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Not Exactly Rocket Science
« Butchered or trampled? Gloves come off in bone mark debate
Sharks gone walkabout – how Australian great whites ended up in the Mediterranean »

Gut bacteria recap the evolution of apes

Gorilla

Welcome to Humanville, a lively metropolis of over a hundred trillion bacteria living in and around your body. Like many cities, most of Humanville’s denizens live in its centre – the bowels – although a sizeable population have set up shop in the surrounding suburbs of the skin. The residents of Humanville, collectively known as the microbiome, are model citizens. They’re the unseen force that processes much of the city’s food supply, regulates its defences against invaders, and keeps it working like a healthy, well-oiled machine.

Humanville isn’t alone. It is one of many similar bacterial conurbations, each thriving in the body of a different animal. Those that live in humans have understandably received the most scientific attention. But Howard Ochman from the University of Arizona wanted to go further afield to study at the locals who live in neighbouring cities – Gorillaville, Chimpville, Bonoboville and so on.

He found that the evolution of these microbes mirrors those of their hosts to a remarkable degree. As an example, the bacteria found in two species of gorilla are more closely related to each other than either one is to the inhabitants of Humanville. The bottom line: you could reconstruct the evolution of the apes, simply by comparing the bacteria in their bowels (provided you used the right methods; more on this later).

In some ways, this isn’t surprising. In the womb, Humanville is empty. It receives its first batch of bacterial migrants at the moment of birth, when they flood in from mum’s vaginal tract. If this was all there was to it, you would naturally expect the bacteria to evolve in the same trajectory as their hosts. But the environment can also change this microscopic community.

As we get older, the bacteria of Humanville change to cope with different sources of food, from the milky diets of babies to the complex carbohydrates of adulthood. As adults, our diet also affects our bowel buddies. In African villages where high-fibre diets are the norm, Humanville is populated by plant-digesting microbes that are relatively rarer in the guts of fat-guzzling Europeans. Diseases, courses of antibiotics, and changes in body weight can also shift the balance of the microbiome, causing some members to move in and others to leave.

But Ochman’s work suggests that these individual variations obscure a broader pattern. Geography, diet and disease aside, the main thing that influences the members of these bacterial cities is the species of the host. There may be millions of variations on the Humanville theme, but as a whole, these communities share common traits that distinguish them from the bacteria in Gorillaville, Chimpville and so on.

Two years ago, Ruth Ley also found that communities of gut bacteria are mainly influenced by the species of their host. By sampling the dung of over 60 species of mammals, including 17 primates, she found that even zoo animals from separate continents had similar microbes in their stools.

However, she also found that the evolutionary relationships between these communities were odd, and certainly nothing like the family trees that link their hosts. Instead, the bacterial tree seemed to be defined by diet. For example, there was a ‘generalist’ branch that included bacteria from humans, gorillas, bonobos, lemurs, elephants and armadillos. The microbes from chimps, orang-utans and flying foxes clustered on a different part of the tree entirely.

But Ley’s study, large though it was, involved a lot of captive animals that were raised in zoos. To get a more realistic perspective on the gut bacteria of wild apes, Ochman relied on a massive bank of ape poo, collected by experienced trackers from remote sites across central Africa. All in all, he analysed 26 samples taken from two species of gorilla (western lowland and eastern lowland), bonobos, three subspecies of chimps, and humans.

These samples, combined with a far more detailed look at the genes of the bacteria within, gave Ochman a family tree that mirrors the relationships between the host species. The three versions of Chimpville – one for each subspecies – all clustered together on a tight branch, as did the two Gorillavilles. The host species completely overwhelms the influence of things like geography. For example, one of the chimp groups lives in the same area as one of the gorillas, but their gut bacteria are only distantly related.

The two diagrams below highlight this match – the one on the left is built using the apes’ own DNA, and the one on the right comes from the DNA of their bacterial tenants. The odds of randomly getting such a close match are just one in two million.

Ape_trees

Of course, it could be the case that the apes all eat unique diets, and that it’s this that determines in the bacteria in their bowels. But Ochman ruled out that explanation. In his stool samples, he also sequenced genes from chloroplasts, small compartments inside every plant cell that carry their own small genomes. These genes tell us about the types of plants that the apes were eating, and Ochman couldn’t find any clear differences between the veggie diets of the different species. As he concludes, “It seems after all that you are not what you eat.”

NB: I use “bacteria” in this story as an unfortunate shorthand. Alongside bacteria, gut communities also contain archaea – a group of microbes that look superficially similar to bacteria but are vastly different in terms of their biochemistry and evolutionary history.

Reference: PloS Biology http://dx.doi.org/10.1371/journal.pbio.1000546

Image: by me

More on microbiomes:

  • An introduction to the microbiome
  • Gut bacteria change the sexual preferences of fruit flies
  • You are what you eat – how your diet defines you in trillions of ways
  • Baby’s first bacteria depend on route of delivery
  • The bacterial zoo in your bowel
  • Gut bacteria reflect diet and evolutionary past
  • Gut bacteria – fat or thin, family or friends, shared or unique

If the citation link isn’t working, read why here
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An introduction to the microbiome

<p>You could be sitting alone and still be completely outnumbered for your body is home to trillions upon trillions of tiny passengers – bacteria. Your body is made up of around ten trillion cells, but you harbour <em>a hundred </em>trillion bacteria. For every gene in your genome, there are 100 bacterial ones. This is your ‘microbiome’ and it has a huge impact on your health, your ability to digest food and more. We, in turn, affect them. Everything from the food we eat to the way we’re born influences the species of bacteria that take up residence in our bodies.</p>
<p>This slideshow is a tour through this “<a href="http://www.nytimes.com/2010/07/20/opinion/20tue4.html?_r=1">universe of us</a>”. Every slide has links to previous pieces that I’ve written on the subject if you want to delve deeper. Or download a podcast of <a href="blogs.discovermagazine.com/notrocketscience/2011/10/19/i-microbes-my-radio-4-talk-on-the-hordes-of-microbes-inside-us/">my Radio 4 programme on these hidden partners</a>.</p>
<p>Image by David Gregory &amp; Debbie Marshall, Wellcome Images</p><p>To our microbiome, the human body must seem like an entire planet, full of different ecosystems. This is especially true for those that <a title="Permanent Link to The bacterial zoo living on your skin" href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/06/23/2009/05/28/the-bacterial-zoo-living-on-your-skin/">live on our skin</a>. At the microscopic scale, the hairy, moist surface of your armpits is as different from the smooth, dry skin of your forearms as a rainforest is to a desert.</p>
<p>In a thorough survey of our skin microbiome, Elizabeth Grice identified species from at least 205 different genera. Your forearm has the richest community with an average of 44 species, while your nostril, ears and inguinal crease (between leg and groin) are the most stable habitats. Grice also found at bacteria from a specific body part have more in common than those from a specific person. Your butt microbes have more in common with mine than they do with your elbow microbes.</p><p>Despite its diversity, the skin microbiome is a tiny country village compared to the <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/06/23/2010/03/03/the-bacterial-zoo-in-your-bowel/">bustling metropolis inside your bowels</a>. The dark corridors of your intestine house more bacteria than any other part of your body. A team of international scientists led by Junjie Qin and Ruiqiang Li discovered that each of our bowels carries at least 160 bacterial species. Together, our collective guts have just under 3.3 million bacterial genes, more than 150 times as many as reside in our own genomes. They also showed that the gut microbiome of a healthy person looks very different to that of someone with a bowel condition like Crohn’s disease or ulcerative colitis.</p>
<p>Despite this diversity, Peer Bork has shown that the gut bacteria of people from Europe, North American and Japan collapse <a href="http://blogs.discovermagazine.com/notrocketscience/2011/04/20/divided-by-language-united-by-gut-bacteria-%e2%80%93-people-have-three-common-gut-types/">into three enterotypes, or gut types</a>. These clusters cut across age, gender, body weight and nationality. Each produces energy in a slightly different way, manufactures a different vitamin and may affect our susceptibility to different diseases.</p>
<p>The quest to understand gut microbes may seem like an arcane niche of science, but it’s actually very important for public health. We rely on these microscopic passengers more than we realise. They harvest energy from our food, provide us with nutrients that would otherwise be denied to us, prevent the growth of harmful bacteria, and more. In many ways, they’re like a forgotten organ. They can also go rogue, changing their community in ways that are linked to obesity or bowel diseases.</p>
<p> </p>
<p>Image by Med. Mic. Sciences Cardiff Uni, Wellcome Images</p><p><a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/06/23/baby%e2%80%99s-first-bacteria-depend-on-route-of-delivery/">We inherit our microbiomes from our mother</a>, picking up billions of them as we slide from her largely bacteria-free womb through her microbe-laden vagina. Being slathered in vaginal microbes might not seem like much of a treat but it’s vital for a newborn.</p>
<p>Babies end up with a very different portfolio of skin and gut bacteria depending on how they are delivered. Those who are born naturally harbour a more diverse array of bacteria, which resemble those in their mother’s vagina, including several species that are important for digestion. Those who are delivered by C-section are colonised by a less diverse array of bacteria, including some like <em>Staphylococcus</em> that are picked up from the hospital environment.</p>
<p>These early differences could directly affect a baby’s health for these first colonisers determine which the species that will follow. The bacterial heirlooms that babies inherit from their mothers might act as a shield, preventing more dangerous microbes like from setting up shop. By changing baby’s first bacteria, C-sections could alter the make-up of their later communities, leading to long-term effects on health and nutrition.</p><p><a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/08/03/you-are-what-you-eat-%e2%80%93-how-your-diet-defines-you-in-trillions-of-ways/">Our microbiome is like a hidden organ</a>, helping us to break down foodstuffs that our own cells cannot cope with. And in turn, our food affects our microbiome. Our first set is laden with genes for digesting milk proteins, allowing us to make full use of our only source of nourishment as babies. Breast milk might even have evolved to nourish the most beneficial bacteria with special sugars.</p>
<p>Just before we move onto solid foods, our microbiome starts activating genes that break down the complex sugars and starches in plants, preparing us for the menu to come. As our diet diversifies, so do our bacteria. They activate genes that use carbohydrates effectively, produce vitamins, and break down unusual and diverse chemicals. As adults, our microbiome becomes relatively stable, but its membership roster depends on the food we eat. The guts of African villagers who eat high-fibre diets are dominated by plant-digesting specialists, which are much rarer in the guts of Europeans who eat high-fat diets.</p><p>Before the age of better food hygiene, our meals used to provide a rich source of foreign bacteria that our microbiome could plunder for genetic tools. Bacteria trade genes as easily as humans trade gifts. For example, the gut bacteria of Japanese people have borrowed genes from a marine species, which now <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/04/07/gut-bacteria-in-japanese-people-borrowed-sushi-digesting-genes-from-ocean-bacteria/">allows them to digest the special carbohydrates in seaweed</a>. The marine bacterium eats seaweed, including the types that are used to make nori, a common sushi ingredient.  In the past, when diners wolfed down morsels of nori, some also swallowed seaweed-eating bacteria, which traded genes with those in their own guts.</p>
<p>This wouldn’t happen nowadays because nori is roasted before being eaten. In fact, processing food presents a blockade to bacteria from the outside world and as a result, Western gut communities have become gentrified. They lack genetic diversity, and they have few ways of increasing it.</p>
<p>Images by Alice Wiegand, Alex Kovach, Tristan Barbeyron and Mirjam Czjzek</p><p>The microbiome is more than just our partners-in-digestion – they affect our health too. They have been linked to a variety of medical conditions, including allergies, immune diseases, and even obesity. For example, the balance of the two major groups – the Bacteroidetes and Firmicutes – <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/06/23/2008/10/06/human-gut-bacteria-linked-to-obesity/">could influence our body weight</a>.</p>
<p>Fat mice and humans have a less diverse milieu of gut bacteria, with a <a href="http://blogs.discovermagazine.com/notrocketscience//notrocketscience/2008/12/01/gut-bacteria-fat-or-thin-family-or-friends-shared-or-unique/">greater proportion of Firmicutes to Bacteroidetes in their bowels</a>. This ratio increases if we eat high-fat diets and falls if we eat low-fat diets. And if the gut bacteria from fat mice are transplanted into mice with no gut bacteria of their own, they can make the new hosts overeat and pile on the pounds. This research suggests that gut bacteria could be manipulating us for their own ends. Some species send out signals that make us hungrier, encourage us to eat more, and affect the way we store fat. And some of our immune genes help to moderate these signals.</p>
<p>As we learn more about our bacterial partners, we might eventually find ways of influencing them to improve our health. This is already happening. In 2008, Alexander Khoruts from the University of Minnesota managed to cure a woman with a “vicious gut infection” by giving her <a href="http://www.nytimes.com/2010/07/13/science/13micro.html?_r=2&amp;pagewanted=1">a transplant of her husband’s gut bacteria</a>.</p><p>What happens in the gut doesn’t stay in the gut – it sometimes affects the brain. Animal studies have started to show that the microbiome, from its staging ground in the bowel, can influence the development of its host’s brain.</p>
<p>Rochellys Diaz Heijtz found that <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2011/01/31/gut-bacteria-steer-the-development-of-the-young-brain/">germ-free mice, without any microbiome</a>, were more active, less anxious and less risk-averse than usual. Their brains differed in the activity of over a hundred genes that provide cells with energy, influence chemical communications in the brain and strengthen the connection between nerve cells. Heijtz could even shift her germ-free mice towards “normal” behaviour and genetic activity by giving them a microbiome transplant, but this only worked early in their lives.</p>
<p>But later,  Javier Bravo  at University College Cork managed to<a href="http://blogs.discovermagazine.com/notrocketscience/2011/08/29/from-guts-to-brains-%e2%80%93-eating-probiotic-bacteria-changes-behaviour-in-mice/"> change the behaviour of normal adult mice</a> by feeding them with a probiotic bacterium  called <span id="apture_prvw1" class="aptureLink"><span class="aptureLinkIcon" style="background-position: right -1348px;"> </span><span class="aptureLink snap_noshots"><em>Lactobacillus rhamnosus</em></span></span>,  often found in yoghurts and dairy products. The bacterial menu changed  the levels of signalling chemicals in the rodents’ brains, and reduced  behaviours associated with stress, anxiety and depression.</p>
<p>Meanwhile, Gil Sharon found that <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/11/01/gut-bacteria-change-the-sexual-preferences-of-fruit-flies/">gut bacteria can shape the sexual choices of flies</a>. Flies that are raised on diets of starch prefer to mate with other “starch flies” while those raised on maltose prefer “maltose flies”. When Sharon dosed the flies with antibiotics, she killed both their gut bacteria <em>and </em>their sexual preferences. If she inoculated the sterile flies with the microbiome of their peers, their preferences reappeared instantly. It’s possible that the bacteria influence the levels of sex pheromones that affect the fly’s attractiveness.</p>
<p>These studies show that you can’t understand an animal’s evolution simply by considering the evolutionary pressures that act on its genome. You also have to consider the genes of the bacteria and other passengers that live inside it. We’re each like a superorganism – a unified alliance between the genes of several different species, only one of which is human.</p>The teeming masses of the microbiome also contain a record of our evolutionary past. Howard Ochman found that the <a href="http://blogs.discovermagazine.com/notrocketscience/notrocketscience/2010/11/16/gut-bacteria-recap-the-evolution-of-apes/">evolution of the gut microbes in great apes</a> perfectly recaps that of their host. The bacteria from the two species of gorilla are more closely related to each other than they are to human gut bacteria. Geography, diet and disease aside, the main thing that influences the members of these bacterial cities is the species of the host. You could reconstruct the evolution of the apes, simply by comparing the bacteria in their bowels.<p>The bacteria of our microbiome are mostly our allies. <a href="http://blogs.discovermagazine.com/notrocketscience/2011/10/13/beneficial-gut-bacteria-can-become-virus-collaborators/">But they can also they can be turned against us.</a> Two new studies in mice have found  that viruses - including one that causes polio, and another that causes cancer - can exploit gut bacteria to infect our bodies.</p>
<p>They use molecules on the bacteria's surfaces as reins, to ride towards host cells, or backstage passes to sneak past the immune system. Our microscopic allies can turn into  unwitting collaborators for dangerous infections.</p>
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November 16th, 2010 by Ed Yong in Animals, Bacteria, Chimps and other apes, Evolution, Human evolution, Mammals, Microbiome | 9 comments | RSS feed | Trackback >

9 Responses to “Gut bacteria recap the evolution of apes”

  1. 1.   Nathan Myers Says:
    November 17th, 2010 at 1:41 am

    “Gut bugs” might be a better choice of term than “gut bacteria”.

    This is a really interesting report. Now we need to understand how each species succeeds in favoring its characteristic flora and keeping the rest out.

  2. 2.   Guy Plunkett Says:
    November 17th, 2010 at 9:24 am

    Fascinating.

    RE: “I use ‘bacteria’ in this story as an unfortunate shorthand.” This is why retaining the term “prokaryotes” is useful; we often need a shorthand for “archaea and/or bacteria.”

  3. 3.   Ed Yong Says:
    November 17th, 2010 at 12:06 pm

    @Guy – But prokaryotes is completely useless when talking to a general audience, which is the level I’m aiming at. Try asking how many people on the street know what it means.

  4. 4.   Shade Says:
    November 18th, 2010 at 7:47 am

    Just make the word a link to wikipedia or other site, and if they can’t be bothered to read what a prokaryote is that is their loss.

  5. 5.   Ed Yong Says:
    November 18th, 2010 at 8:11 am

    Are you being serious? While I’m at it, why bother writing papers up at all? I could just put the entire text up and then put links from any technical term across to the relevant Wikipedia page. I could probably write a script to do that for me and get some sleep.

  6. 6.   natselrox Says:
    November 18th, 2010 at 8:23 am

    Great writeup as usual, Ed!

    I posted this story on the RatSkep forum and Calilasseia pointed out a research about a similar study with regards to lice and how the lice in humans, chimps and gorillas mirror the phylogenetic tree of hominids. For those interested, the article can be read here: http://www.rationalskepticism.org/evolution/evolution-of-hominids-mirrored-by-gut-microbiota-t15973.html#p582411

  7. 7.   Matt Shipman Says:
    November 18th, 2010 at 9:06 am

    Nice write-up Ed. And I back your decision not to use the term prokaryote — unless you want to spend a paragraph defining it for the lay audience (which is the audience for this blog). After all, what you’re writing is “Not Exactly Rocket Science.” I also agree that linking to Wikipedia would be hazardous at best, given the unpredictable nature of its entries. Cheers!

  8. 8.   Ed Yong Says:
    November 18th, 2010 at 9:16 am

    @ Matt – Thanks. And of course, I have used the term prokaryote before on this blog – twice – but only when the story absolutely required it and only after careful definition.

    This is all Writing 101 stuff. If you make your audience do extra work to understand what you’ve written and that audience goes somewhere else, it’s not because they’re lazy, it’s because you’re a rubbish communicator.

    @Natselrox – Awesome link. Thanks for that.

  9. 9.   Matt Shipman Says:
    November 18th, 2010 at 1:53 pm

    Sums it up perfectly: “If [your] audience goes somewhere else, it’s not because they’re lazy, it’s because you’re a rubbish communicator.”

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