Can Microbes Affect Our Social Behavior?

The answer may surprise you (also the answer is yes)

Weighing in at about 20,000 genes, your genome is like an Ikea assembly manual from hell. Genes are fundamental instructions to what your body looks like and how it works: your eye color, freckles, whether or not you’re a morning person, and even if bright lights make you sneeze. But despite having sequenced thousands of human genomes, we still haven’t found all the pieces that result in a walking, talking, texting human. We’re learning more and more about what products our genes encode, but we don’t fully understand how different parts go together or how many of each piece we need. And in some cases, it even looks like our packages are missing a few key parts.

For example: One component lacking in the human genome is the ability to synthesize certain essential vitamins, like biotin and B12. Our genome doesn’t have genes for making these vitamins, and yet we do have genes that encode transporters to move the vitamins into our intestinal cells. These transporters recognize specific forms of the vitamins that are produced by bacteria that live in our intestines. We (the hosts) contain bacterial communities (our ‘gut microbiome’) that trade us nutrients in exchange for a cozy home (our guts). The complete process of making the vitamin and getting it into your cells is required for the maintenance of you. However, only part of that process is encoded by your genes.

Introducing the ‘Hologenome’

As the above example shows, our genome provides a robust, but ultimately incomplete, picture of how our bodies really work. To get the full story, we need to look at what scientists call the “hologenome.” The hologenome (“holo” is Greek for “whole”) refers to host genes, plus all the genes of its symbiotic microbes. To figure out how many genes come from our microbes, scientists sequenced DNA from human feces. They found about 3 million genes from microbial inhabitants of the gut tract. In other words, our genetic instruction manual might be about 150 times longer than we thought it was.

The massive size and complexity of the human microbiome has researchers wondering what impacts these bacteria have on their hosts. Decades of evidence suggests that microbes change the way we digest food, but it seems like an arsenal of 3 million genes could do a lot more than help you eat some corn flakes. Scientists studying other animal species have found that while bacteria are often found in the gut, they can exhibit unexpected effects on their hosts’ brains.

Consider the Fruit Fly

Credit: Scott Bauer, U.S. Department of Agriculture

To gain some perspective, scientists turned to a classic model organism: the fruit fly. Flies can be fed a variety of diets, which, just like us, influences their microbiomes. A population of flies was split into two groups: one fed molasses, the other starch. Flies fed molasses were attracted to other molasses-fed flies, whereas flies fed starch preferred other starch-fed flies. Antibiotic treatment eliminated the bias, and reinfection restored it. This behavioral change all came down to a single bacterium, Lactobacillus plantarum, which was plentiful in the starch-fed flies but rare in the other group. Further study showed that L. plantarum modified the secreted chemical pheromones that flies use for mate choice and other social communication. The biological process that had these flies swiping left was encoded in the hologenome: fly genes produced the pheromones, and bacterial genes modified them.

Pheromones: From Hyenas to Humans

Credit: Natalya Zahn

Mammals use similar pheromone signaling cues to find the perfect date, and it looks like their microbiomes have a strong influence. Hyenas deposit a smelly paste — affectionately/disgustingly referred to as hyena butter — onto grass stalks.

Wild populations of spotted and striped hyenas differentiate their packs using distinct chemical profiles of this paste, which is secreted from bacteria-filled glands. Hyena genes are the instructions for the raw material of this paste, and the bacterial genes modify these compounds to determine its signature odor profile. Even within the striped and spotted hyena groups, bacterial and chemical profiles differ between sexes and reproductive states. When a hyena gets a whiff of this paste, they’re getting a lot of information to act on. Is this hyena a friend? A potential mate? Is it a lactating female? These complex social cues all inform hyena behavior, and each are encoded across the hologenome.

Our sense of smell is less sensitive than hyenas’, but odor still plays an important role in human attraction (though perhaps at a subconscious level). The famous “T-shirt” study showed that women preferred the scent of shirts worn by men with very different immune genes from themselves. Women could smell evidence of genes that would give their children greater chances of fighting diseases. But the sweat itself is actually odorless. It’s the bacteria living in the men’s sweat glands that fermented those compounds to produce a distinct smell in each man. Once again, host genes started the process and bacterial genes finished it.

Of course, the environment also plays a part in what traits we like or dislike in our potential mates. At the end of the day, however, our genes outline the basic instructions. Maybe I have a gene encoding a preference for sports fans, and a potential mate has a gene for being enthusiastic about sports. But if I grew up in Boston and they grew up in Denver, we might be wearing mutually repulsive football jerseys when our paths finally cross.

We Are Just Scratching the Surface of How Our Microbiome Affects Behavior

For better or for worse, the genetic component of our attractions may not come from just our human cells, but from the microbes that inhabit us. The aforementioned T-shirt study could just be the tip of the iceberg — we simply don’t yet know just how important these kinds of microbial influences are when it comes to people. Given evidence for the microbial influence on mate choice in other mammals, scientists are expanding their search to look for similar determinants of human attraction in our symbiotic organisms. The mechanisms for how these host–microbe signaling events happen are still poorly understood, but the implications are clear. What makes you you and me me is not just our DNA, but the DNA of all the bacteria that live within us.

I Contain Multitudes is a multi-part video series dedicated to exploring the wonderful, hidden world of the microbiome. The series is hosted by science writer Ed Yong and produced by HHMI Tangled Bank Studios in association with Room 608.

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