Population-specific transcriptional differences associated with freeze tolerance in a terrestrial worm

Tjalf E. de Boer, Dick Roelofs*, Riet Vooijs, Martin Holmstrup, Mónica J.B. Amorim

*Corresponding author for this work

    Research output: Contribution to JournalArticleAcademicpeer-review

    Abstract

    Enchytraeus albidus is a terrestrial earthworm widespread along the coasts of northern Europe and the Arctic. This species tolerates freezing of body fluids and survives winters in a frozen state. Their acclimatory physiological mechanisms behind freeze tolerance involve increased fluidity of membrane lipids during cold exposure and accumulation of cryoprotectants (glucose) during the freezing process. Gene regulatory processes of these physiological responses have not been studied, partly because no gene expression tools were developed. The main aim of this study was to understand whether the freeze tolerance mechanisms have a transcriptomic basis in E. albidus. For that purpose, first the transcriptome of E. albidus was assembled with RNAseq data. Second, two strains from contrasting thermal environments (Germany and Greenland) were compared by mapping barcoded RNAseq data onto the assembled transcriptome. Both of these strains are freeze tolerant, but Greenland is extremely freeze tolerant. Results showed more plastic responses in the Greenland strain as well as higher constitutive expression of particular stress response genes. These altered transcriptional networks are associated with an adapted homeostasis coping with prolonged freezing conditions in Greenland animals. Previously identified physiological alterations in freeze-tolerant strains of E. albidus are underpinned at the transcriptome level. These processes involve anion transport in the hemolymph, fatty acid metabolism, metabolism, and transport of cryoprotective sugars as well as protection against oxidative stress. Pathway analysis supported most of these processes, and identified additional differentially expressed pathways such as peroxisome and Toll-like receptor signaling. We propose that the freeze-tolerant phenotype is the consequence of genetic adaptation to cold stress and may have driven evolutionary divergence of the two strains.

    Original languageEnglish
    Pages (from-to)3774-3786
    Number of pages13
    JournalEcology and Evolution
    Volume8
    Issue number7
    Early online date11 Mar 2018
    DOIs
    Publication statusPublished - Apr 2018

    Funding

    DR is supported by grants from the BE-BASIC foundation (F08.001.03, and F07.003.05) and received additional funding from EU FP7 program Sustainable Nanotechnologies (SUN) grant number 604305). MA received funds from the research project NM_OREO (POCI-01-0145-FEDER-016771, PTDC/AAG-MAA/4084/2014) and CESAM (UID/AMB/50017), by FEDER through COMPETE Programa Operacional Factores de Competitividade, through FCT-Fundação para a Ciência e Tecnologia, and within the PT2020 Partnership Agreement and Compete 2020. MH was supported by The Danish Council for Independent Research (contract no. 10-084579). We acknowledge the help provided by A.L. Patricio-Silva during the exposures of the animals. Finally, TEdB would like to thank SurfSARA to allow transcriptome assembly on their high performance computing cloud.

    FundersFunder number
    EU FP7 program Sustainable Nanotechnologies
    Seventh Framework Programme604305
    Centro de Estudos Ambientais e Marinhos, Universidade de AveiroUID/AMB/50017
    Fundação para a Ciência e a Tecnologia
    Seconda Università degli Studi di NapoliPOCI-01-0145-FEDER-016771, PTDC/AAG-MAA/4084/2014
    Danmarks Frie Forskningsfond10-084579
    BE-Basic FoundationF07.003.05, F08.001.03

      Keywords

      • cryoprotectant
      • membrane lipid
      • oxidative stress
      • RNAseq
      • sodium transport
      • transcriptional plasticity

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