Our bodies are a global marketplace where bacteria trade genes

By Ed Yong | October 31, 2011 9:00 am

There is a vast, unseen marketplace that connects us all. The traders are the trillions of bacteria that live on or within our bodies; the commodities they exchange are genes. This flow of genes around our bodies allows bacteria to rapidly evolve new skills, including the abilities to resist antibiotics, cause disease, or break down environmental chemicals. In the past, scientists have caught glimpses of individual deals, but now the full size of the marketplace is becoming clear.

The human body is home to 100 trillion microbes, whose cells outnumber ours by ten to one, and whose genes outnumber ours by a hundred to one. These genes are not only more numerous than ours, but they operate under different rules. While we can only pass down our DNA to our children, bacteria and other microbes can swap genes between one another. For example, the gut bacteria of Japanese people have a gene that helps them to digest seaweed. They borrowed it from an oceanic species that hitched its way into Japanese bowels, aboard uncooked pieces of sushi.

This was an isolated example, but such ‘horizontal gene transfers’ are fairly commonplace. When Chris Smillie and Mark Smith from MIT looked at the genomes of over 2,200 species of bacteria, they found 10,000 genes that had been recently swapped. These genes were more than 99 percent identical, even though they came from bacteria that were distantly related*. Standing out like beacons of similarity amid seas of difference, they must have been transferred from one species to another, rather than inherited from mother cell to daughter.

Our bodies turn out to be hotbeds of horizontal transfers. Around half of the bacteria species from Smillie and Smith’s study are part of the human microbiome – a term that refers to our collective microbes and the genes they carry. These species are 25 times more likely to have swapped genes with one another than those that have nothing to do with humans. The x-axis represents the evolutionary relationships between two species of bacteria: the further to the right, the more distantly they’re related. The y-axis shows the frequency of genetic trades.

The graph also shows that these exchanges are largely dictated by the environments that different species live in. To bacteria, our bodies are worlds of different habitats, from rainforest-like armpits to desert-like forearms. Perhaps unsurprisingly, species that inhabit the same body parts are particularly strong trading partners. Even those that live in the gums, for example, are more likely to swap genes with other gum species than those from elsewhere in the mouth.

In this way, ecology trumps history and geography. Bacteria that are separated by billions of years of evolution can still transfer genes to one another, as can species that live on different continents – what matters is that they share the same environment. If that’s the case, they’re more likely to swap genes than close relatives from different habitats.

These incoming genes probably make bacteria even better adapted to their particular niches, just like seaweed-digesting genes allowed Japanese gut bacteria to break down a commonly encountered food. The most beneficial genes are likely to spread quickly through the local species. By searching for them, Smillie and Smith hope to identify the genetic ace cards that give bacteria an edge in a given environment. They have already started to identify transferred genes associated with life in hot springs or soil, and those that allow disease-causing bacteria to cause infections and resist antibiotics.

The latter group could be particularly useful to us. For example, the bacteria that cause meningitis have 24,000 mystery genes. No one knows what they do, and it would take too long to test them all to see which, if any, help the bacteria to infect humans. But Smilie and Smith found that 13 of these genes have been recently acquired from other species – they are a good place to start.

They also identified 42 antibiotic-resistance genes that had hopped into the human microbiome from bacteria that contaminate food, or live in farm animals. These microbes can act as proving grounds for genetic defences that eventually find their way into human infections.

Smillie and Smith also found that 43 resistance genes in the human microbiome hadn’t just transferred between bacteria, but across national borders. The genes were identical in different bacterial species sampled from different countries. Nothing makes it clearer that our bacteria are connected in ways that transcend our bodies and even our nations. If we introduce new genes, say for resisting antibiotics, into a local pool, we can soon pay an international price.

Reference: Smilie, Smith, Friedman, Cordero, David & Alm. 2011. Ecology drives a global network of gene exchange connecting the human microbiome. Nature http://dx.doi.org/doi:10.1038/nature10571

Photo by Ester Inbar

An introductory slideshow to the microbiome:

mouse_neurons_gut_bacteria
apes
bacteria-with-guts
genetic-loans
introduction
our-zeroeth-birthday-present
poliovirus_reovirus
the-bacteria-that-make-you-
the-zoo-on-your-skin
your-are-what-you-eat

Comments (4)

  1. Rebecca

    Mark Smith, the lead scientist on this project is answering questions from users about the study here: http://www.zopost.com/article?articleId=6

  2. James Freeman

    Mark,

    Some very interesting research. I do have some questions:

    1. Does it follow from your findings that each human, in creating a unique “market-place”, could have a unique population/species of bacteria found no where else? Is it possible to define separable species in this context, when there is such widescale trading of genetic material?

    2. How quickly in the life of a human does the “marketplace” get established? Does it happen in utero (and if so, how do they get there?), or, within the days and weeks after birth?

    3. Do the residents change with changes in age and diet, or, do the existing residents adapt to the changing environment genetically, or, do they simply switch on/off existing protein catalysts (where they have them) to respond to shifts in food availability?

    4. How does the production of IgA in the mucosal lining of the intestine influence the “marketplace”?

  3. Hi James,

    These are insightful questions!

    1) Although many bacterial strains and genes are common and shared among many of us, we do suspect that each person harbors their own, unique bacterial community (possibly enabling forensic use as described here: http://www.pnas.org/content/107/14/6477). Although we know this is true at the species level, we’re still unclear whether its true at the level of transferred genes – this is an active area of research in our lab at the moment. Your second question about the difficulty of defining bacterial species in the context of promiscuous HGT highlights a deep, open problem in the microbiology community. I’m afraid I don’t have much additional insight to offer here, although I’ll point out that its possible that a core set of genes are transferred much less than the mobile set that we studied. Although the promiscuous nature of HGT means that the concept of ‘species’ among bacteria is undoubtedly quite different from what we think of among vertebrates etc, it is possible to trace bacterial lineages from these core genes which are transferred much less frequently.

    2) Bacterial communities are established quickly after birth (http://www.pnas.org/content/early/2010/07/27/1000081107) but are not believed to assemble in utero. This community assembly process is likely critical for proper immunological development and inadequate or inappropriate exposure underlies the so called ‘hygiene hypothesis’ for many immunological disorders observed in developed countries.

    3) You’ve addressed another very important open question in the field here. This is an area of very active research in ours and other groups. You can expect some interesting results will be published to address these questions in the near future!

    4) IgA is one of several important mechanisms by which our immune systems interact with our microbiota. Although it is almost certain that host immunity plays an important role in shaping our bacterial communities, we haven’t yet determined exactly what the implications are of these interactions.

    These are great points – we’re happy to answer more questions as they arise!

    All the best,
    Mark

  4. James Freeman

    Mark,

    As I get older (I’m 43), I find myself coming back to my love of science (MSc in Electrical Engineering, but that was half my life ago….) in part, prompted by questions my children ask. As a sometimes sufferer of “IBS”, I’m interested in following the latest science in this area, and your work very much hits home. Please keep it up, and thank you for taking the time to respond to my modest questions.

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