Sea lettuce that washed upon the shore of Maryland.

Charles Darwin described life as an eternal struggle for existence. Species compete for a limited amount of space and resources, so only those varieties that are best adapted to their niche will survive. The logic behind this reasoning is sound, yet it doesn't apply to microbes living on sea lettuce. This humble seaweed picks bacteria on a basis of first-come, first-served, no competition involved. Not the fittest, but the luckiest shall survive.

That's what Catherine Burke and her colleagues conclude after studying the microbial ecosystems that live on the leaves of sea lettuces from intertidal pools. The team extracted and sequenced the DNA of these microbes directly, without first culturing them in the lab. Such a genetic census, the method is called metagenomics, presumably gives an unbiased reflection of all the microbes that live in a certain environment.

After matching the DNA sequences to species, Burke found that each lettuce harbours a unique community of microbes. Between the six algal samples, only 15% of the microbial species were shared. This suggests that microbes colonize sea lettuce more or less randomly. It doesn't matter who these bacteria are. As long as they can grow on sea lettuce and get there soon enough, they will become part of the lettuce's microbial ecosystem. Ecologists recognize this scenario as the lottery model: whichever species arrives first, wins the lottery.

This lottery hypothesis was first proposed by Peter Sale in 1976. Sale didn't have microbes and sea lettuce in mind when he described his theory, but fish and coral reefs. Given two similar species of fish and a vacant reef, the species that colonizes the coral reef first will be able to defend it against further intruders. Philip Munday later provided experimental evidence for this lottery effect. He showed that when a reef fish colonized a reef with a head start of 8 hours, a competing species couldn't displace the resident later. When both fish were introduced together, each species won half of the times.

Gobiodon histrio, or the Green coral goby, was one of the species used in the lottery study by Munday.

A lottery can only be fair and random if each species has a similar chance of winning. This is only possible if competing species resemble each other. For animals this is almost synonymous to being closely related, such as the gobies that Munday used in his experiments. When two animals are only distantly related, one will always have an advantage over the other, by virtue of being bigger, smarter or sneakier. But relatedness isn't really an issue for bacteria. They can share genes across species boundaries with relative ease, after all.

Although the sea lettuce lottery was won by different bacteria every time, Burke discovered that each microbial community has a similar core set of genes that differed from the genes that were present in the surrounding sea water. An impressive 70% of the genes in the different communities have similar functions. Many of these genes make community life on a mass of floating algae possible. Take the genes that produce adhesion proteins. These proteins make microbes stick to surfaces and each other, forming biofilms. Other examples include proteins that convert the sugars that algae produce, or genes that make bacteria switch from a mobile to a sessile lifestyle.

This conservation of genes across different communities could mean that there are only so many ways of colonizing see lettuce. The genes are like lottery tickets that many different bacteria buy to enter the sweepstakes. The species that win the lottery might be random, but their genes are not.

These insights mirror findings elsewhere. Earlier this year, researchers from Heidelberg discovered that each person has one of three different types of bacterial ecosystems in their gut. These ecosystems didn't correlate with the diet, sex, weight, age or health of their test subjects. For all we know, they could arise from random colonizations of microbes when we are young, just like the microbes that live on sea lettuce.

Metagenomics is a young field, but it has already revealed many hidden aspects of microbial community life. Teasing apart the random and non-random forces that shape these communities should keep microbial ecologists busy for years to come.


Images:

Sea lettuce by Eutrophication&hypoxia.

Green coral goby by WonderKris.

References:

C Burke, P Steinberg, D Rusch, S Kjelleberg, & T Thomas (2011). Bacterial community assembly based on functional genes rather than species Proceedings of the National Academy of Sciences : doi/10.1073/pnas.1101591108

Munday, P. (2004). Competetive coexistence of coral-dwelling fishes: the lottery hypothesis revisited Ecology, 85 (3), 623-628 DOI: 10.1890/03-3100