microRNA expression variation as a potential molecular mechanism contributing to adaptation to hydrogen sulphide

Abstract

microRNAs (miRNAs) are post‐transcriptional regulators of gene expression and can play an important role in modulating organismal development and physiology in response to environmental stress. However, the role of miRNAs in mediating adaptation to diverse environments in natural study systems remains largely unexplored. Here, we characterized miRNAs and their expression in Poecilia mexicana, a species of small fish that inhabits both normal streams and extreme environments in the form of springs rich in toxic hydrogen sulphide (H2S). We found that P. mexicana has a similar number of miRNA genes as other teleosts. In addition, we identified a large population of mature miRNAs that were differentially expressed between locally adapted populations in contrasting habitats, indicating that miRNAs may contribute to P. mexicana adaptation to sulphidic environments. In silico identification of differentially expressed miRNA‐mRNA pairs revealed, in the sulphidic environment, the downregulation of miRNAs predicted to target mRNAs involved in sulphide detoxification and cellular homeostasis, which are pathways essential for life in H2S‐rich springs. In addition, we found that predicted targets of upregulated miRNAs act in the mitochondria (16.6% of predicted annotated targets), which is the main site of H2S toxicity and detoxification, possibly modulating mitochondrial function. Together, the differential regulation of miRNAs between these natural populations suggests that miRNAs may be involved in H2S adaptation by promoting functions needed for survival and reducing functions affected by H2S. This study lays the groundwork for further research to directly demonstrate the role of miRNAs in adaptation to H2S. Overall, this study provides a critical stepping‐stone towards a comprehensive understanding of the regulatory mechanisms underlying the adaptive variation in gene expression in a natural system.

Epigenetic inheritance of DNA methylation changes in fish living in hydrogen sulfide–rich springs

“…We have previously shown that P. mexicana from sulfidic populations can survive in high levels of H 2 S by constitutively expressing high levels of important H 2 S detoxification genes (40)(41)(42), and some sulfidic populations have evolved a resistant cytochrome c oxidase (43). Moreover, there is heritable variation in gene expression, especially in key genes related to H 2 S toxicity and detoxification (44), some of which may be driven by expression differences of relevant microRNAs (45). Despite these observations, a key gap in our knowledge is the effect of H 2 S exposure on epigenetics and whether expression changes due to H 2 S exposure and local adaptation are potentially mediated by DNA methylation changes.…”

Circulating miRNA diversity, origin and response to changing metabolic and reproductive states, new insights from the rainbow trout

“…[31], which was first run using the rainbow trout reference genome (NCBI RefSeq assembly accession GCF_002163495.1) and all ovarian fluid and plasma reads generated in the present study. This was performed using a set of five manually curated fish mature and hairpin sequences ( Lepisosteus oculatus, Danio rero , Poecilia Mexicana, Gasterosteus aculeatus , and Chaenocephalus aceratus ) [30,32,33]. Prost!…”

Inheritance of Acquired Traits in Insects and Other Animals and the Epigenetic Mechanisms That Break the Weismann Barrier

“…These regions of DNA methylation were related to various cellular activities ranging from signaling to apoptosis, and sulfur metabolism. These methylated regions showed a high degree of overlap across generations, suggesting DNA methylation as a possible epigenetic mechanism for this heritable adaptive phenotype [35].…”