Transposable element insertions in fission yeast drive adaptation to environmental stress

Abstract

Cells are regularly exposed to a range of naturally occurring stress that can restrict growth or cause lethality. In response, cells activate expression networks with hundreds of genes that together increase resistance to common environmental insults. However, stress response networks can be insufficient to ensure survival, which raises the question of whether cells possess genetic programs that can promote adaptation to novel forms of stress. We found transposable element (TE) mobility in Schizosaccharomyces pombe was greatly increased when cells were exposed to unusual forms of stress such as heavy metals, caffeine, and the plasticizer phthalate. By subjecting TE-tagged cells to CoCl 2 , we found the TE integration provided the major path to resistance. Groups of insertions that provided resistance were linked to TOR regulation and metal response genes. We extended our study of adaptation by analyzing TE positions in 57 genetically distinct wild strains. The genomic positions of 1048 polymorphic LTRs were strongly associated with a range of stress response genes, indicating TE integration promotes adaptation in natural conditions. These data provide strong support for the idea, first proposed by Barbara McClintock, that TEs provide a system to modify the genome in response to stress.

Diverse transposable element landscapes in pathogenic and nonpathogenic yeast models: the value of a comparative perspective

“…The TOR pathway was shown to provide resistance to cobalt, indicating that changes in expression of TOR-regulated genes due to neighboring Tf1 sequences could account for overrepresentation of those strains [226]. Strains harboring specific individual Tf1 insertions outcompeted wild type strains when grown in cobalt, but showed a growth disadvantage in the absence of the stress [226]. Overall, these observations support a role for Tf1 in adaptive gene expression changes conferring increased resistance to particular stresses.…”

“…Tf1 transcription is induced by a short heat stress (39°C for 15 min) or a low dose of hydrogen peroxide, but not osmotic stress or cadmium [225]. Retrotransposition of at least some individual elements also increases in reponse to cobalt, zinc, caffeine, or phthalate [226]. There is only limited overlap between the stresses that regulate Tf1 and those that regulate Ty1 in S. cerevisiae.…”

“…Particular Tf1 insertions can also provide selective advantages to cells in specific environmental contexts. A library of > 40,000 strains each harboring a single newly integrated Tf1 grown together for many generations in the presence of a moderate concentration of cobalt (a stress that can activate Tf1) showed that while thousands of strains became underrepresented, a subset of > 100 strains became consistently overrepresented in replicate final populations [226]. These latter strains had Tf1 insertions that were frequently near genes that are induced by cadmium or peroxide, or genes regulated by the TOR pathway involved in nutrient sensing and cell growth.…”

“…These latter strains had Tf1 insertions that were frequently near genes that are induced by cadmium or peroxide, or genes regulated by the TOR pathway involved in nutrient sensing and cell growth. The TOR pathway was shown to provide resistance to cobalt, indicating that changes in expression of TOR-regulated genes due to neighboring Tf1 sequences could account for overrepresentation of those strains [226]. Strains harboring specific individual Tf1 insertions outcompeted wild type strains when grown in cobalt, but showed a growth disadvantage in the absence of the stress [226].…”

Remodeling of theC. elegansNon-coding RNA Transcriptome by Heat Shock

“…Additionally, changes in genomic arrangement caused by stress induced expression of transposons could foster beneficial changes in the progeny of stressed parents. Evidence for this idea was recently documented in Schizosaccharomyces pombe, where certain forms of stress induced the mobility of transposable elements and the new insertions were linked to enhanced adaptation to the assault (75). As elevated temperatures have been associated with increased genetic mobility in C. elegans (76), it is possible that relaxed silencing of transposons during HS could sometimes provide an advantageous genetic change in the progeny of stressed animals.…”