Neuroanthropology

For a greater understanding of the encultured brain and body…

What’s in your gut? Termites, for example

Posted by gregdowney on August 4, 2010

Science News has a fascinating short story, Gut bacteria reflect dietary differences, by Gwyneth Dickey, that highlights one of the ecological dimensions of ‘enculturation’ that I think some symbolic models of culture have a hard time grasping. It turns out that a Western diet produces a less-varied gut ecology in Italian children than was found in African children. Moreover, the old adage ‘you are what you eat’ could apply in a particularly interesting way to those who eat termites.

The original article, Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe (urban Florence) and rural Africa (Boulkiemde province, Burkina Faso), by Carlotta De Filippo and colleagues, is open access on the Proceedings of the National Academy of Sciences website, so you should definitely surf over there if you find this interesting.

De Filippo and colleagues discuss the microbiome, the ‘complex consortium of trillions of microbes, whose collective genomes contain at least 100 times as many genes as our own eukaryote genome’ (see also Gill et al. 2006). This enormous, varied ecosystem in the gut, a symbiotic community, supplements human metabolic capabilities, provides a first line of defense against pathogens, modulates gastrointestinal development and even informs the configuration of the immune system (paraphrased from De Filippo et al. 2010).

Different gut ecologies brought about both by environmental factors and by food production techniques, dietary preferences, and even food handling practices are one way that human groups might inadvertently induce biological variation in our species, a subtle culture-biology link through the populations in our gastrointestinal tracts. Now De Filippo and colleagues has gone out and actually demonstrated this variation empirically, using high-throughput 16S rDNA sequencing and biochemical analyses of fecal microbiota.


What’s on YOUR plate?

In Burkina Faso, children’s diets after weening were ‘low in fat and animal protein and rich in starch, fiber, and plant polysaccharides, and predominantly vegetarian.’ Diet was primarily composed of cereals (millet grain, sorghum), legumes (black-eyed peas), and vegetables, providing ample amounts of nonanimal protein, carbohydrate and dietary fibre (children in Burkina Faso were getting more than three times the fibre eaten by the comparative population from Italy).

The children in Burkina Faso got very little animal protein, primarily a bit of chicken from time to time and, during the rainy season, termites (also interesting because of their role in chimpanzee diets, but we’ll be back to the termites because they’re the punchline of the article).

In contrast, the Italian children, after being weaned at an earlier age, on average, were taking in a diet much higher in animal protein, sugar, starch, and fat, with lower fiber (in part due to greater food processing) and much greater energy.

Startlingly, the children, 2- to 6-years-old, in Burkina Faso got 996 kcal/day compared to the Italian children who were eating 1,512.7 kcal/day; even prior to the age of 2, children in Italy were taking in an average of 60% more calories than Italian children! (This also harkens back to our discussion of what makes WEIRD populations truly odd.)

The community inside them

The faecal samples from children in Burkina Faso especially differed from the Italian subjects because of the presence of Prevotella, Xylanibacter (Bacteroidetes), Treponema (Spirochaetes), and Butyrivibrio; all appeared in the African samples but were not found in the Italian. The researchers hypothesize that these distinctive bacterial genera might help to extract energy from the polysaccharides in the children’s heavier fiber diet. Theses bacteria are capable of fermenting cellulose and xylan through a number of carbohydrate-active enzymes, producing anti-inflammatory effects at the same time.

From the Science News article by Dickey:

Children from Burkina Faso, who ate millet grain, sorghum wheat, legumes and vegetables, had high numbers of bacteria that digest plant fibers. Also found in the guts of termites, these bacteria break down fibers that humans typically can’t. The bacteria make short-chain fatty acids that give people energy and protect them from inflammatory gut diseases such as Crohn’s disease and inflammatory bowel disorder.

Burkina Faso’s children also had decreased numbers of diarrhea-causing bacteria compared with children from Italy. That finding surprised the team, because the African children often drank water polluted with such bacteria.

The diminished diversity of microbiota in the human gut is especially interesting because some theorists have pointed to this dietary-provoked transformation, together with increasing hygiene and anti-bacterial technologies in human environments, as possible contributors to an upsurge in rates of allergies, auto-immune disorders and inflammatory bowel diseases (see, for example, Strachan 1989). Recent research has suggested a relationship between ecological imbalances in gut microbiota and obesity, and inflammatory conditions in the bowel have been directly linked to changes in gut microflora. For example, bacterial species correlated with a high-fat, high-sugar diet promote obesity in gnotobiotic mice (Turnbaugh et al. 2009). In other words, the diet can have a twin-pronged attack on our ability to maintain low body weight, as it provides both higher calories as well as a shift in microbiota to a population that promotes obesity.

The team led by De Filippo compared the diversity of microbial life in the fecal samples from both locations, finding that the African samples, by several measures, had greater diversity and richness of symbiotic life.

Exposure to the large variety of environmental microbes associated with a high-fiber diet could increase the potentially beneficial bacterial genomes, enriching the microbiome. Reduction in microbial richness is possibly one of the undesirable effects of globalization and of eating generic, nutrient-rich, uncontaminated foods. Both in the Western world and in developing countries diets rich in fat, protein, and sugar, together with reduced intake of unabsorbable fibers, are associated with a rapid increase in the incidence of noninfectious intestinal diseases. The potential protective effects of the diet on bowel disorders was first described by Burkitt [1973] who, working in Africa in the 1960s, noticed the remarkable absence of non-infectious colonic diseases in Africans consuming a traditional diet rich in fiber.

The fact that the youngest children in both populations had similar microbial profiles in their GI system suggests that diet primarily is effecting the difference between the two populations; while both groups are still breastfeeding, they are more similar, only diverging later when they start to eat their distinctive cultural diets.

Horizontal transfer of microbial life

The short piece in Science News makes clearer, in my admittedly non-specialist reading, an interesting little wrinkle in the story of diet affecting gut microbiota: the horizontal transfer of microbes from our food to our own guts. As Gwyneth Dickey writes:

A termite a day may keep the doctor away. African children who eat a high-fiber diet (and the occasional wood-digesting insect) have gut bacteria that help them digest plant fibers and protect them from diarrhea and inflammatory disease, a new study finds.

What I’m struck by here, and I’m not sure if this is Dickey’s interpretation or something one of the researchers said, is the suggestion that some of the microbes most able to turn whole grains into short chain fatty acids might be colonizing the large intestines of children in Burkina Faso through the rainy season practice of dining upon termites! (She quotes co-author Duccio Cavalieri warning, ‘We’re not saying you should eat termites,’ but it’s unclear where the original suggestion might have come from – Dickey or the research team.) I have absolutely no idea if this is actually possible, but there is the case of microbes being transferred from food to Japanese individuals who dine on some forms of algae (see Hehemann et al. 2010).

The more I think about this possibility – that we might pick up symbiotic microfauna by eating the guts of other animals – the more I find it both weirdly fantastic and simultaneously plausible. After all, what living organism is more likely to survive the digestion process to colonize the human gut than a microbe that’s already adapted to the gastro-intestinal tract of another animal?

But if it’s happening, we have a case where children are picking up microbes that will live in their guts and help them to digest dense fibrous foods by eating termites. What could be a better example of a kind of dietary ‘contagious magic’ than eating an animal and gaining some of its distinctive powers of digestion?! Eating termites might make it possible for your body to digest ‘woody’ food sources.

Further reading:

It’s not the gut, but I’ve written about the microbial life on the skin back in The human ‘super-organism’.

Image:
Gut population cartoon originally from Yakult.

References:

Burkitt, D. P. 1973. Epidemiology of large bowel disease: The role of fibre. Proceedings of the Nutrition Society 32:145–149. doi:10.1079/PNS19730032

De Filippo, Carlotta, Duccio Cavalieria, Monica Di Paolab, Matteo Ramazzottic, Jean Baptiste Poulletd, Sebastien Massartd, Silvia Collinib, Giuseppe Pieraccini, and Paolo Lionetti. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proceedings of the National Academy of Sciences. Published online August 2, 2010. doi: 10.1073/pnas.1005963107.

Gill, Steven R., Mihai Pop, Robert T. DeBoy, Paul B. Eckburg, Peter J. Turnbaugh, Buck S. Samuel, Jeffrey I. Gordon, David A. Relman, Claire M. Fraser-Liggett, and Karen E. Nelson. 2006. Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359. doi: 10.1126/science.1124234

Hehemann, J. H., G. Correc, T. Barbeyron, W. Helbert, M. Czjzek, and G. Michel. 2010. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464:908–912. doi:10.1038/nature08937

Strachan, David P. 1989. Hay fever, hygiene, and household size. British Medical Journal 299:1259–1260. doi:10.1136/bmj.299.6710.1259

Turnbaugh, Peter J., Vanessa K. Ridaura, Jeremiah J. Faith, Federico E. Rey, Rob Knight and Jeffrey I. Gordon. 2009. The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Science Translation Medicine 1:6ra14. doi: 10.1126/scitranslmed.3000322

8 Responses to “What’s in your gut? Termites, for example”

  1. Adam said

    Not too surprising to me – it’s why people take probiotic pills (especially after antibacterial regimens) and eat yogurt, among other probiotic foods. I’m not sure I’m ready to start chowing on termites, but it’d probably be more efficient than coming up with a way to culture these biota for WEIRD-comfortable consumption.

    • Adam said

      Also, I wonder if there could be any connection here to folks who have problems with gluten… I don’t know enough, but have friends with allergies or Celiacs and it popped into my head.

  2. Well, with the termite thing… the majority of cellulose digestion in wood-eating termites is done by various highly specialised protists (Google “Trichonympha”, “Streblomastix” and “Trichomitopsis” for some truly awesome organisms…); treatments with anti-bacterial drugs do not inhibit cellulose digestion in termites (in the short term), though the removal of the eukaryotic endosymbionts does. So if eating termites were at all potentially beneficial by transferring microbiota between the guts, it would be the protists, and not the prokaryotes, that would do much of the work.

    Now, the termite protists turn out to be exceptionally fragile outside their host. A major problem is that oxygen simply kills them (we can keep them going for a few hours in special media, but early death is inevitable). Of course. the human gut is quite low in oxygen, and may well be suitable for the protists in that regard. However, the other aspects of the human gut (eg. acidity, enzymatic composition) differs substantially from that of the termite, and it is quite unlikely the protists would survive in conditions so different from the environment they have specialised for. One could perhaps test that by attempting to grow the protists in a medium simulating the human gut, but until then, one can’t really believe much in that theory.

    So while it’s a cool idea and not entirely impossible, in the particular case of termites it seems rather unlikely. Disregarding the protistology aspect, it doesn’t seem like anything besides an observed correlation (of that) is offered in support of this theory; a much simpler and more plausible alternative is that a high-cellulose diet provides an environment wherein a stray cellulose-digesting bacterium can survive and take hold, unlike a lower-cellulose gut. The bacteria coming through may well be the same in both cases. One must test whether a specialised diet is *necessary* for a higher level of such bacteria, or whether a high-cellulose diet would simply suffice.

    And this is why one should know basic protistology ;-) Sadly, even many fellow biologists don’t know we exist…

    • gregdowney said

      Thanks, Psi!

      Caught out be a lack of basic protistology knowledge (including not even knowing until your email what protistology is)! I was surprised to read the suggestion that termites might be donating digestive microbes to African kids in the press release, but it was too juicy to pass up on.

      I’m sure you’re right – the termite hypothesis is not terribly plausible. The simple presence of a lot of fibre in gut ecology more likely would allow an opportunistic cellulose-loving microbial strain to gain a gastro-intestinal foot-hold (or whatever bacteria use to get a hold). Unless someone knows of a pretty versatile protist, one that could feel comfortable in a human gut, termite donation will have to remain a stretch for an explanation.

      Thanks for the information though. Like so many of these press releases based on research papers, some of the stuff that’s the most fun isn’t really in the paper and turns out to be pushing the envelope of credulity.

  3. MTBradley said

    The fact that I am an allergy sufferer who has been in Burkina Faso for the past month doesn’t make up for my below grade level knowledge of statistics, but after having a look at the piece I have one cavil and one non-trivial critique. The cavil is that Boulpon has a population of over 4,000 and is about an hour’s drive from a city of 1.5 million so using it as an analog for early Neolithic settlements comes across as a little forced to me. Less trivial is the portrayal of the subjects’ diet as being high in fiber. Toh does contain millet but in the urban areas where I have been based here it also contains a lot of processed corn meal. I gave a quick look to the study’s dataset and it didn’t really seem to indicate that the authors had done any observation, measurement, or analysis of food ingredients and/or prepared food. I rather got the impression that they did some minimal observation and documentation (or possibly just relied on previous studies) of diet and extrapolated the nutrient contents from that. So I would say that the results are interesting and suggestive but I would like to be sure that the team was as rigorous with what was going in as with what was coming out.

    Again, I just skimmed the article so anyone who has picked through the article closely is encouraged to correct anything I got wrong here.

    • Microbiota2010 said

      @MTBradley, The Boulpon village is located in the Bulkiandè province and it’s not a village of 4,000 people as is well documented by photos of article (around 100 peolple; Figure 1). The fact that the village is 80 km from the capital does not justify the impossibility of a lifestyle similar to the Neolithic. The village was chosen for these characteristics of life and diet that are very close to those of humans in the Neolithic era. As the commentator is doubtful since it has never been in the village? The diet has been carefully analyzed as described in the supplementary materials that might MTBradley not consulted. It ‘was conducted by a dietary questionnaire pediatricians Italian international cooperation that are present in the region in question. Each mother was interviewed in relation to their child’s diet. Same thing has been conducted on the Italian population. The Tô is not totally prepared with refined maize meal as happens in cities. Everything is locally produced and worked on large stone plans to produce flour of millet and sorghum that will be used to prepare Tô o (Flour in Figure 1). Everything is thoroughly described in the paper and supplementary materials. The nutritional values were calculated based on the FAO tables as shown in the paper (additional material). The data are not based on superficial observation, nor any other work of other authors. Then I suggest reading the paper in detail if you want to criticize the details. C. De Filippo

      • MTBradley said

        “an in-depth interview on BF children’s diet was obtained directly from their mothers” (p. 5 of 6)

        If the claim is that the collection of retrospective data is an adequate proxy for the observation of behavior I know someone who would like to have a word with you. Were the interviews conducted in French? or More? via translators? etc.

        The Boulpon village is located in the Bulkiandè province and it’s not a village of 4,000 people as is well documented by photos of article (around 100 peolple; Figure 1).

        But I have consulted a source which contradicts yours. After spending a month in Burkina Faso’s second largest city and having gained a knowledge of how woeful the infrastructure for travelers in the country is even there I can’t help but see a few red flags. If I wanted a field site over which I could claim ethnographic authority with little chance that anyone would appear to check up on my results a small settlement in the DPRK would be my first choice. A small settlement in Burkina Faso would be my second.

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