The spontaneous mutation frequencies of Prochlorococcus strains are commensurate with those of other bacteria

Abstract

Summary 23The marine cyanobacterium Prochlorococcus, the smallest and most abundant 24 oxygenic phototroph, has an extremely streamlined genome and a high rate of protein 25 evolution. High-light adapted strains of Prochlorococcus in particular have seemingly 26 inadequate DNA repair systems, raising the possibility that inadequate repair may lead 27 to high mutation rates. Prochlorococcus mutation rates have been difficult to determine, 28 in part because traditional methods involving quantifying colonies on solid selective 29 media are not straightforward for this organism. Here we used a liquid dilution method 30 to measure the approximate number of antibiotic-resistant mutants in liquid cultures of 31Prochlorococcus strains previously unexposed to antibiotic selection. Several antibiotics 32 for which resistance in other bacteria is known to result from a single base pair change 33 were used. The resulting frequencies of antibiotic resistance in Prochlorococcus 34 cultures allowed us to then estimate maximum spontaneous mutation rates, which were 35 similar to those in organisms such as E. coli (~5.4x10 -7 per gene per generation). 36 Therefore, despite the lack of some DNA repair genes, it appears unlikely that the 37 Prochlorcoccus genomes studied here are currently being shaped by unusually high 38 mutation rates.

Mutator genomes decay, despite sustained fitness gains, in a long-term experiment with bacteria

“…However, their ocean-wide distribution and massive populations should severely limit the effect of drift with respect to genome decay (78). It has been hypothesized that these genomic properties could have arisen as a consequence of the absence of DNA repair genes in their genomes (79), but direct measurements of Prochlorococcus mutation rates do not indicate a hypermutable phenotype (80). These discrepant observations might be reconciled by a scenario that combines strong genetic draft in a hypermutable progenitor of Prochlorococcus followed by a more recent compensation event that reestablished a low mutation rate.…”

How do divergent ecological strategies emerge among marine bacterioplankton lineages?

“…Another nonselective mechanism, acceleration of mutation rate as a result of loss of certain DNA repair genes accompanied by mutational bias toward deletion, is well known for endosymbionts [52], but this has not been demonstrated for marine bacterioplankton [73,87]. It is worth noting that measuring the spontaneous mutation rate of streamlined bacteria is difficult because they grow slowly and are not easily propagated under laboratory conditions.…”

“…Are there life-history strategies distinct from adaptation to organic matter concentration that could also provide insights into the evolutionary path of marine bacteria? Assuming an average genome size of 4.5 Mb [32] and 1.15 generations per day [53] for a patch-associated Roseobacter cell, and 1.3 Mb [33] and 0.51 generations [53] for a free-living SAR11 cell, along with a spontaneous mutation rate of 10 -10 to 10 -9 per generation per base pair (as is typical for non-endosymbiotic bacteria such as Escherichia coli, Bacillus subtilis, Prochlorococcus spp., and others; [52,73]), we can expect a mutation to arise every 0.5-5 years in a Roseobacter cell and every 4-40 years in a SAR11 cell. On the temporal scale relevant to recorded climate change over the past 100 years [74] and a projected steeper change in the next 100 years [75], approximately 40-380 mutations will arise in a typical Roseobacter genome and 5-50 mutations in a SAR11 genome in these 200 years.…”

Microdiversity shapes the traits, niche space, and biogeography of microbial taxa

“…The microdiversity models examined here are relatively simple, but result in highly complex and dynamic communities of microorganisms. Given the enormous effective population size of most microbial taxa, there is a high chance for selection to act upon genetic variation and create a high number of subtle fitness differences between microdiverse sub-taxa (Osburne et al, 2011;Baumdicker et al, 2012;Biller et al, 2015). Under the Renaissance model, a wide variety of traits can be acquired through horizontal gene transfer, resulting in access to a myriad of trait axes.…”

“…The large fundamental niches of microbes with microdiverse sub-taxa (Osburne et al, 2011;Baumdicker et al, 2012) decrease the likelihood of novel conditions arising that are not currently captured by the fundamental niche of the taxon. Therefore, if the full biogeographic distribution of a taxon is known, and a small portion of that distribution is subjected to conditions that match future predictions, then it is possible to subsequently predict the future composition of the community since migration is more likely than adaptation (Pearman et al, 2008;Morin and Thuiller, 2009;Lavergne et al, 2010).…”