Mutational meltdown of microbial altruists in Streptomyces coelicolor colonies

Abstract In colonies of the filamentous multicellular bacterium Streptomyces coelicolor, a sub-population of cells arise that hyper-produce metabolically costly antibiotics, resulting in a division of labor that maximizes colony fitness. Because these cells contain large genomic deletions that cause massive reductions to individual fitness, their behavior is altruistic, much like worker castes in eusocial insects. To understand the reproductive and genomic fate of these mutant cells after their emergence, we use experimental evolution by serially transferring populations via spore-to-spore transfer for 25 cycles, reflective of the natural mode of bottlenecked transmission for these spore-forming bacteria. We show that, in contrast to wild-type cells, altruistic mutant cells continue to significantly decline in fitness during transfer while they delete larger and larger fragments from their chromosome ends. In addition, altruistic mutants acquire a roughly 10-fold increase in their base-substitution rates due to mutations in genes for DNA replication and repair. Ecological damage, caused by reduced sporulation, coupled with irreversible DNA damage due to point mutation and deletions, leads to an inevitable and irreversible type of mutational meltdown in these cells. Taken together, these results suggest that the altruistic cells arising in this division of labor are equivalent to reproductively sterile castes of social insects.