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

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Population-specific transcriptional differences associated with freeze tolerance in a terrestrial worm. / de Boer, Tjalf E.; Roelofs, Dick; Vooijs, Riet; Holmstrup, Martin; Amorim, Monica J. B.

I: Ecology and Evolution, Bind 8, Nr. 7, 04.2018, s. 3774-3786.

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avisTidsskriftartikelForskningpeer review

Harvard

de Boer, TE, Roelofs, D, Vooijs, R, Holmstrup, M & Amorim, MJB 2018, 'Population-specific transcriptional differences associated with freeze tolerance in a terrestrial worm', Ecology and Evolution, bind 8, nr. 7, s. 3774-3786. https://doi.org/10.1002/ece3.3602

APA

de Boer, T. E., Roelofs, D., Vooijs, R., Holmstrup, M., & Amorim, M. J. B. (2018). Population-specific transcriptional differences associated with freeze tolerance in a terrestrial worm. Ecology and Evolution, 8(7), 3774-3786. https://doi.org/10.1002/ece3.3602

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MLA

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Author

de Boer, Tjalf E. ; Roelofs, Dick ; Vooijs, Riet ; Holmstrup, Martin ; Amorim, Monica J. B. / Population-specific transcriptional differences associated with freeze tolerance in a terrestrial worm. I: Ecology and Evolution. 2018 ; Bind 8, Nr. 7. s. 3774-3786.

Bibtex

@article{4b4ee1c5b6954df3b884d4d414b8aa20,
title = "Population-specific transcriptional differences associated with freeze tolerance in a terrestrial worm",
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.",
keywords = "cryoprotectant, membrane lipid, oxidative stress, RNAseq, sodium transport, transcriptional plasticity, ENCHYTRAEUS-ALBIDUS OLIGOCHAETA, GENE-EXPRESSION, OXIDATIVE STRESS, DENDROBAENA-OCTAEDRA, LOW-TEMPERATURES, COLD TOLERANCE, METALLOTHIONEIN, RESPONSES, ADAPTATION, SALINITY",
author = "{de Boer}, {Tjalf E.} and Dick Roelofs and Riet Vooijs and Martin Holmstrup and Amorim, {Monica J. B.}",
year = "2018",
month = apr,
doi = "10.1002/ece3.3602",
language = "English",
volume = "8",
pages = "3774--3786",
journal = "Ecology and Evolution",
issn = "2045-7758",
publisher = "John Wiley Sons Ltd",
number = "7",

}

RIS

TY - JOUR

T1 - Population-specific transcriptional differences associated with freeze tolerance in a terrestrial worm

AU - de Boer, Tjalf E.

AU - Roelofs, Dick

AU - Vooijs, Riet

AU - Holmstrup, Martin

AU - Amorim, Monica J. B.

PY - 2018/4

Y1 - 2018/4

N2 - 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.

AB - 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.

KW - cryoprotectant

KW - membrane lipid

KW - oxidative stress

KW - RNAseq

KW - sodium transport

KW - transcriptional plasticity

KW - ENCHYTRAEUS-ALBIDUS OLIGOCHAETA

KW - GENE-EXPRESSION

KW - OXIDATIVE STRESS

KW - DENDROBAENA-OCTAEDRA

KW - LOW-TEMPERATURES

KW - COLD TOLERANCE

KW - METALLOTHIONEIN

KW - RESPONSES

KW - ADAPTATION

KW - SALINITY

U2 - 10.1002/ece3.3602

DO - 10.1002/ece3.3602

M3 - Journal article

C2 - 29686857

VL - 8

SP - 3774

EP - 3786

JO - Ecology and Evolution

JF - Ecology and Evolution

SN - 2045-7758

IS - 7

ER -