Gut bacteria in Japanese people borrowed sushi-digesting genes from ocean bacteria

View Images

Japanese people have special tools that let them get more out of eating sushi than Americans can. They are probably raised with these utensils from an early age and each person wields millions of them. By now, you’ve probably worked out that I’m not talking about chopsticks.

The tools in question are genes that can break down some of the complex carbohydrate molecules in seaweed, one of the main ingredients in sushi. The genes are wielded by the hordes of bacteria lurking in the guts of every Japanese person, but not by those in American intestines. And most amazingly of all, this genetic cutlery set is a loan. Some gut bacteria have borrowed their seaweed-digesting genes from other microbes living in the coastal oceans. This is the story of how these genes emigrated from the sea into the bowels of Japanese people.

Within each of our bowels, there are around a hundred trillion microbesa hundred trillion microbesa hundred trillion microbes, whose cells outnumber our own by ten to one. This ‘gut microbiome’ acts like an extra organ, helping us to digest molecules in our food that we couldn’t break down ourselves. These include the large carbohydrate molecules found in the plants we eat. But marine algae – seaweeds – contain special sulphur-rich carbohydrates that aren’t found on land. Breaking these down is a tough challenge for our partners-in-digestion. The genes and enzymes that they normally use aren’t up to the task.

Fortunately, bacteria aren’t just limited to the genes that they inherit from their ancestors. Individuals can swap genes as easily as we humans trade money or gifts. This ‘horizontal gene transfer’ means that bacteria have an entire kingdom of genes, ripe for the borrowing. All they need to do is sidle up to the right donor. And in the world’s oceans, one such donor exists – a seagoing bacterium called Zobellia galactanivorans.

Zobellia is a seaweed-eater. It lives on, and digests, several species including those used to make nori. Nori is an extremely common ingredient in Japanese cuisine, used to garnish dishes and wrap sushi. And when hungry diners wolfed down morsels of these algae, some of them also swallowed marine bacteria. Suddenly, this exotic species was thrust among our own gut residents. As the unlikely partners mingled, they traded genes, including those that allow them to break down the carbohydrates of their marine meals. The gut bacteria suddenly gained the ability to exploit an extra source of energy and those that retained their genetic loans prospered.

This incredible genetic voyage from sea to land was charted by Jan-Hendrik Hehemann from the University of Victoria. Hehemann was originally on the hunt for genes that could help bacteria to digest the unique carbohydrates of seaweed, such as porphyran. He had no idea where this quest would eventually lead. Mirjam Czjzek, one of the study leaders, said, “The link to the Japanese human gut bacteria was just a very lucky, opportunistic hit that we clearly had no idea about before starting our project. Like so often in science, chance is a good collaborative fellow!”

From oceans to bowels

Hehemann began with Zobellia, whose genome had been recently sequenced. This bacterium turned out to be the proud owner of no fewer than five porphyran-breaking enzymes. These enzymes were entirely new to science, they are all closely related and they clearly originated in marine bacteria. Their unique ability earned them the name of ‘porphyranases’ and the genes that encode them were named PorA, PorB, PorC and so on.

They are clearly not alone. Using his quintet as a guide, Hehemann found six more genes with similar abilities. Five of them hailed from the genomes of other marine bacteria – that was hardly surprising. But the sixth source was a far bigger shock: the human gut bacterium Bacteroides plebeius. What was an oceanic gene doing in such an unlikely species? Previous studies provided a massive clue. Until then, six strains of B.plebeius had been discovered, and all of them came from the bowels of Japanese people.

Nori is, by far, the most likely source of bacteria with porphyran-digesting genes. It’s the only food that humans eat that contains any porphyrans and until recently, Japanese chefs didn’t cook nori before eating it. Any bacteria that lingered on the green fronds weren’t killed before they could mingle with gut bacteria like B.plebius. Ruth LeyRuth LeyRuth Ley, who works on microbiomes, says, “People have been saying that gut microbes can pick up genes from environmental microbes but it’s never been demonstrated as beautifully as in this paper.”

In fact, B.plebeius seems to have a habit of scrounging genes from marine bacteria. Its genome is rife with genes that are more closely related to their counterparts in marine species like Zobellia than to those in other gut microbes. All of these borrowed genes do the same thing – they break down the complex carbohydrates of marine algae.

To see whether this was a common event, Hehemann screened the gut bacteria of 13 Japanese volunteers for signs of porphyranases. These “gut metagenomes” yielded at least seven potential enzymes that fitted the bill, along with six others from another group with a similar role. On the other hand, Hehemann couldn’t find a single such gene among 18 North Americans. “We were trying at lunch to think about where you might see patterns this clean,” says Ley. “You’d have to find another group of people with a very specialised diet.  Because this involved seaweed and marine bacteria, it might be one of the cleanest demonstrations you’d get.”

For now, it’s not clear how long these marine genes have been living inside the bowels of the Japanese. People might only gain the genes after eating lots and lots of sushi but Hehemann has some evidence that they could be passed down from parent to child. One of the people he studied was an unweaned baby girl, who had clearly never eaten a mouthful of sushi in her life. And yet, her gut bacteria had a porphyranase gene, just as her mother’s did. We already known that mums can pass on their microbiomes to their children, so if mummy’s gut bacteria can break down seaweed carbs, then baby’s bugs should also be able to.

Are we what we eat?

This study is just the beginning. Throughout our history, our diet has changed substantially and every mouthful of new food could have acted as a genetic tasting platter for our gut bacteria to sample. Personally, I’ve been eating sushi for around two years ago and I was intrigued to know if my own intestinal buddies have gained incredible new powers since then. Sadly, Czjzek dispelled my illusions. “Today, sushi is prepared with roasted nori and the chance of making contact with marine bacteria is low,” she said. The project’s other leader, Gurvan Michel, concurs. He notes that of all the gut bacteria from the Japanese volunteers, only B.plebeius as acquired the porphyranase enzymes. “This horizontal gene transfer remains a rare event,” he says.

Michel also says that for these genes to become permanent fixtures of the B.plebeius repertoire, the bacterium would have needed a strong evolutionary pressure to keep them. “Daily access to ingested seaweeds as a carbon source” would have provided such a pressure. My weekly nibbles on highly sterile pieces of sushi probably wouldn’t.

That’s one question down; there are many to go. How did the advent of agriculture or cooking affect this genetic bonanza? How is the Western style of hyper-hygienic, processed and mass-produced food doing so now? As different styles of cuisines spread all over the globe, will our bacterial passengers also become more genetically uniform?

The only way to get more answers is to accelerate our efforts to sequence different gut microbiomes. Let’s take a look at those of other human populations, including hunter-gatherers. Let’s peer into fossilised or mummified stool samples left behind by our ancestors. Let’s look inside the intestines of our closest relatives, the great apes. These investigations will tell us more about the intestinal genetic trade that has surely played a big role in our evolution.

Rob Knight, a microbiome researcher from the University of Colorado, agrees. “This result reinforces the need to conduct a broad and culturally diverse survey of who harbours what microbes. The key to understanding obesity or IBD might well be in genes or microbes acquired under circumstances very different to those we experience in Western society.” Gastronomics, anyone?

Reference: Hehemann, J., Correc, G., Barbeyron, T., Helbert, W., Czjzek, M., & Michel, G. (2010). Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota Nature, 464 (7290), 908-912 DOI: 10.1038/nature08937

Images: nori by Alice Wiegand; sushi chef by Alex Kovach; Zobellia by Tristan Barbeyron; seaweed by Mirjam Czjzek

More on microbiomes:

More on horizontal gene transfer: