Soybean root nodules. Credit: USDA
Soybean root nodules. Credit: USDA

With Evolutionary Rocket Fuel, Bacteria Give Peas a Chance

Imagine that I could implant all the world’s medical knowledge into your head. You blink, and you instantly know every bit of anatomy, every surgical procedure, and every diagnostic criterion for every disease. You land a job in a hospital. And you suck. Despite your newfound skills, you still have no idea how hospitals work, how to talk to patients, or how to cooperate with your fellow doctors. Ill-suited and out-of-place, you quit.

The lesson behind this little vignette is that it takes social skills, as well as technical savvy, to succeed in a new job. And that’s a guideline that bacteria duly follow.

If you look at the roots of legumes, like peas or beans, you’ll find small swollen nodules. Each one contains billions of bacteria that live nowhere else. They earn their keep by ‘fixing’ nitrogen. That is, they convert it into ammonia, which can then be used to make amino acids, DNA and other essential molecules. The plants depend on this process, and the bacteria depend on the plants. It’s a classic case of symbiosis.

These root bacteria are called rhizobia. They come from at least 13 different lineages, which are typically full of species that digest dead plants or infect living ones. But from these groups of undertakers and disease-makers, several members have repeatedly and independently evolved into plant partners. They did it by picking up large packages of genes from other microbes that had already colonised roots. These “horizontal gene transfers” are everyday events for bacteria, allowing them to instantly pick up new skills without having to evolve them from scratch.

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In this case, the packages contain genes for colonising plant roots, creating nodules to live in, and fixing nitrogen—everything an unassuming soil bacterium would theoretically need to become a plant collaborator.

Scientists know this happened in the wild because they can trace the history of the same symbiosis genes as they jump form one bacterial group to another. But this process is hard to duplicate in the lab. Bacteria that receive the packages don’t immediately become productive partners. They still need to adapt to their hosts. They’re like the hypothetical person from the start of this piece—armed with all the right know-how, but incapable of fitting in.

Philippe Remigi and colleagues from the Laboratory of Plant-Microorganism Interactions in France have discovered how the microbes seal the deal. Their symbiosis packages also contain genes that trigger a temporary flurry of new mutations in a recipient’s genome. These genes are adaption accelerants—a kind of evolutionary rocket fuel that microbes can pass to one another. They allow bacteria, now suddenly armed with the tools for symbiosis, to quickly adapt to life with a plant.

Bacteria often pick up simple skills by trading genes, such as resistance to antibiotics or the ability to cause infections. Here, they’re picking up evolvability.

The team, led by Catherine Masson-Boivin, began this line of research began in 2010. They transferred a cluster of symbiosis genes from a bacterium that lives on the touch-me-not plant into Ralstonia solanacearum, a soil microbe that causes a wilting disease. Ralstonia didn’t become a symbiont straight away, but quickly evolved into one when placed on touch-me-nots. Some strains picked up mutations that disabled their virulence genes. They stopped causing disease, and started forming nodules and fixing nitrogen instead. Over 400 generations—no time at all for a bacterium—they became dramatically better partners.

When the team sequenced the genomes of these newly minted symbionts, they found an astonishing number of mutations—more than would usually have appeared in that amount of time. The cause of these mutations lay within the symbiosis cluster itself. It contained three genes called ImuABC, which the team hadn’t noticed before. Two of these create enzymes that copy DNA, but in a very sloppy way. They make errors as they work, introducing mutations into the genomes that they create. The team found that the ImuABC cluster increases Ralstonia’s mutation rate by 15 times. And strains with this cluster transformed into root symbionts much faster than those without it.

ImuABC is only activated under stressful competitions, and an unfamiliar environment like a plant root certainly counts. When Ralstonia first landed on the touch-me-nots, ImuABC sprang into action, triggering a temporary burst of new mutations. Some of these knocked out disease-causing genes, allowing Ralstonia to colonise the plants in more beneficial ways. The other symbiosis genes equipped Ralstonia with the technical skills it needed in its new job, but ImuABC gave it the social skills it needed to get on with its new partner.

ImuABC is widespread among bacteria, but root symbionts are far more likely to have it on a plasmid—a free-floating ring of DNA that can be easily transferred from one cell to another. In some of these microbes, ImuABC has started to degenerate. It’s possible that after facilitating the early handshakes of the plant-microbe relationship, these genes were no longer needed, and are gradually being lost.

Time and again, microbes have formed alliances with plants, animals, and other organisms (I’m writing a book about this, coming out in 2016). They hide squid with light, they supplement the diets of bed bugs, and they fix nitrogen for beans. These symbioses underlie the evolutionary success of entire groups of organisms, from the grazing herds in Africa’s savannahs to animal communities in the abyssal oceans, to the aphids currently wrecking my garden.

But their earliest stages of these alliances are often mysterious. How does a random environmental bacterium, or one that causes disease, set up a lasting and productive partnership with a host? How does symbiosis itself evolve? Studies like this provide a clue. They show that bacteria can pick up traits that allow them to evolve more quickly into fitting partners—to shoot past that difficult getting-to-know-you phase, and go straight into a peaceful co-existence.

Reference: Remigi, Capela, Clerissi, Tasse, Torchet, Bouchez, Batut, Cruveiller, Rocha & Masson-Boivin. 2014. Transient Hypermutagenesis Accelerates the Evolution of Legume Endosymbionts following Horizontal Gene Transfer. PLoS Biol 12(9): e1001942.