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Structural characterization of neutral and acidic oligosaccharides in the milks of strepsirrhine primates: greater galago, aye-aye, Coquerel’s sifaka and mongoose lemur

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Abstract

The structures of milk oligosaccharides were characterized for four strepsirrhine primates to examine the extent to which they resemble milk oligosaccharides in other primates. Neutral and acidic oligosaccharides were isolated from milk of the greater galago (Galagidae: Otolemur crassicaudatus), aye-aye (Daubentoniidae: Daubentonia madagascariensis), Coquerel’s sifaka (Indriidae: Propithecus coquereli) and mongoose lemur (Lemuridae: Eulemur mongoz), and their chemical structures were characterized by 1H-NMR spectroscopy. The oligosaccharide patterns observed among strepsirrhines did not appear to correlate to phylogeny, sociality or pattern of infant care. Both type I and type II neutral oligosaccharides were found in the milk of the aye-aye, but type II predominate over type I. Only type II oligosaccharides were identified in other strepsirrhine milks. α3′-GL (isoglobotriose, Gal(α1-3)Gal(β1-4)Glc) was found in the milks of Coquerel’s sifaka and mongoose lemur, which is the first report of this oligosaccharide in the milk of any primate species. 2′-FL (Fuc(α1-2)Gal(β1-4)Glc) was found in the milk of an aye-aye with an ill infant. Oligosaccharides containing the Lewis x epitope were found in aye-aye and mongoose lemur milk. Among acidic oligosaccharides, 3′-N-acetylneuraminyllactose (3′-SL-NAc, Neu5Ac(α2-3)Gal(β1-4)Glc) was found in all studied species, whereas 6′-N-acetylneuraminyllactose (6′-SL-NAc, Neu5Ac(α2-6)Gal(β1-4)Glc) was found in all species except greater galago. Greater galago milk also contained 3′-N-glycolylneuraminyllactose (3′-SL-NGc, Neu5Gc(α2-3)Gal(β1-4)Glc). The finding of a variety of neutral and acidic oligosaccharides in the milks of strepsirrhines, as previously reported for haplorhines, suggests that such constituents are ancient rather than derived features, and are as characteristic of primate lactation is the classic disaccharide, lactose.

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Acknowledgements

We thank Global COE Program “Frontier Program for Animal Global Health and Hygiene”; Ministry of Education, Culture, Sports, Science, and Technology, Japan for supporting the travel of Dr. Akitsugu Senda to the Smithsonian National Zoological Park (SNZP) in Washington, DC for the purpose of extracting carbohydrates from milk samples. We thank Kelly Glenn and the staff of the Duke Lemur Center for assistance with milk collection and Michael Jakubasz for his assistance at SNZP. A portion of the work at the Duke Lemur Center was supported by National Science Foundation grant # DBI-0549091.

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  1. Chris Tilden

    Present address: No Orgname, 1607 W Jefferson St, Boise, ID, USA

  2. Epi Taufik

    Present address: Faculty of Animal Science, Bogor Agricultural University, Bogor, Indonesia

Authors and Affiliations

  1. Graduate School of Animal and Food Hygiene, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido, 080-8555, Japan

    Epi Taufik, Kenji Fukuda, Akitsugu Senda & Tadasu Urashima

  2. Graduate School of Agriculture, Tohoku University, Sendai, Japan

    Tadao Saito

  3. Duke Lemur Center, Durham, NC, USA

    Cathy Williams & Chris Tilden

  4. Smithsonian Environmental Research Center, Edgewater, MD, USA

    Regina Eisert & Olav Oftedal

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  1. Epi Taufik
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Taufik, E., Fukuda, K., Senda, A. et al. Structural characterization of neutral and acidic oligosaccharides in the milks of strepsirrhine primates: greater galago, aye-aye, Coquerel’s sifaka and mongoose lemur. Glycoconj J 29, 119–134 (2012). https://doi.org/10.1007/s10719-012-9370-9

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