Genetics of Adaptation of the Ascomycetous Fungus Podospora anserina to Submerged Cultivation

Abstract

Podospora anserina is a model ascomycetous fungus which shows pronounced phenotypic senescence when grown on solid medium but possesses unlimited lifespan under submerged cultivation. In order to study the genetic aspects of adaptation of P. anserina to submerged cultivation, we initiated a long-term evolution experiment. In the course of the first 4 years of the experiment, 125 single-nucleotide substitutions and 23 short indels were fixed in eight independently evolving populations. Six proteins that affect fungal growth and development evolved in more than one population; in particular, in the G-protein alpha subunit FadA, new alleles fixed in seven out of eight experimental populations, and these fixations affected just four amino acid sites, which is an unprecedented level of parallelism in experimental evolution. Parallel evolution at the level of genes and pathways, an excess of nonsense and missense substitutions, and an elevated conservation of proteins and their sites where the changes occurred suggest that many of the observed fixations were adaptive and driven by positive selection.

Dynamics of Podospora anserina Genome Evolution in a Long-Term Experiment

“…Such changes were described with great care in the course of our preliminary short-term P. anserina experiment [11]. By starting the PaLTEE, we noted similar phenotypic changes in all independent lineages [10]. Thus, the visible changes were reproducible not only in parallel cultivated lines, but also in independent experiments on the adaptation of P. anserina to submerged cultivation.…”

“…268). As a result, SNPs and indels were detected [10]. Over the next 4 years, the whole genome sequence of all of the lineages was performed two more times (for passages no.…”

“…During the first 4 years of the experiment, at selected time points, we tested whether de novo mutations were fixed in our model system. Using two different sequencing methods, we demonstrated the fixation of single-nucleotide polymorphisms (SNPs) and short insertion and deletion mutations (indels) in the genomes of all of the experimental populations [10]. Thus, the P. anserina model system was assessed as promising, and we decided to continue the experiment.…”

The role of tradeoffs among life-history traits in a filamentous fungus

“…Mutations in veA and AN5849 seem clearly adaptive, since they appear in four populations at an early time-point, and likely went to high frequency by the end of the experiment in five populations, as we picked them up by sequencing random clones (see figure 5.2). An evolution experiment studying adaptation to submerged cultivation in the ascomycete Podospora anserina also found parallel mutations in veA along with proI homologs of P. anserina (Kudryavtseva et al, 2019). Thus, suggesting filamentous fungi adapt to laboratory environment by mutating veA.…”

“…Filamentous fungi have been used in experimental evolution to address a range of topics; for example, the role of environmental structure (Kudryavtseva et al, 2019), epistasis (Schoustra et al, 2016), bet-hedging (Graham et al, 2014), and rate and distribution of mutations (Gifford et al, 2011;Schoustra et al, 2009) during adaptation. Fungi have been used to address the evolution of antimicrobial resistance and the role of compensatory mutations during evolution of antimicrobial resistance (Schoustra et al, 2006;Zhang et al, 2015).…”