TY - JOUR
T1 - Diversity and temporal dynamics of primate milk microbiomes
AU - Muletz-Wolz, Carly R.
AU - Kurata, Naoko P.
AU - Himschoot, Elizabeth A.
AU - Wenker, Elizabeth S.
AU - Quinn, Elizabeth A.
AU - Hinde, Katie
AU - Power, Michael L.
AU - Fleischer, Robert C.
N1 - Funding Information:
We thank the animals and their keepers for providing and assisting in sample collection. Specifically, we thank Erin Stromberg of the National Zoological Park and Jennifer Mickelberg and Jodi Carrigan of Zoo Atlanta for coordinating the collection of gorilla and orangutan milk. Lauren Milligan Newmark was essential for the samples from the Fresno Zoo. We thank Larry Williams of the M.D. Anderson Cancer Center for the owl monkey samples. The howler monkey samples were courtesy of Ken Glander. We thank Nancy McInerney and Charlie Wang for guidance in molecular procedures. We thank the US Food and Drug Administration and Marc Allard for providing a GS FLX+ to CCG. We thank Caitlin Arlotta and Katie Murtough for help in the initial phase of this project. This project was funded by a Smithsonian Competitive Grant for Science (MLP and RCF) and PHS grant R24OD020347. Additional funding included NSF (DDIG 0525025 awarded to K.H. and Joan Silk and DDIG: 0746320 awarded to E.Q. and Chris Kuzawa), NIH (RR019970 & RR000169 awarded to John Capitanio and the California National Primate Research Center, and DK77639 awarded to MLP), and American Society of Primatologists awarded to K.H.
Publisher Copyright:
© 2019 Wiley Periodicals, Inc.
PY - 2019/10/1
Y1 - 2019/10/1
N2 - Milk is inhabited by a community of bacteria and is one of the first postnatal sources of microbial exposure for mammalian young. Bacteria in breast milk may enhance immune development, improve intestinal health, and stimulate the gut-brain axis for infants. Variation in milk microbiome structure (e.g., operational taxonomic unit [OTU] diversity, community composition) may lead to different infant developmental outcomes. Milk microbiome structure may depend on evolutionary processes acting at the host species level and ecological processes occurring over lactation time, among others. We quantified milk microbiomes using 16S rRNA high-throughput sequencing for nine primate species and for six primate mothers sampled over lactation. Our data set included humans (Homo sapiens, Philippines and USA) and eight nonhuman primate species living in captivity (bonobo [Pan paniscus], chimpanzee [Pan troglodytes], western lowland gorilla [Gorilla gorilla gorilla], Bornean orangutan [Pongo pygmaeus], Sumatran orangutan [Pongo abelii], rhesus macaque [Macaca mulatta], owl monkey [Aotus nancymaae]) and in the wild (mantled howler monkey [Alouatta palliata]). For a subset of the data, we paired microbiome data with nutrient and hormone assay results to quantify the effect of milk chemistry on milk microbiomes. We detected a core primate milk microbiome of seven bacterial OTUs indicating a robust relationship between these bacteria and primate species. Milk microbiomes differed among primate species with rhesus macaques, humans and mantled howler monkeys having notably distinct milk microbiomes. Gross energy in milk from protein and fat explained some of the variations in microbiome composition among species. Microbiome composition changed in a predictable manner for three primate mothers over lactation time, suggesting that different bacterial communities may be selected for as the infant ages. Our results contribute to understanding ecological and evolutionary relationships between bacteria and primate hosts, which can have applied benefits for humans and endangered primates in our care.
AB - Milk is inhabited by a community of bacteria and is one of the first postnatal sources of microbial exposure for mammalian young. Bacteria in breast milk may enhance immune development, improve intestinal health, and stimulate the gut-brain axis for infants. Variation in milk microbiome structure (e.g., operational taxonomic unit [OTU] diversity, community composition) may lead to different infant developmental outcomes. Milk microbiome structure may depend on evolutionary processes acting at the host species level and ecological processes occurring over lactation time, among others. We quantified milk microbiomes using 16S rRNA high-throughput sequencing for nine primate species and for six primate mothers sampled over lactation. Our data set included humans (Homo sapiens, Philippines and USA) and eight nonhuman primate species living in captivity (bonobo [Pan paniscus], chimpanzee [Pan troglodytes], western lowland gorilla [Gorilla gorilla gorilla], Bornean orangutan [Pongo pygmaeus], Sumatran orangutan [Pongo abelii], rhesus macaque [Macaca mulatta], owl monkey [Aotus nancymaae]) and in the wild (mantled howler monkey [Alouatta palliata]). For a subset of the data, we paired microbiome data with nutrient and hormone assay results to quantify the effect of milk chemistry on milk microbiomes. We detected a core primate milk microbiome of seven bacterial OTUs indicating a robust relationship between these bacteria and primate species. Milk microbiomes differed among primate species with rhesus macaques, humans and mantled howler monkeys having notably distinct milk microbiomes. Gross energy in milk from protein and fat explained some of the variations in microbiome composition among species. Microbiome composition changed in a predictable manner for three primate mothers over lactation time, suggesting that different bacterial communities may be selected for as the infant ages. Our results contribute to understanding ecological and evolutionary relationships between bacteria and primate hosts, which can have applied benefits for humans and endangered primates in our care.
KW - bacteria
KW - breast milk
KW - infant
KW - lactation
KW - mammals
KW - microbiota
KW - symbiosis
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U2 - 10.1002/ajp.22994
DO - 10.1002/ajp.22994
M3 - Article
C2 - 31219214
AN - SCOPUS:85067890403
VL - 81
JO - American Journal of Primatology
JF - American Journal of Primatology
SN - 0275-2565
IS - 10-11
M1 - e22994
ER -