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Milk microbiomes of three great ape species vary among host species and over time

  • Kim, S. Y. & Yi, D. Y. Components of human breast milk: From macronutrient to microbiome and microRNA. Clin. Exp. Pediatr. 63(8), 301 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Power, M. L. & Schulkin, J. Maternal regulation of offspring development in mammals is an ancient adaptation tied to lactation. Appl. Transl. Genomics. 2, 55–63 (2013).

    CAS 
    Article 

    Google Scholar 

  • Pannaraj, P. S. et al. Association between breast milk bacterial communities and establishment and development of the infant gut microbiome. JAMA Pediatr. 171(7), 647–654 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Lyons, K. E., Ryan, C. A., Dempsey, E. M., Ross, R. P. & Stanton, C. Breast milk, a source of beneficial microbes and associated benefits for infant health. Nutrients 12(4), 1039 (2020).

    CAS 
    PubMed Central 
    Article 

    Google Scholar 

  • Fehr, K. et al. Breastmilk feeding practices are associated with the co-occurrence of bacteria in mothers’ milk and the infant gut: The CHILD cohort study. Cell Host Microbe. 28(2), 285–297 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Moossavi, S. & Azad, M. B. Origins of human milk microbiota: New evidence and arising questions. Gut Microbes. 12(1), 1667722. https://doi.org/10.1080/19490976.2019.1667722 (2020).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Groer, M. W., Morgan, K. H., Louis-Jacques, A. & Miller, E. M. A scoping review of research on the human milk microbiome. J. Hum. Lact. 36(4), 628–643 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Gopalakrishna, K. P. & Hand, T. W. Influence of maternal milk on the neonatal intestinal microbiome. Nutrients 12(3), 823 (2020).

    CAS 
    PubMed Central 
    Article 

    Google Scholar 

  • Ayoub Moubareck, C., Lootah, M., Tahlak, M. & Venema, K. Profiles of human milk oligosaccharides and their relations to the milk microbiota of breastfeeding mothers in Dubai. Nutrients 12(6), 1727 (2020).

    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Henrick, B. M. et al. Bifidobacteria-mediated immune system imprinting early in life. Cell 184, 3884–3898 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Walker, W. A. & Iyengar, R. S. Breast milk, microbiota, and intestinal immune homeostasis. Pediatr. Res. 77(1), 220–228 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Petrullo, L. et al. The early life microbiota mediates maternal effects on offspring growth in a nonhuman primate. Iscience. 25(3), 103948 (2022).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bowen, W. D., Boness, D. J. & Oftedal, O. T. Mass transfer from mother to pup and subsequent mass loss by the weaned pup in the hooded seal, Cystophora cristata. Can. J. Zool. 65(1), 1–8 (1987).

    Article 

    Google Scholar 

  • Smith, T. M., Austin, C., Hinde, K., Vogel, E. R. & Arora, M. Cyclical nursing patterns in wild orangutans. Sci. Adv. 3(5), e1601517 (2017).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Park, Y. W. & Haenlein, G. F. W. Handbook of Milk of Non-Bovine Mammals (Wiley, 2008).

    Google Scholar 

  • Oftedal, O. T. Use of maternal reserves as a lactation strategy in large mammals. Proc. Nutr. Soc. 59(1), 99–106 (2000).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Hinde, K. & Milligan, L. A. Primate milk: Proximate mechanisms and ultimate perspectives. Evol. Anthropol. Issues News Rev. 20(1), 9–23 (2011).

    Article 

    Google Scholar 

  • Osthoff, G., Hugo, A., De Wit, M., Nguyen, T. P. M. & Seier, J. Milk composition of captive vervet monkey (Chlorocebus pygerythrus) and rhesus macaque (Macaca mulatta) with observations on gorilla (Gorilla gorilla gorilla) and white handed gibbon (Hylobates lar). Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 152(4), 332–338 (2009).

    CAS 
    Article 

    Google Scholar 

  • Power, M. L., Oftedal, O. T. & Tardif, S. D. Does the milk of callitrichid monkeys differ from that of larger anthropoids?. Am. J. Primatol. Off. J. Am. Soc. Primatol. 56(2), 117–127 (2002).

    Google Scholar 

  • Power, M. L. et al. Patterns of milk macronutrients and bioactive molecules across lactation in a western lowland gorilla (Gorilla gorilla) and a Sumatran orangutan (Pongo abelii). Am. J. Primatol. 79(3), e22609 (2017).

    Article 
    CAS 

    Google Scholar 

  • Garcia, M., Power, M. L. & Moyes, K. M. Immunoglobulin A and nutrients in milk from great apes throughout lactation. Am. J. Primatol. 79(3), e22614 (2017).

    Article 
    CAS 

    Google Scholar 

  • Muletz-Wolz, C. R. et al. Diversity and temporal dynamics of primate milk microbiomes. Am. J. Primatol. 81(10–11), e22994 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Rodríguez, J. M. The origin of human milk bacteria: Is there a bacterial entero-mammary pathway during late pregnancy and lactation?. Adv. Nutr. 5(6), 779–784 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • LaTuga MS, Stuebe A, Seed PC. A review of the source and function of microbiota in breast milk. In Seminars in Reproductive Medicine, Vol 32, 68–73 (Thieme Medical Publishers, 2014).

  • Chen, W. et al. Lactation stage-dependency of the sow milk microbiota. Front. Microbiol. 9, 945 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • McInnis, E. A., Kalanetra, K. M., Mills, D. A. & Maga, E. A. Analysis of raw goat milk microbiota: Impact of stage of lactation and lysozyme on microbial diversity. Food Microbiol. 46, 121–131 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Gonzalez, E. et al. Distinct changes occur in the human breast milk microbiome between early and established lactation in breastfeeding Guatemalan mothers. Front. Microbiol. 12, 194 (2021).

    Article 

    Google Scholar 

  • Ge, Y. et al. The maternal milk microbiome in mammals of different types and its potential role in the neonatal gut microbiota composition. Animals 11(12), 3349 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Kordy, K. et al. Contributions to human breast milk microbiome and enteromammary transfer of Bifidobacterium breve. PLoS ONE 15(1), e0219633 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Jost, T., Lacroix, C., Braegger, C. & Chassard, C. Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutr. Rev. 73(7), 426–437 (2015).

    PubMed 
    Article 

    Google Scholar 

  • Fernández, L. et al. The human milk microbiota: Origin and potential roles in health and disease. Pharmacol. Res. 69(1), 1–10 (2013).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Cabrera-Rubio, R. et al. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am. J. Clin. Nutr. 96(3), 544–551 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Gomez-Gallego, C., Garcia-Mantrana, I., Salminen, S. & Collado, M. C. The human milk microbiome and factors influencing its composition and activity. In Seminars in Fetal and Neonatal Medicine. Vol 21, 400–405 (Elsevier, 2016).

  • Khodayar-Pardo, P., Mira-Pascual, L., Collado, M. C. & Martínez-Costa, C. Impact of lactation stage, gestational age and mode of delivery on breast milk microbiota. J. Perinatol. 34(8), 599–605 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wan, Y. et al. Human milk microbiota development during lactation and its relation to maternal geographic location and gestational hypertensive status. Gut Microbes. 11(5), 1438–1449 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Hunt, K. M. et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE 6(6), e21313 (2011).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Petrullo, L., Jorgensen, M. J., Snyder-Mackler, N. & Lu, A. Composition and stability of the vervet monkey milk microbiome. Am. J. Primatol. 81(10–11), e22982 (2019).

    PubMed 

    Google Scholar 

  • Mittermeier, R. A. et al. Primates in peril: The world’s 25 most endangered primates 2008–2010. Primate Conserv. 24(1), 1–57 (2009).

    Article 

    Google Scholar 

  • Williams, J. E. et al. Human milk microbial community structure is relatively stable and related to variations in macronutrient and micronutrient intakes in healthy lactating women. J. Nutr. 147(9), 1739–1748 (2017).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kumar, H. et al. Distinct patterns in human milk microbiota and fatty acid profiles across specific geographic locations. Front. Microbiol. 7, 1619 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Keady, M. et al. Clinical health issues, reproductive hormones, and metabolic hormones associated with gut microbiome structure in African and Asian elephants. Anim. Microbiome. 3, 1–19 (2021).

    Article 
    CAS 

    Google Scholar 

  • RStudio Team. RStudio: Integrated Development for R. http://www.rstudio.com/ (2020).

  • Bolyen, E. et al. QIIME 2: Reproducible, Interactive, Scalable, and Extensible Microbiome Data Science. PeerJ Preprints (2018).

  • Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods. 13(7), 581 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Cole, J. R. et al. Ribosomal Database Project: Data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42(D1), D633–D642 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Davis, N. M., Proctor, D. M., Holmes, S. P., Relman, D. A. & Callahan, B. J. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome. 6(1), 1–14 (2018).

    Article 

    Google Scholar 

  • McMurdie, P. J. & Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8(4), e61217 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Beule, L. & Karlovsky, P. Improved normalization of species count data in ecology by scaling with ranked subsampling (SRS): Application to microbial communities. PeerJ 8, e9593 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Gloor, G. B., Macklaim, J. M., Pawlowsky-Glahn, V. & Egozcue, J. J. Microbiome datasets are compositional: And this is not optional. Front. Microbiol. 8, 2224 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Oksanen, J. et al. vegan: Community Ecology Package. https://cran.r-project.org/package=vegan (2020).

  • Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289–300 (1995).

    MathSciNet 
    MATH 

    Google Scholar 

  • Kumbhare, S. V., Patangia, D. V., Patil, R. H., Shouche, Y. S. & Patil, N. P. Factors influencing the gut microbiome in children: From infancy to childhood. J. Biosci. 44(2), 1–19 (2019).

    Article 

    Google Scholar 

  • Amato, K. R. et al. Phylogenetic and ecological factors impact the gut microbiota of two Neotropical primate species. Oecologia 180(3), 717–733 (2016).

    ADS 
    PubMed 
    Article 

    Google Scholar 

  • Mulligan, M. E. et al. Methicillin-resistant Staphylococcus aureus: A consensus review of the microbiology, pathogenesis, and epidemiology with implications for prevention and management. Am. J. Med. 94(3), 313–328 (1993).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ruegg, P. L. A 100-Year Review: Mastitis detection, management, and prevention. J. Dairy Sci. 100(12), 10381–10397 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Clarridge, J. E. III. Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin. Microbiol. Rev. 17(4), 840–862 (2004).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Martín, V., Mediano, P., Del Campo, R., Rodríguez, J. M. & Marín, M. Streptococcal diversity of human milk and comparison of different methods for the taxonomic identification of streptococci. J. Hum. Lact. 32(4), NP84–NP94 (2016).

    PubMed 
    Article 

    Google Scholar 

  • Ghebremedhin, B., Layer, F., Konig, W. & Konig, B. Genetic classification and distinguishing of Staphylococcus species based on different partial gap, 16S rRNA, hsp60, rpoB, sodA, and tuf gene sequences. J. Clin. Microbiol. 46(3), 1019–1025 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Chen, Q. et al. Quantification of human oral and fecal Streptococcus parasanguinis by use of quantitative real-time PCR targeting the groEL gene. Front. Microbiol. 10, 2910 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Plows, J. F. et al. Longitudinal changes in human milk oligosaccharides (HMOs) over the course of 24 months of lactation. J. Nutr. 151(4), 876–882 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Boehm, G. & Stahl, B. Oligosaccharides from milk. J. Nutr. 137(3), 847S-849S (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • van Leeuwen, S. S. et al. Goat milk oligosaccharides: Their diversity, quantity, and functional properties in comparison to human milk oligosaccharides. J. Agric. Food Chem. 68(47), 13469–13485 (2020).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Tao, N. et al. Evolutionary glycomics: Characterization of milk oligosaccharides in primates. J. Proteome Res. 10(4), 1548–1557 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Yu, Z.-T., Chen, C. & Newburg, D. S. Utilization of major fucosylated and sialylated human milk oligosaccharides by isolated human gut microbes. Glycobiology 23(11), 1281–1292 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bolotin, A. et al. Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus. Nat. Biotechnol. 22(12), 1554–1558 (2004).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Schwab, C. & Gänzle, M. Lactic acid bacteria fermentation of human milk oligosaccharide components, human milk oligosaccharides and galactooligosaccharides. FEMS Microbiol. Lett. 315(2), 141–148 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Marcobal, A. et al. Consumption of human milk oligosaccharides by gut-related microbes. J. Agric. Food Chem. 58(9), 5334–5340 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Uriot, O. et al. Streptococcus thermophilus: From yogurt starter to a new promising probiotic candidate?. J. Funct. Foods. 37, 74–89 (2017).

    CAS 
    Article 

    Google Scholar 

  • Duar, R. M., Henrick, B. M., Casaburi, G. & Frese, S. A. Integrating the ecosystem services framework to define dysbiosis of the breastfed infant gut: The role of B. infantis and human milk oligosaccharides. Front. Nutr. 7, 33 (2020).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Singh, R. P., Niharika, J., Kondepudi, K. K., Bishnoi, M. & Tingirikari, J. M. R. Recent understanding of human milk oligosaccharides in establishing infant gut microbiome and roles in immune system. Food Res. Int. 151, 110884. https://doi.org/10.1016/j.foodres.2021.110884 (2022).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Ximenez, C. & Torres, J. Development of microbiota in infants and its role in maturation of gut mucosa and immune system. Arch. Med. Res. 48(8), 666–680. https://doi.org/10.1016/j.arcmed.2017.11.007 (2017).

    Article 
    PubMed 

    Google Scholar 

  • Meehan, C. L. et al. Social networks, cooperative breeding, and the human milk microbiome. Am. J. Hum. Biol. 30(4), e23131 (2018).

    PubMed 
    Article 

    Google Scholar 

  • Bornbusch, S. L. et al. Stable and transient structural variation in lemur vaginal, labial and axillary microbiomes: Patterns by species, body site, ovarian hormones and forest access. FEMS Microbiol. Ecol. 96(6), fiaa090 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Bornbusch, S. L. & Drea, C. M. Antibiotic resistance genes in lemur gut and soil microbiota along a gradient of anthropogenic disturbance. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2021.704070 (2021).

    Article 

    Google Scholar 

  • Grieneisen, L. E. et al. Genes, geology and germs: Gut microbiota across a primate hybrid zone are explained by site soil properties, not host species. Proc. R. Soc. B. 2019(286), 20190431 (1901).

    Google Scholar 

  • Ellison, S. et al. The influence of habitat and phylogeny on the skin microbiome of amphibians in Guatemala and Mexico. Microb. Ecol. 78(1), 257–267 (2019).

    PubMed 
    Article 

    Google Scholar 

  • Phillips, C. D. et al. Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol. Ecol. 21(11), 2617–2627 (2012).

    PubMed 
    Article 

    Google Scholar 


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