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.

Unravelling the DNA sequences carried by Streptomyces coelicolor membrane vesicles

“…Streptomyces is a genus of filamentous Gram-positive bacteria that are ubiquitous in terrestrial and marine environments, where they can live in symbiosis, for example, with plants, fungi, insects, and sponges 22 : adaptation to such diverse ecological niches and interaction with other (micro)organisms have led to the peculiar chemical diversity of their bioactive metabolites, whose production is regulated by a complex network of environmental signals, such as nutrient shortage and presence of competitors 22 – 24 . Streptomycetes have a complex life cycle as the mycelium of a colony is formed by distinct cell types (i.e., vegetative hyphae, aerial hyphae, and spores) and even different subpopulations: indeed, Streptomyces colonies have been recently described as similar to colonies of social insects with labor division, because of the presence of mutant cell subpopulations that are characterized by deletions and/or amplifications in the arms of their linear chromosomes, and that hyperproduce antibiotics at the expenses of their own fitness 25 , 26 .…”

Genomic adaptation in the CAZyome and specialised metabolism of the plant-associated Streptomyces violaceusniger clade

“…Streptomyces chromosome organisation consists in a central conserved genome whilst terminal sequences contain more variable gene content described as accessory genome [81][82][83]. This accessory genome undergoes frequent rearrangement, amplification and deletion events as well as interspecies homologous recombination [79,[84][85][86][87][88][89]. We decided to investigate commonalities and differences in the BGC organisation accross S. violaceusniger clade and to pinpoint original features of our newly sequenced AgN23 strain.…”

Evolution of genome fragility enables microbial division of labor

“…The antibiotic‐hyperproducing subset of cells in S. coelicolor colonies arises due to massive and irreversible deletions at the left and right arms of the Streptomyces linear chromosome (Zhang et al , 2020b). Cells with larger deletions produce more antibiotics but also produce significantly fewer spores, a deficit that effectively ensures their elimination during each replicative cycle (preprint: Zhang et al , 2020a). These antibiotic‐hyperproducing cells are instead repeatedly re‐generated independently in each colony following spore germination.…”

“…In Streptomyces , these variable chromosomal regions are located towards the telomeres of their linear chromosome and are known to evolve rapidly through DNA amplification, insertion, deletion, and recombination (Hoff et al , 2018; Tidjani et al , 2019, 2020). In particular, megabase‐long deletions occur frequently in the Streptomyces chromosome (Birch et al , 1990; Leblond & Decaris, 1994; Volff & Altenbuchner, 1998; preprint: Zhang et al , 2020a; Zhang et al , 2020b). These mutations are generated through homologous and nonhomologous recombination (possibly of sister chromatids; Fischer et al , 1998) of repeated genomic elements, typically transposons, which are unusually abundant towards the telomeres of the Streptomyces chromosome (Volff & Altenbuchner, 1998; Chen et al , 2002).…”