Metabolomics

, 13:105

Profiling of faecal water and urine metabolites among Papua New Guinea highlanders believed to be adapted to low protein intake

  • Eriko Tomitsuka
  • Katsura Igai
  • Kiyoshi Tadokoro
  • Ayako Morita
  • Jun Baba
  • Wataru Suda
  • Andrew R. Greenhill
  • Paul F. Horwood
  • Kevin W. Soli
  • Peter M. Siba
  • Shingo Odani
  • Kazumi Natsuhara
  • Hidetoshi Morita
  • Masahiro Umezaki
Original Article

Abstract

Introduction

Adequate amount of proteins from foods are normally needed to maintain muscle mass of the human body. Although protein intakes of Papua New Guinea (PNG) highlanders are less than biologically adequate, protein deficiency related disorders have rarely been reported. It has been postulated that gut microbiota play a role in such low-protein-adaptation.

Objective

To explore underlying biological mechanisms of low-protein adaptation among PNG highlanders by investigating metabolomic profiles of faecal water and urine.

Methods

We performed metabolome analysis using faecal water extracted from faecal samples of PNG highlanders, PNG non-highlanders and Japanese subjects. We paid special attention to amino acids and other metabolites produced by gut microbiota, as well as to metabolites involved in nitrogen recycling in the human gut.

Results

Our results indicated that amino acid levels were higher in faecal water from PNG highlanders than PNG non-highlanders, but amino acid levels did not differ between PNG highlanders and Japanese subjects. Among PNG highlander samples, amino acid levels tended to be higher in those who consumed less protein.

Conclusion

We speculated that a greater proportion of urea was excreted to the intestine among the PNG highlanders than other groups, and that the urea was used for nitrogen salvage. Intestinal bacteria are essential for producing ammonia from urea and also for producing amino acids from ammonia, which is a key process in low-protein adaptation. Profiling the gut microbiota of PNG highlanders is an important avenue for further research into the mechanisms of low-protein adaptation.

Keywords

Gut microbiota Metabolomics CE-TOFMS 

Supplementary material

11306_2017_1243_MOESM1_ESM.pptx (59 kb)
Scatter plot between the first and the second principal components obtained from principle component analysis for 228 metabolites identified in urinary samples. Closed circles indicate PNG highlanders samples (n=6), open circles indicate PNG non-highlanders samples (n=4). Percentages of variation explained by the first component and the second component are shown. Supplementary Material 1 (PPTX 58 KB)
11306_2017_1243_MOESM2_ESM.xlsx (91 kb)
Supplementary Material 2 (XLSX 91 KB)

References

  1. Bergen, W. G., Wu, G. (2009). Intestinal nitrogen recycling and utilization in health and disease. Journal of Nutrition, 139(5), 821–825.CrossRefPubMedGoogle Scholar
  2. Bistrian, B. R. (1990). Recent advances in parenteral and enteral nutrition: A personal perspective. The Journal of Parenteral and Enteral Nutrition, 14(4), 329–334.CrossRefPubMedGoogle Scholar
  3. Bourke, R. M. (1985). Sweet potato (Ipomoea batatas) production and research in Papua New Guinea. Papua New Guinea Journal of Agriculture, Forestry and Fisheries, 33(3–4), 89–108.Google Scholar
  4. Date, C., Baba, M., Kajiwara, N. M., Minamide, T., Fujita, Y., Ichikawa, M., Miyatani, S., Hayashi, M., Tanaka, H., Heywood, P., Alpers, M., & Koishi, H. (1988). Nutritional status of some Papua New Guinea highlanders as assessed by physical measurements and blood analysis. Ecology of Food and Nutrition, 20, 185–196.CrossRefGoogle Scholar
  5. De Angelis, M., Montemurno, E., Piccolo, M., Vannini, L., Lauriero, G., Maranzano, V., Gozzi, G., Serrazanetti, D., Dalfino, G., Gobbetti, M., Gesualdo, L. (2014). Microbiota and metabolome associated with immunoglobulin A nephropathy (IgAN). PLoS ONE, 9(6), e99006.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Debnam ES, Grimble GK. (2001) Methods for assessing intestinal absorptive function in relation to enteral nutrition. Current Opinion in Clinical Nutrition & Metabolic Care, 4(5):355–367.CrossRefGoogle Scholar
  7. Di Cagno, R., De Angelis, M., De Pasquale, I., Ndagijimana, M., Vernocchi, P., Ricciuti, P., Gagliardi, F., Laghi, L., Crecchio, C., Guerzoni, M. E., Gobbetti, M., Francavilla, R (2011). Duodenal and faecal microbiota of celiac children: Molecular, phenotype and metabolome characterization. BMC Microbiology, 11, 219.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Eben, H., Clements, F. W. (1947). Report of the New Guinea Nutrition Survey Expedition.Google Scholar
  9. Ferro-Luzzi, A., Norgan, N. G., & Durnin, J. V. (1975). Food intake, its relationship to body weight and age, and its apparent nutritional adequacy in New Guinean children. The American Journal of Clinical Nutrition, 28(12), 1443–1453.PubMedGoogle Scholar
  10. Greenhill, A. R., Tsuji, H., Ogata, K., Natsuhara, K., Morita, A., Soli, K., Larkins, J. A., Tadokoro, K., Odani, S., Baba, J., Naito, Y., Tomitsuka, E., Nomoto, K., Siba, P. M., Horwood, P. F., Umezaki, M. (2015). Characterization of the Gut Microbiota of Papua New Guineans Using Reverse Transcription Quantitative PCR. PLoS ONE, 10(2), e0117427.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Hipsley, E. H., & Clements, F. W. (1950). Reports of the New Guinea nutrition expedition 1947. Canberra: Department of External Territories.Google Scholar
  12. Itoh, S., Sugawa-Katayama, Y., Koishi, H., & Izumi, S. (1982). Serum concentration of protein, triglyceride, β-lipoproteins and cholesterol in Papua New Guinean highlanders. The Journal of Nutritional Science and Vitaminology, 28, 411–417.CrossRefPubMedGoogle Scholar
  13. Jansson, J., Willing, B., Lucio, M., Fekete, A., Dicksved, J., Halfvarson, J., Tysk, C., & Schmitt-Kopplin, P. (2009). Metabolomics reveals metabolic biomarkers of Crohn’s disease. PLoS ONE, 4(7), e6386.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Kajiwara, N. M., Okuda, T., Miyatani, S., Date, C., Minamide, T., Fujita, Y., Ichikawa, M., Baba, M., Heywood, P., & Koishi, H. (1984). Nutritional status of Papua New Guinea highlanders: Seasonal comparison of festival and non-festival times. Journal of Food and Nutrition Research, 41, 55–61.Google Scholar
  15. Kim, S. W., Suda, W., Kim, S., Oshima, K., Fukuda, S., Ohno, H., Morita, H., & Hattori, M. (2013). Robustness of gut microbiota of healthy adults in response to probiotic intervention revealed by high-throughput pyrosequencing. DNA Research, 20(3), 241–253.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Klinder, A., Karlsson, P. C., Clune, Y., Hughes, R., Glei, M., Rafter, J. J., Rowland, I., Collins, J. K., & Pool-Zobel, B. L. (2007). Fecal water as a non-invasive biomarker in nutritional intervention: Comparison of preparation methods and refinement of different endpoints. Nutrition and Cancer, 57(2), 158–167.CrossRefPubMedGoogle Scholar
  17. Koishi, H. (1990). Nutritional adaptation of Papua New Guinea Highlanders. European Journal of Clinical Nutrition, 44(12), 851–911.PubMedGoogle Scholar
  18. Luyken, R., Pikaar, N. A., & Luekenko, F. W. (1964). Nutrition studies in New Guinea. The American Journal of Clinical Nutrition, 14, 13–27.PubMedGoogle Scholar
  19. Millward, D. J. (1979). Protein deficiency, starvation and protein metabolism. Proceedings of the Nutrition Society, 38(1), 77–88.CrossRefPubMedGoogle Scholar
  20. Ministry of Health, Labour and Welfare in Japan. (2015). Annual report of National Health and Nutrition Survey.Google Scholar
  21. Mora, D., & Arioli, S. (2014). Microbial urease in health and disease. PLoS Pathogens, 10(12), e1004472.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Morita, A., Natsuhara, K., Tomitsuka, E., Odani, S., Baba, J., Tadokoro, K., Igai, K., Greenhill, A. R., Horwood, P. F., Soli, K. W., Phuanukoonnon, S., Siba, P. M., & Umezaki, M. (2015). Development, validation, and use of a semi-quantitative food frequency questionnaire for assessing protein intake in Papua New Guinean Highlanders. American Journal of Human Biology, 27(3), 349–357.CrossRefPubMedGoogle Scholar
  23. Naito, Y. I., Morita, A., Natsuhara, K., Tadokoro, K., Baba, J., Odani, S., Tomitsuka, E., Igai, K., Tsutaya, T., Yoneda, M., Greenhill, A. R., Horwood, P. F., Soli, K. W., Suparat, P., Siba, P. M., & Umezaki, M. (2015). Association of protein intakes and variation of diet-scalp hair nitrogen isotopic discrimination factor in Papua New Guinea Highlanders. American Journal of Physical Anthropology, 158(3), 359–370.CrossRefPubMedGoogle Scholar
  24. Nishijima, S., Suda, W., Oshima, K., Kim, S. W., Hirose, Y., Morita, H., & Hattori, M. (2016). The gut microbiome of healthy Japanese and its microbial and functional uniqueness. DNA Research, 23(2), 125–133.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Norgan, N. G., Ferroluz, A., & Durnin, J. V. G. (1974). Energy and nutrient intake and energy expenditure of 204 New Guineas adults. Philosophical transactions of the Royal Society of London B, Biological Science, 268(893), 309–348.CrossRefGoogle Scholar
  26. Okuda, T., Kajiwara, N., Date, C., Sugimoto, K., Rikimaru, T., Fujita, Y., & Koishi, H. (1981). Nutritional status of Papua New Guinea highlanders. Journal of Nutritional Science and Vitaminology, 27, 319–331.CrossRefPubMedGoogle Scholar
  27. Okuda, T., Yamaguchi, Y., Fujita, Y., Minamide, T., Kajiwara, N. M., Miyatani, S., Rikimaru, T., Oi, Y., Izuta, A., Nakano, Y., & Koishi, H. (1984). The change of the diet on Papua New Guinea highlanders. Annual report of science of living (vol. 32, pp. 39–50). Osaka: Osaka City University.Google Scholar
  28. Oomen, H. A. (1961). The nutrition situation in western New Guinea. Tropical and Geographical Medicine, 3, 321–335.Google Scholar
  29. Oomen, H. A. (1972). Distribution of nitrogen and composition of nitrogen compounds in food, urine and faeces in habitual consumers of sweet potato and taro. Nutrition and Metabolism, 14(2), 65–82.CrossRefPubMedGoogle Scholar
  30. Picou, D., & Phillips, M. (1972). Urea metabolism in malnourished and recovered children receiving a high or low protein diet. American Journal of Clinical Nutrition, 25(11), 1261–1266.PubMedGoogle Scholar
  31. Richards, P., Metcalfe-Gibson, A., Ward, E. E., Wrong, O., & Houghton, B. J. (1967). Utilisation of ammonia nitrogen for protein synthesis in man, and the effect of protein restriction and uraemia. Lancet, 2(7521), 845–849.CrossRefPubMedGoogle Scholar
  32. Soga, T., & Heiger, D. N. (2000). Amino acid analysis by capillary electrophoresis electrospray ionization mass spectrometry. Analytical Chemistry, 72(6), 1236–1241.CrossRefPubMedGoogle Scholar
  33. Soga, T., Ohashi, Y., Ueno, Y., Naraoka, H., Tomita, M., & Nishioka, T. (2003). Quantitative metabolome analysis using capillary electrophoresis mass spectrometry. Journal of Proteome Research, 2(5), 488–494.CrossRefPubMedGoogle Scholar
  34. Soga, T., Ueno, Y., Naraoka, H., Ohashi, Y., Tomita, M., & Nishioka, T. (2002). Simultaneous determination of anionic intermediates for Bacillus subtilis metabolic pathways by capillary electrophoresis electrospray ionization mass spectrometry. Analytical Chemistry, 74(10), 2233–2239.CrossRefPubMedGoogle Scholar
  35. Stewart, G. S., & Smith, C. P. (2005). Urea nitrogen salvage mechanisms and their relevance to ruminants, non-ruminants and man. Nutrition Research Reviews, 18(1), 49–62.CrossRefPubMedGoogle Scholar
  36. Takahashi, M., Benno, Y., & Mitsuoka, T. (1980). Utilization of ammonia nitrogen by intestinal bacteria isolated from pigs. Applied and Environmental Microbiology, 39(1), 30–35.PubMedPubMedCentralGoogle Scholar
  37. Tomé D, Bos C. (2000) Dietary protein and nitrogen utilization. Journal of Nutrition, 130(7):1868S–1873S.PubMedGoogle Scholar
  38. Walser, M., & Bodenlos, L. J. (1959). Urea metabolism in man. The Journal of Clinical Investigation, 38, 1617–1626.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wapnir, R. A., Hawkins, R. L., & Lifshitz, F. (1972). Hyperaminoacidemia effects on intestinal transport of related amino acids. American Journal of Physiology, 223(4), 788–793.PubMedGoogle Scholar
  40. WHO/FAO/UNU. (2007). Protein and amino acid requirements in human nutrition. World Health Organization Technical Report Series, 935, 1–265.Google Scholar
  41. Wolpert, E., Phillips, S. F., & Summerskill, W. H. (1971). Transport of urea and ammonia production in the human colon. Lancet, 2(7739), 1387–1390.CrossRefPubMedGoogle Scholar
  42. Younes, H., Alphonse, J. C., Behr, S. R., Demigné, C., & Rémésy, C. (1999). Role of fermentable carbohydrate supplements with a low-protein diet in the course of chronic renal failure: Experimental bases. American Journal of Kidney Diseases, 33(4), 633–646.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Eriko Tomitsuka
    • 1
    • 2
  • Katsura Igai
    • 1
    • 3
  • Kiyoshi Tadokoro
    • 1
    • 4
  • Ayako Morita
    • 1
    • 5
  • Jun Baba
    • 6
  • Wataru Suda
    • 7
  • Andrew R. Greenhill
    • 8
  • Paul F. Horwood
    • 8
  • Kevin W. Soli
    • 8
  • Peter M. Siba
    • 8
  • Shingo Odani
    • 9
  • Kazumi Natsuhara
    • 10
  • Hidetoshi Morita
    • 11
  • Masahiro Umezaki
    • 1
  1. 1.Department of Human Ecology, Graduate School of MedicineThe University of TokyoTokyoJapan
  2. 2.Department of Health Chemistry, Faculty of Pharmaceutical SciencesNiigata University of Pharmacy and Applied SciencesNiigata CityJapan
  3. 3.Graduate School of Biomedical SciencesNagasaki UniversitySakamotoJapan
  4. 4.Department of Resource Policy and Management, Faculty of International Resource SciencesAkita UniversityAkita CityJapan
  5. 5.Department of Global Health PromotionTokyo Medical and Dental UniversityTokyoJapan
  6. 6.Faculty of Human SciencesWako UniversityMachida CityJapan
  7. 7.IMS RIKEN Center for Integrative Medical SciencesYokoham CityJapan
  8. 8.Papua New Guinea Institute of Medical ResearchGorokaPapua New Guinea
  9. 9.Faculty of LettersChiba UniversityChibaJapan
  10. 10.The Japanese Red Cross Akita College of NursingAkita CityJapan
  11. 11.Graduate School of Environmental and Life ScienceOkayama UniversityOkayama CityJapan

Personalised recommendations