Abstract
Stable isotope analysis of amino acids has been employed as a powerful tool for estimating the trophic position of organisms and for identifying the resource utilization of them in food webs. This tool is based on empirical knowledge of the trophic discrimination of nitrogen and carbon isotopes (i.e., 15 N/ 14 N and 13 C/ 12 C) associated with the degradation and biosynthesis of amino acids in consumer species and based on the assumption that amino acids are major fuels for the life energy of organisms. However, because many organisms have used not only amino acids but also carbohydrates (e.g., sugar) and lipids (e.g., triacylglycerols) as their energy sources, the magnitude of trophic discrimination of amino acids potentially varies when organisms utilize the other energy sources together with amino acids. In the present study, we conducted controlled feeding experiments with the ant Formica japonica under three conditions: colony I, ants feed on frozen crickets; colony II, ants feed on frozen crickets and sugar; and colony III, ants feed on fried crickets and sugar. The nitrogen and carbon isotope ratios of larvae and pupae collected from these colonies reveal that (1) the effect of sugar utilization is negligible for a source-essential amino acid (i.e., phenylalanine), trophic-essential amino acids (i.e., valine, isoleucine, and leucine), and a trophic-nonessential amino acid (i.e., glutamic acid) but large for the other trophic-nonessential amino acids (i.e., alanine, glycine, and proline), and that (2) the effect of lipid utilization is negligible for a source-essential amino acid (i.e., phenylalanine) and a trophic-essential amino acid (isoleucine) but considerably large for the other trophic-essential and trophic-nonessential amino acids (i.e., valine, leucine, alanine, glycine, and proline). Based on these results, we conclude that the trophic isotopic discrimination of amino acids varies with the utilization of carbohydrates and lipids. Moreover, we predict that this variation in the isotope ratios found in the present study will be useful for better understanding how the trophic isotopic discrimination of amino acids is changed in organisms and for evaluating the carbohydrate and lipid utilization of organisms in wild food webs.
References
- Arrese L.E. and Soulages L.J. (2010) Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 55, 207–225.
- Ashhurst E.D. and Bailey J.A. (1980) Locust Collagen: Morphological and Biochemical Characterization. Eur. J. Biochem. 103, 73-83.
- Chikaraishi Y., Kashiyama Y., Ogawa N.O., Kitazato H. and Ohkouchi N. (2007) Metabolic control of nitrogen isotope composition of amino acids in macroalgae and gastropods: implications for aquatic food web studies. Mar. Ecol. Prog. Ser. 342, 85-90.
- Chikaraishi Y., Ogawa N.O., Kashiyama Y., Takano Y., Suga H., Tomitani A. Miyashita H., Kitazato H. and Ohkouchi O. (2009) Determination of aquatic food web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol. Oceanogr. Meth. 7, 740-750.
- Chikaraishi Y., Steffan A.S., Takano Y. and Ohkouchi O. (2015) Diet quality influences isotopic discrimination among amino acids in an aquatic vertebrate. Ecol. Evol. 5, 2048-2059.
- Gäde G. and Auerswald L. (2002) Beetles’ choice—proline for energy output: control by AKHs. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 132, 117-129.
- Hall B.M. and Eastridge L.M. (2014) INVITED REVIEW: Carbohydrate and fat: Considerations for energy and more. Prof. Anim. Sci. 30, 140-149.
- Kanaya M., Takizawa Y. and Chikaraishi Y (2022) Fractionation of Carbon isotopes during acetylation of alcohols. Res. Org. Cgeochem 38, 1-6.
- Larsen T., Taylor D.L., Leigh B.M. and O'Brien M.D. (2009) Stable isotope fingerprinting: a novel method for identifying plant, fungal, or bacterial origins of amino acids. Ecology 90, 3526-3535.
- Larsen T., Ventura M., Anderson N., O'Brien M.D, Piatkowski U. and McCarthy D.M. (2013) Tracing Carbon Sources through Aquatic and TerrestrialFood Webs Using Amino Acid Stable Isotope Fingerprinting PLOS ONE. 8: e73441.
- McCarthy D.M., Benner R., Lee C. and Fogel M.L. (2007) Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. Geochim. Cosmochim. Acta. 71, 4727-4744.
- McMahon K.W. and McCarthy D.M. (2016) Embracing variability in amino acid δ15N fractionation: mechanisms, implications, and applications for trophic ecology. Ecosphere. 7, 1-26.
- McMahon K.W. Thorrold S.R., Elsdon T.S. and McCarthy M.D. (2015) Trophic discrimination of nitrogen stable isotopes in amino acids varies with diet quality in a marine fish. Limnol. Oceanogr. 60, 1076-1087.
- Popp B.N., Graham B.S., Olson R. J., Hannides C.C.S., Lott M.J., López-Ibarra G.A., Galván-Magaña F. and Fry B. (2007 Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. In: Dawson, T., Siegwolf, R. (Eds.), Stable isotopes as indicators of ecological change, Terrestrial ecology series. Elsevier Academic Press., 173-190.
- Sutherland D.T., Peng Y.Y., Trueman E.H., Weisman S., Okada S., Walker A.A., Sriskantha A., White F.J.,
- Huson G.M., Werkmeister A.J., Glattauer V., Stoichevska V., Mudie T.S., Haritos S.V. and Ramshaw A.M.J. (2013) A new class of animal collagen masquerading as an insect silk. Nature Sci. Rep. 3, 2864.
- Takizawa Y., Takano Y., Choi B., Dharampal S.P., Steffan A.S., Ogawa O.N., Ohkouchi N. and Chikaraishi Y. (2020) A new insight into isotopic fractionation associated with decarboxylation in organisms: implications for amino acid isotope approaches in biogeoscience. Prog. Earth Planet. Sci. 7, 1-13.
- Takizawa Y. and Chikaraishi Y. (2021) Stable isotope analysis-1: gas chromatograph-isotope ratio mass spectrometer. Low. Tem. Sci. 79, 1-11.
- Teulier L., Weber M.J., Crevier J. and Darveau A.C. (2016). Proline as a fuel for insect flight: enhancing carbohydrate oxidation in hymenopterans. Proc. R. Soc. B. 28320160333.
- Wali A.J., Ni D., Facey J.W.H., Dodgson T., Pulpitel J. T., Senior M.A., Raubenheimer D., Macia L. and
- Simpson . J.S. (2022) Determining the metabolic effects of dietary fat, sugars and fat-sugar interaction using nutritional geometry in a dietary challenge study with male mice. Nat. commun. 14, 1-12.