If we believe the popular press, animals are little more than glorified buses for the multitude of microbes that live on and within us. These microbes coordinate our diets, our immunity, our mate choice and much else. Given these claims, it is easy to believe that our microbial passengers are uniformly beneficial, that they toil for our betterment. But this is not quite the reality. Our bacteria instead run the gamut of utility, sometimes beneficial, sometimes harmful, but most often entirely indifferent to our welfare. And to make it more interesting, these functions can change through time and context. But how do these roles evolve? And can commensal bacteria, which neither hurt nor harm us, be pushed to become mutualists that help their hosts?
To address these questions, Kayla King from the University of Oxford, UK, and her colleagues from the Universities of York and Liverpool focused their experimental attention on the microbiota of the soil nematode, Caenorhabditis elegans. These nematodes eat bacteria, but not everything they eat is food. Instead, some bacterial species like Enterococcus faecalis take up residence in the nematode gut as mildly harmful commensals, while others like Staphylococcus aureus are highly pathogenic. On its own, E. faecalis kills less than 1% of worms, while S. aureus wipes out more than half of the worms that eat it. More interesting, when worms are colonized with E. faecalis before infection with S. aureus, mortality drops markedly. So far so good: by providing protection to the worms, the role of E. faecalis transitions from minor pest to major partner. But how does this protection arise and can it improve?
The team experimentally evolved E. faecalis within worms under two different regimes. In the first, E. faecalis was passaged serially through worms for 15 transfer cycles, while in the second E. faecalis was forced to share its space with S. aureus. This small change led to striking differences. Whereas E. faecalis in the first regime became marginally more aggressive towards the worms, E. faecalis in the second regime evolved into highly effective mutualists that fully suppressed S. aureus virulence. Instead of killing 20% of worms when grown with E. faecalis from the first regime, S. aureus grown with E. faecalis from the second regime killed almost none.
One possible conclusion from this study is that E. faecalis evolved to benefit worms because of some positive feedback between these two organisms. The bacteria helped the worms, and the worms helped the bacteria. However, the actual conclusion drawn by the authors is more interesting and, probably, more general. To suppress S. aureus virulence, E. faecalis simply evolved the ability to secrete toxins that killed its competitors. In other words, E. faecalis didn't evolve to become mutualistic because it cared about worms or gained something in return, but rather because it cared about its own welfare. By killing S. aureus, E. faecalis benefited directly, while any positive consequence of this for the worms was only a fortuitous by-product of inter-bacterial warfare. Fortunately for the worms, they were as indifferent to E. faecalis toxins as E. faecalis was to the worms.
What is particularly neat about this work is how rapidly the role of E. faecalis evolved. But do the bacteria in our guts have a similar capacity for change? At present, this isn't entirely clear. While the bacteria in our microbiome are extremely numerous, subject to huge mutational and ecological diversity, they are also rarely on their own. Enterococcus faecalis in the present work faced a static challenger. If S. aureus could co-evolve with E. faecalis, or if the competitive environment of the laboratory worm gut was more reflective of the wild-type gut, would the results have been the same? I certainly hope that the next step in this study is to find out.