Your First Birthday Present: A Microbiota

Moms go to great lengths to pass on their microbial genes.

Horse owners are often startled when they see a foal eat its mother's poop, but it's perfectly normal. Eating poop is an efficient, if indelicate, way to inherit the mare's gut microbes — her microbiota. Horses spend their entire day grazing. To process the absurdly low energy content of grass, a mature horse has a cecum containing up to eight gallons of cellulose-degrading bacteria – and that has to come from somewhere. Lots of animals – especially young ones – eat poop to jump-start their microbiota, including rabbits, koalas, pandas, pigs, geese, elephants, hippos, dogs, mice, and monkeys. And, often, humans.

When a baby is squeezed down the birth canal, we know that it picks up vaginal microbes along the way. But with all that squeezing, the baby often picks up mom's fecal microbes as well. Natural birth is far from antiseptic. From an evolutionary standpoint, that makes sense: The world is lousy with pathogens, and newborn babies are totally doomed without protective microbes. They need to be anointed with their mom's microbiota as quickly as possible. But poop? Well, if mom has a good gut, her poop will have good microbes. So, as disgusting as it sounds, a messy birth may provide an important starter kit for the baby's microbiota.

Babies born by C-section have a different microbiota, more like a hospital room. These kids have an increased likelihood of asthma and allergies than babies born vaginally. They often have higher gut permeability and lower microbial diversity, both associated with depression and anxiety. Mothers are typically given antibiotics before a C-section, so some of the microbial changes may be attributed to that as well. New research shows that many of the differences disappear after a couple of months and fortunately, C-section babies get a second chance to establish a good microbiota: Babies are born to suckle.

Breast milk is alive

Breast milk is an amazingly rich concoction of sugars, fats, and immune factors. It also contains a starter microbiota that includes live bacteria and fungus from the mother — and her mother before her. They are carefully curated from the mother's gut by dendritic cells and then ferried to the milk ducts via the lymphatic system. These microbes are accompanied by a rich broth of sugary prebiotics to feed them. In fact, most of the sugars in milk are for those microbes, not the baby. That seems callous, but it's not: The microbes convert those indigestible sugars into energy-packed fatty acids that feed the baby and nourish the gut lining.

Wait a minute

Don't we all have an immune system specifically designed to kill microbes? Even mom's microbes? How does the immune system know which ones are the good guys? The answer is early education. In anticipation of these mother-approved microbes, the baby's immune system lets down its guard. It learns to accept this initial batch of microbes. Mom's microbiota thus provides an early lesson in tolerance.

Milk also includes antibodies and white blood cells that the mother has built up against previous illness – the baby's first vaccination. Thus, mother's milk is a prebiotic, probiotic, and antibiotic formula that has played a starring role in 200 million years of mammalian history. That arrangement allows us to share genes with microbes, and we’re talking about a lot of genes; the gut microbiota has 100 times as many genes as humans do. Those microbes haven’t evolved separately from us. We have co-evolved, ensuring that both sets of genes are passed down. We need each other.

Making up your mind

Microbes play a role in brain development, an incredible statement that should give us all pause. In 2004, Nobuyuki Sudo showed that germ-free mice raised in a sterile environment develop an abnormal stress response. Sudo was able to normalize that stress response by feeding them bacteria from healthy mice. However, that only works while the mice are still young. After that, the window of education is slammed shut and the immune system settles in to an adult groove.

In 2015, Roman Stilling and Pauline Luczyinski showed that germ-free mice develop abnormal amygdalas, with unusual brain chemistry. Abnormal amygdalas are associated with anxiety, depression, and autism. As well as the amygdala, studies in John Cryan and Ted Dinan's lab have shown that a germ-free mouse may have an unusual hippocampus, a part of the brain involved with both memory and emotion. Somehow, amazingly, the microbiota is affecting the development of important memory and anxiety centers of the brain.

Mice are not people, but we use them because we can't do germ-free experiments on humans. Multiple animal studies, however, show a fundamental connection between the microbiota and the developing brain. The odds are good that something similar happens to people.

After about 1000 days, a baby has settled on its own unique microbial formula. After that, it is difficult to alter the basic structure of your microbiota, but not impossible. In future articles, I'll discuss some strategies to improve your microbial balance. Stay tuned!

References

Neu, Josef, and Jona Rushing. “Cesarean versus Vaginal Delivery: Long Term Infant Outcomes and the Hygiene Hypothesis.” Clinics in Perinatology 38, no. 2 (June 2011): 321–31.

Boix-Amorós, Alba, Fernando Puente-Sánchez, Elloise du Toit, Kaisa M. Linderborg, Yumei Zhang, Baoru Yang, Seppo Salminen, et al. “Mycobiome Profiles in Breast Milk from Healthy Women Depend on Mode of Delivery, Geographic Location and Interaction with Bacteria.” Appl. Environ. Microbiol., March 1, 2019, AEM.02994-18.

Funkhouser, Lisa J., and Seth R. Bordenstein. “Mom Knows Best: The Universality of Maternal Microbial Transmission.” PLOS Biol 11, no. 8 (August 20, 2013): e1001631.

Dinan, Timothy G., and John F. Cryan. “Gut Instincts: Microbiota as a Key Regulator of Brain Development, Ageing and Neurodegeneration.” The Journal of Physiology 595, no. 2 (2017): 489–503.

Sudo, Nobuyuki, Yoichi Chida, Yuji Aiba, Junko Sonoda, Naomi Oyama, Xiao-Nian Yu, Chiharu Kubo, and Yasuhiro Koga. “Postnatal Microbial Colonization Programs the Hypothalamic-Pituitary-Adrenal System for Stress Response in Mice.” The Journal of Physiology 558, no. Pt 1 (July 1, 2004): 263–75.

Stilling, Roman M., Feargal J. Ryan, Alan E. Hoban, Fergus Shanahan, Gerard Clarke, Marcus J. Claesson, Timothy G. Dinan, and John F. Cryan. “Microbes & Neurodevelopment--Absence of Microbiota during Early Life Increases Activity-Related Transcriptional Pathways in the Amygdala.” Brain, Behavior, and Immunity 50 (November 2015): 209–20.