Initial acquisition of microbiota

An illustration highlighting selected internal and external sources of maternal microbial transmission.

Microbiota, also known as flora, are the microorganisms that colonize an organism, including bacteria, fungi, and archaea. This article is concerned with how these organisms colonize a host in the time period immediately before or after birth. The microbiome refers to their genomes.

Many of these microorganisms interact with the host in ways that are beneficial and often play an integral role in processes like digestion and immunity.[1] The microbiome is dynamic: it varies between individuals, over time, and can influenced by both endogenous and exogenous forces.[2]

Abundant research in invertebrates [3][4][5] has shown that endosymbionts may be transmitted vertically to oocytes or externally transmitted during oviposition. Research on the acquisition of microbial communities in vertebrates is relatively sparse, but also suggests that vertical transmission may occur.[6][7]

In humans

Early hypotheses assumed that human babies are born sterile and that any bacterial presence in the uterus would be harmful to the fetus.[6] Some believed that both the womb and maternal milk were sterile, and that bacteria did not enter an infant’s intestinal tract until supplementary food was provided.[8] In 1900, the French pediatrician Henry Tissier isolated Bifidobacterium from the stool of healthy, breast-fed infants.[9][10] He concluded that breast milk was not sterile and suggested that diarrhea caused by an imbalance of intestinal flora could be treated by supplementing food with Bifidobacterium.[11] However, Tissier still claimed that the womb was sterile and that infants did not come into contact with bacteria until entering the birth canal.[10]

Over the last few decades, research on the perinatal acquisition of microbiota in humans has expanded as a result of developments in DNA sequencing technology.[6] Bacteria have been detected in umbilical cord blood,[12] amniotic fluid,[13] and fetal membranes[14] of healthy, term babies. The meconium, an infant’s first bowel movement of digested amniotic fluid, has also been shown to contain a diverse community of microbes.[12] These microbial communities consist of genera commonly found in the mouth and intestines, which may be transmitted to the uterus via the blood stream, and in the vagina, which may ascend through the cervix.[6][12]

In non-human vertebrates

In one experiment, pregnant mice were given food containing genetically labeled Enterococcus faecium.[15] The meconium of term offspring delivered by these mice via sterile C-section was found to contain labeled E. faecium, while pups from control mice given non-inoculated food did not contain E. faecium. This evidence supports the possibility of vertical microbial transmission in mammals.

Most research on vertical transmission in non-mammalian vertebrates focuses on pathogens in agricultural animals (e.g. chicken, fish).[6][16][17] It is not known whether these species also incorporate commensal flora into eggs.

In invertebrates

Marine sponges are host to many sponge-specific microbe species that are found across several sponge lineages.[18] These microbes are detected in divergent populations without overlapping ranges but are not found in the sponges' immediate environment. As a result, it is thought that the symbionts were established by a colonization event before sponges diversified and are maintained through vertical (and, to a lesser extent, horizontal) transmission.[19] The presence of microorganisms in both the oocytes and in the embryos of sponges has been confirmed.[19][20]

Many insects depend on microbial symbionts to obtain amino acids and other nutrients that are not available from their primary food source.[6] Microbiota may be passed on to offspring via bacteriocytes associated with the ovaries or developing embryo,[5][21][22] by feeding larvae with microbe-fortified food,[23] or by smearing eggs with a medium containing microbes during oviposition.[24][25]

See also

References

  1. ↑ Harmon, Katherine (16 December 2009). "Bugs Inside: What Happens When the Microbes That Keep Us Healthy Disappear?". Scientific American.
  2. ↑ Mundasad, Smitha (13 June 2012). "Human Microbiome Project reveals largest microbial map". BBC News.
  3. ↑ Feldhaar, Heike; Gross, Roy (January 2009). "Insects as hosts for mutualistic bacteria". International Journal of Medical Microbiology 299 (1): 1–8. doi:10.1016/j.ijmm.2008.05.010.
  4. ↑ Douglas, A.E. (1989). "Mycetocyte symbiosis in insects". Biological Reviews 69 (4): 409–434. doi:10.1111/j.1469-185X.1989.tb00682.x. PMID 2696562.
  5. 1 2 Buchner, P. (1965). Endosymbiosis of animals with plant microorganisms. New York: Interscience Publishers. ISBN 978-0470115176.
  6. 1 2 3 4 5 6 Funkhouser, L.J.; Bordenstein, S.R. (2013). "Mom Knows Best: The Universality of Maternal Microbial Transmission". PLoS Biol 11 (8): e1001631. doi:10.1371/journal.pbio.1001631.
  7. ↑ Gantois, Inne; Ducatelle, Richard; Pasmans, Frank; et al. (2009). "Mechanisms of egg contamination by Salmonella Enteritidis". Microbiology Reviews 33 (4): 718–738. doi:10.1111/j.1574-6976.2008.00161.x. PMID 19207743.
  8. ↑ Kendall, A.I.; Day, A.A.; Walker, A.W. (1926). "Chemistry of the Intestinal Bacteria of Artificially Fed Infants: Studies in Bacterial Metabolism". The Journal of Infectious Diseases 38 (3): 205–210. doi:10.1093/infdis/38.3.205.
  9. ↑ Weiss, J.E.; Rettger, L.F. (1938). "Taxonomic Relationships of Lactobacillus bifidus (B. bifidus Tissier) and Bacteroides bifidus". The Journal of Infectious Diseases 62 (1): 115–120. doi:10.1093/infdis/62.1.115.
  10. 1 2 Tissier, H. (1900). Recherches sur la flore intestinale des nourrissons (état normal et pathologique). Thesis. Paris: G. Carre and C. Naud.
  11. ↑ Tissier, H. (1906). Traitement des infections intestinales par la méthode de la flore bactérienne de l’intestin. CR de la Société de Biologie. 60: 359-361.
  12. 1 2 3 Jiménez, E.; et al. (2005). "Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section". Current Microbiology 51: 270–274. doi:10.1007/s00284-005-0020-3.
  13. ↑ Bearfield, C; Davenport, E.S.; et al. (2002). "Possible association between amniotic fluid microorganism infection and microflora in the mouth". British journal of obstetrics and gynecology 109: 527–533. doi:10.1016/s1470-0328(02)01349-6.
  14. ↑ Steel, J.H.; Malatos, S.; Kennea, N.; et al. (2005). "Bacteria and inflammatory cells in fetal membranes do not always cause preterm labor". Pediatric Research 57: 404–411. doi:10.1203/01.pdr.0000153869.96337.90.
  15. ↑ Jiménez, E.; Marin, M.L.; Martin, R.; et al. (April 2008). "Is meconium from healthy newborns actually sterile?". Research in Microbiology 159 (3): 187–193. doi:10.1016/j.resmic.2007.12.007.
  16. ↑ Gantois, I.; Ducatelle, R.; Pasmans, F.; et al. (2009). "Mechanisms of egg contamination by Salmonella Enteritidis". FEMS Microbiology Reviews 33: 718–738. doi:10.1111/j.1574-6976.2008.00161.x. PMID 19207743.
  17. ↑ Brock, J.A.; Bullis, R. (2001). "Disease prevention and control for gametes and embryos of fish and marine shrimp". Aquaculture 197: 137–159. doi:10.1016/s0044-8486(01)00585-3.
  18. ↑ Wilkinson, C.R. (1984). "Origin of bacterial symbioses in marine sponges". Proceedings of the Royal Society of London 220: 509–517. doi:10.1098/rspb.1984.0017.
  19. 1 2 Schmitt, S.; Angermeier, H.; Schiller, R.; et al. (2008). "Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts". Applied and Environmental Microbiology 74: 7694–7708. doi:10.1128/aem.00878-08. PMID 18820053.
  20. ↑ Schmitt, S.; Weisz, J.B.; Lindquist, N.; Hentschel, U. (2007). "Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix". Applied and Environmental Microbiology 73: 2067–2078. doi:10.1128/aem.01944-06.
  21. ↑ Koga, R.; Meng, X.Y.; Tsuchida, T.; Fukatsu, T. (2012). "Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface". Proceedings of the National Academy of Sciences USA 109: E1230–E1237. doi:10.1073/pnas.1119212109.
  22. ↑ Sacchi, L.; Grigolo, A.; Laudani, U; et al. (1985). "Behavior of symbionts during oogenesis and early stages of development in the German cockroach, Blatella germanica (Blattodea)". Journal of Invertebrate Pathology 46: 139–152. doi:10.1016/0022-2011(85)90142-9.
  23. ↑ Attardo, G.M.; Lohs, C.; Heddi, A.; et al. (2008). "Analysis of milk gland structure and function in Glossina morsitans: milk protein production, symbiont populations and fecundity". Journal of Insect Physiology 54: 1236–1242. doi:10.1016/j.jinsphys.2008.06.008. PMC 2613686. PMID 18647605.
  24. ↑ Prado, S.S.; Zucchi, T.D. (2012). "Host-symbiont interactions for potentially managing Heteropteran pests". Psyche 2012: 1–9. doi:10.1155/2012/269473.
  25. ↑ Goettler, W.; Kaltenpoth, M.; Hernzner, G.; Strohm, E. (2007). "Morphology and ultrastructure of a bacteria cultivation organ: the antennal glands of female European beewolves, Philanthus triangulum (Hymenoptera, Crabronidae)". Arthropod Structure & Development 36: 1–9. doi:10.1016/j.asd.2006.08.003.
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