In mBio this week, authors Joel Sachs and A.C. Hollowell of the University of California Riverside comment on "The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss" , a paper that created a bit of a stir when it was published earlier this month. Sachs and Hollowell write that the hypothesis has implications for how we understand the evolution of bacterial genomes and for the development of new techniques for growing bacteria in the lab. It also helps us understand how complex consortia of microorganisms are created and how they continue to work even when it appears some participants act against their own best interests.
The Black Queen Hypothesis, as described by the authors J. Jeffrey Morris, Richard Lenski, and Erik Zinser, describes the idea that microorganisms can lose the ability to carry out certain "leaky" functions if they can benefit from another organism to do it for them. It gives a name and a shape to the idea that cooperation among microbial species can be automatic and based upon purely selfish traits. The name comes from the card game Hearts, in which players generally try to avoid holding the queen of spades, the black queen. According to the hypothesis, the microbe unlucky enough to be providing a commodity or a service that is "leaky" and can be enjoyed by others in the vicinity, is holding the black queen - carrying the burden of producing for others while not necessarily getting much in return.
According to Sachs and Hollowell, one of the more helpful aspects of the hypothesis is that it helps us to understand what we see around us everywhere: microbial communities marked by disentangleable networks of interactions. The theory meshes nicely, they say, with models of by-product mutualism or by-product reciprocity, which predict that natural selection will shape receivers of by-products to maximize these benefits by being cooperative to by-product producers. Hence, they say, the trade-off in which one organism loses a gene and gains benefits from a "leaky" producer don't end there: it is in the benefitting organism's interest to give back, maximizing its benefits by being cooperative with the producers. Thus, the predicted evolutionary steps are as follows: (i) selfish usage of another species’ products, (ii) genome streamlining to minimize production of resources that can be gotten from others, and finally (iii) the evolution of costly cooperative traits to maximize vital functions produced by others. It's easy to see how gives and takes like this could quickly lead to a group of interacting partners who cannot be extricated from their surroundings and grown in the lab environment.