Nascent transcription reveals regulatory changes in extremophile fishes inhabiting hydrogen sulfide-rich environments

Author:

Perry Blair W.1ORCID,McGowan Kerry L.1ORCID,Arias-Rodriguez Lenin2,Duttke Sascha H.3,Tobler Michael456,Kelley Joanna L.7ORCID

Affiliation:

1. School of Biological Sciences, Washington State University, Pullman, WA 99164, USA

2. División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco, Villahermosa, Tabasco 86150, México

3. School of Molecular Biosciences, Washington State University, Pullman, WA 99164, USA

4. Department of Biology, University of Missouri—St Louis, St Louis, MO 63121, USA

5. Whitney R. Harris World Ecology Center, University of Missouri—St Louis, St Louis, MO 63121, USA

6. WildCare Institute, Saint Louis Zoo, St Louis, MO 63110, USA

7. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA 95060, USA

Abstract

Regulating transcription allows organisms to respond to their environment, both within a single generation (plasticity) and across generations (adaptation). We examined transcriptional differences in gill tissues of fishes in the Poecilia mexicana species complex (family Poeciliidae), which have colonized toxic springs rich in hydrogen sulfide (H 2 S) in southern Mexico. There are gene expression differences between sulfidic and non-sulfidic populations, yet regulatory mechanisms mediating this gene expression variation remain poorly studied. We combined capped-small RNA sequencing (csRNA-seq), which captures actively transcribed (i.e. nascent) transcripts, and messenger RNA sequencing (mRNA-seq) to examine how variation in transcription, enhancer activity, and associated transcription factor binding sites may facilitate adaptation to extreme environments. csRNA-seq revealed thousands of differentially initiated transcripts between sulfidic and non-sulfidic populations, many of which are involved in H 2 S detoxification and response. Analyses of transcription factor binding sites in promoter and putative enhancer csRNA-seq peaks identified a suite of transcription factors likely involved in regulating H 2 S-specific shifts in gene expression, including several key transcription factors known to respond to hypoxia. Our findings uncover a complex interplay of regulatory processes that reflect the divergence of extremophile populations of P. mexicana from their non-sulfidic ancestors and suggest shared responses among evolutionarily independent lineages.

Funder

L'Oreal Fellowship for Women in Science

Life Sciences Division, Army Research Office

Division of Integrative Organismal Systems

American Livebearing Association

Publisher

The Royal Society

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