The Black Queen Hypothesis

In the game of Hearts, the object is to not get certain cards. The most vile of them all is the dreaded black queen of spades, which is as bad as all the other bad cards put together.

In a recent theory paper, Jeff Morris, Rich Lenski, and Erik Zinser present the Black Queen Hypothesis to explain why some organisms lose genes that are apparently important for survival.

Prochlorococcus is a bacterium that is able to live in an environment full of a toxic peroxide, HOOH, because they have a gene, KatG, that produces catalase-peroxidase, a compound that neutralizes HOOH. But then why are some forms of Prochlorococcus able to survive in this environment even without a functional copy of KatG? Here is their Black Queen Hypothesis:

In the context of evolution, the BQH posits that certain genes, or more broadly, biological functions, are analogous to the queen of spades. Such functions are costly and therefore undesirable, leading to a selective advantage for organisms that stop performing them. At the same time, the function must provide an indispensable public good, necessitating its retention by at least a subset of the individuals in the community—after all, one cannot play Hearts without a queen of spades. The detoxification of HOOH fulfills both of these criteria, and therefore the BQH predicts that this function will be performed by helpers that comprise only a fraction of the community.

In other words, the mutant form of Prochlorococcus that does not have KatG survives because of the public good produced by the original Prochlorococcus with a functional copy of KatG. And it does not cause the original type to become extinct, because it depends on it for removing HOOH from the environment.

Initially, all Prochlorococcus has the gene, KatG, that allows the bacteria to produce catalase-peroxidase. This allows the cells to live in an environment with a peroxide, HOOH (blue), which is otherwise toxic. The HOOH diffuses into the cells, where it is neutralized by catalase-peroxidase. This creates a gradient such that there is less HOOH the closer you get to the center of the colony.

A mutant is born (red cell) that has lost KatG, and so cannot produce catalase-peroxidase. If it were to live in an environment with HOOH, it would die. However, it can live close to other Prochlorococcus that are resistant to HOOH (blue), because these resistant cells remove HOOH from the environment.

Because producing KatG comes at a slight cost in fitness, those who don't spend the resources producing it has a slight reproductive advantage over those who do. As a result, the mutant Prochlorococcus will soon increase in number.

An equilibrium is established such that the original KatG producing Prochlorococcus and the mutant form coexist, because the higher the number of mutant cells results in less HOOH being removed from the environment. Negative frequency-dependent selection thus ensures that both types can exist side by side, because it is favorable to be the less frequent type.

Negative frequency-dependent selection works like this: If chance would have it that more is born of the mutant type, then there isn't enough space for them where HOOH is being removed, and some will die. However, the original KatG producers are still fine, so they will have a fitness advantage and grow in number. If it happens that there are few mutants, they they again has a fitness advantage over the original type, and now they will grow in number.

Jeff Morris

Luckily, Jeff works three doors down the hall from me, and so I was able to go talk to him about the BQH. The BQH is formulated mathematically as if the organisms/bacteria are in a homogeneous well-mixed environment. However, this is of course, as they discuss in the paper, not 100% realistic. Bacteria often exist in microenvironments, and it matters where the mutant cells are in space in relation to the original KatG producers; if they are too far away, HOOH is not removed from their environment, and they die. Jeff agrees that this heterogeneity - as portrayed in the figures above, where HOOH isn't removed equally from all of space - changes the dynamics somewhat, most probably by shifting the equilibrium frequencies of the two types, such that there are fewer mutants in a heterogeneous environment compared to a well-mixed homogeneous environment.

Jeff has this to add (personal correspondence):

No modern Prochlorococcus (that we've found so far) has katG. Almost all other cyanobacteria do, however, so we infer that Pro lost it at some point. The "helpers" in the modern ocean are entirely different species. So really what you're describing in the blog is the hypothetical process by which the first Pro to lost katG was able to invade its ancestral population.

The neat thing is that, because other species exist that aren't in competition with Pro but still degrade HOOH, the katG-deficient Pro was able to sweep its ancestor to extinction. In general BQH stands out (along with Red Queen) in considering interspecies interactions more explicitly than most evolutionary ideas.

Read more about the BQH on BEACON's blog and Science Daily.

Reference:
Morris JJ, Lenski RE, & Zinser ER (2012). The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. mBio, 3 (2) PMID: 22448042.