations used: BHMT, betaine-Hcy methyltransferase; CGM, corn gluten meal; CP, crude protein; PC, phosphatidylcholine; PE, phosphatidylethanolamine; PEMT, PE methyltransferase; SAA, sulfur amino acid; SAM, S-adenosylmethionine; SMM, S-methylmethionine; SPI, soy protein isolate. Back

Manuscript received 18 February 2005. Initial review completed 7 April 2005. Revision accepted 14 April 2005.


   LITERATURE CITED
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

1. Grunau J. A., Swiader J. M. Chromatographic quantitation of free amino acids: S-methylmethionine, methionine and lysine in corn. J. Plant Nutr. 1991;14:653-662.

2. Kim G. H., Hong E.-Y., Kang E.-J., Jeong Y., Kim E.-S. Vitamin U in medicinal food plants. FASEB J. 2003;18:A46 (abs.).

3. Kovatscheva E. G., Popova J. G. S-Methylmethionine content in plant and animal tissues and stability during storage. Die Nahrung. 1977;21:468-472.

4. Hanson A. D., Roje S. One-carbon metabolism in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001;52:119-137.[Medline]

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6. Ranocha P., McNeil S. D., Ziemak M. J., Li C., Tarczynski M. C., Hanson A. D. The S-methylmethionine cycle in angiosperms: ubiquity, antiquity and activity. Plant J. 2001;25:575-584.[Medline]

7. Shapiro S. The biosynthesis of methionine from homocysteine and methylmethionine sulfonium salt. Biochim. Biophys. Acta. 1955;18:134-135.[Medline]

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9. McRorie R. A., Glazener M. R., Skinner C. D., Shive W. Microbiological activity of the methylsulfonium derivative of methionine. J. Biol. Chem. 1954;211:489-497.[Free Full Text]

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34. Pillai P. B., Burkett C. B., Emmert J. L., Beers K. R. Assessment of sulfur amino acid metabolism using growth performance and a stable isotope technique. Poult. Sci. 2002;80(suppl. 1):77 (abs.).

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D. H. Baker
Inaugural Article: Comparative nutrition and metabolism: Explication of open questions with emphasis on protein and amino acids
PNAS, December 13, 2005; 102(50): 17897 - 17902.
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