Horizontal gene transfer can boost fitness quickly, but the conditions matter
by Jessica P. Johnson
Horizontal gene transfer (HGT) is rampant in the bacterial community, as well as in some other members of the tree of life. Researchers have long known that HGT events can improve an organism’s ability to adapt to changing environments. What’s less clear is just how long it takes to accrue such benefits — might it require on the order of hundreds of generations, or are multiple events over longer evolutionary time scales necessary?
Now, researchers have found that exposure to intense environmental pressure and the presence of foreign DNA donors can induce beneficial HGT events in E. coli within just a couple hundred generations. The findings were recently published in BMC Evolutionary Biology.
Previous laboratory-based attempts (for example, this paper as well as this one) to induce immediately beneficial HGT events — in which complete genes, not just alleles, were recombined into the bacterial chromosome — stopped at around 100 bacterial generations. Those studies suggested that although HGT events did occur, they produced either neutral or deleterious changes.
“In the short-term studies, people were working with very few generations … and they were not challenging the bacteria in a difficult environment,” says Hoi Yee (Athena) Chu, lead author on the current study. “So, in that sense, there’s no selective pressure to push the bacteria to innovate, and that’s why they didn’t see a lot of huge benefits.”
Chu and colleagues took a different approach. Over the course of as many as 1,000 generations, they adapted E. coli strains to food sources that the bacteria normally can’t grow on. First they challenged E. colistrain K12 with 4-Hydroxyphenylacetic acid (HPA). To encourage K12 to adapt via HGT, the researchers periodically added pulses of E. coli strains B or W as potential genetic donors. Both donor strains carry the hpa operon, which helps metabolize HPA.
After fewer than 200 generations, some of the replicate K12 cultures showed improved growth on HPA compared with donor-less control cultures. Genomic analysis revealed that all of the adapted K12 populations had received the hpa operon. And although strain B had donated more genetic material to recipients than the W strain, both donor strains conferred equal fitness benefits.
“There haven’t been a lot of studies looking at the transfer of operons in a way that, if you recombine them, what’s going to happen,” says David Baltrus, an evolutionary microbiologist at the University of Arizona in Tucson who was not involved with the study. “In the HPA case, you can make the argument that all you really need is the transfer of an operon or a couple of genes. And that bears out.”
The second phase of the experiment ramped up the challenge. This time, neither the strains serving as donors (in this phase K12 and B) nor the recipient strain (this time W) could grow on the challenge food source, butyric acid (BTA). This meant that the donor strains could not transfer a genetic quick fix to the recipient in the form of a complete operon.
After 800 generations, several populations of the W strain began to grow on BTA. But in contrast with the HPA experiment, both point mutations and HGT drove the adaptation. And, crucially, none of the genomic changes improved the populations’ fitness compared to the donor-less controls.
The contrasting results from the two sets of experiments suggest that beneficial HGT events can accrue quickly in adapting bacteria — but only under certain environmental conditions. And the conferred fitness benefits are greater when the DNA donor is unrelated to the recipient.
“Horizontal gene transfer is happening a lot and sometimes it matters and sometimes it doesn’t,” Baltrus says. “This is the first time that anyone has explicitly set up experiments to clearly test what happens when both HGT and mutation can help bacteria evolve over the same time scales. These are necessary experiments to understand and predict which path (HGT, mutation, or both) is going to be the main force in evolving microbial populations under different conditions.”
A great next step, Chu says, would be to investigate the benefits of HGT between more distantly related bacterial species in different challenging environments. Such studies, she says, could help scientists better understand the intermediate steps that occur before species fully diverge.
