Mutational meltdown of putative microbial altruists in Streptomyces coelicolor colonies

Abstract

In colonies of the filamentous multicellular bacterium Streptomyces coelicolor, a subpopulation of cells arises that hyperproduces metabolically costly antibiotics, resulting in a division of labor that increases colony fitness. Because these cells contain large genomic deletions that cause massive reductions to individual fitness, their behavior is similar to altruistic worker castes in social insects or somatic cells in multicellular organisms. To understand these mutant cells’ reproductive and genomic fate 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, putatively altruistic mutant cells continue to decline in fitness during transfer while they lose more fragments from their chromosome ends. In addition, the base-substitution rate in mutants increases roughly 10-fold, possibly due to mutations in genes for DNA replication and repair. Ecological damage, caused by reduced sporulation, coupled with DNA damage due to point mutations and deletions, leads to an inevitable and irreversible type of mutational meltdown in these cells. Taken together, these results suggest the cells arising in the S. coelicolor division of labor are analogous to altruistic reproductively sterile castes of social insects.

Evolution of genome fragility enables microbial division of labor

“…Fragile sites effectively introduce an asymmetry in the model genome, with the left part of the chromosome being mutationally more quiet than the right side. This mimics the increased telomeric deletion rate observed in the Streptomyces chromosome (Chen et al , 2002; Hopwood, 2006; Hoff et al , 2018; Tidjani et al , 2020), though we note three points: (i) We model only one arm of the Streptomyces chromosome, from the centromere to one telomere; (ii) in the model, the distinction between centromeric and telomeric regions depends solely on fragile sites, whereas Streptomyces telomeres are specific genomic structures that can be recognized independently from the mutational dynamics; (iii) in Streptomyces , fragile site‐induced mutations transiently cause a complex interplay of duplications and deletions, which only after several mutational events result in the large‐scale elimination of DNA (Altenbuchner & Cullum, 1984; Zhang et al , 2022)—here we simplify this complexity by letting activated fragile site delete the entire chromosome to their right. Novel fragile sites are spontaneously generated at random genomic locations with a small probability per replication.…”

Characterization of a novel temperate phage facilitatingin vitrodispersal of multicellular bacteria

“…Assuming that Samy-mediated dispersion may provide a selective advantage under certain conditions ( e.g. switch from BM to SFM growth condition), its production could illustrate a division of labor leading to an ‘altruistic’ loss of fitness within a subpopulation of cells (59).…”

Bacterial multicellular behavior in antiviral defense

“…Genomic diversification has recently been shown for Streptomyces colonies leading to the emergence of hyperproducers of antimicrobial substances [77]. After their emergence, the fraction of genetically degenerated hyperproducers was shown to undergo further mutational meltdown leading to their removal from the population [78] -a concept which is reminiscent to altruism expressed by sterile castes in social insects.…”