Transcriptome resilience predicts thermotolerance in Caenorhabditis elegans

Katharina Jovic, Jacopo Grilli, Mark G. Sterken, Basten L. Snoek, Joost A.G. Riksen, Stefano Allesina, Jan E. Kammenga

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

The detrimental effects of a short bout of stress can persist and potentially turn lethal, long after the return to normal conditions. Thermotolerance, which is the capacity of an organism to withstand relatively extreme temperatures, is influenced by the response during stress exposure, as well as the recovery process afterwards. While heat-shock response mechanisms have been studied intensively, predicting thermal tolerance remains a challenge.
Results: Here, we use the nematode Caenorhabditis elegans to measure transcriptional resilience to heat stress and predict thermotolerance. Using principal component analysis in combination with genome-wide gene expression profiles collected in three high-resolution time series during control, heat stress, and recovery conditions, we infer a quantitative scale capturing the extent of stress-induced transcriptome dynamics in a single value. This scale provides a basis for evaluating transcriptome resilience, defined here as the ability to depart from stress-expression dynamics during recovery. Independent replication across multiple highly divergent genotypes reveals that the transcriptional resilience parameter measured after a spike in temperature is quantitatively linked to long-term survival after heat stress.
Conclusion: Our findings imply that thermotolerance is an intrinsic property that pre-determines long-term outcome of stress and can be predicted by the transcriptional resilience parameter. Inferring the transcriptional resilience parameters of higher organisms could aid in evaluating rehabilitation strategies after stresses such as disease and trauma.
Original languageEnglish
Article number102
JournalBMC Biology
Volume17
Issue number1
DOIs
Publication statusPublished - 10 Dec 2019

Fingerprint

Caenorhabditis elegans
heat tolerance
Transcriptome
transcriptome
heat stress
Hot Temperature
Heat-Shock Response
Temperature
organisms
Principal Component Analysis
lethal genes
Recovery
time series analysis
stress response
temperature
principal component analysis
Rehabilitation
Genotype
Nematoda
Genome

Cite this

Jovic, Katharina ; Grilli, Jacopo ; Sterken, Mark G. ; Snoek, Basten L. ; Riksen, Joost A.G. ; Allesina, Stefano ; Kammenga, Jan E. / Transcriptome resilience predicts thermotolerance in Caenorhabditis elegans. In: BMC Biology. 2019 ; Vol. 17, No. 1.
@article{f166a0be8b244fb384df8895b5ad6752,
title = "Transcriptome resilience predicts thermotolerance in Caenorhabditis elegans",
abstract = "The detrimental effects of a short bout of stress can persist and potentially turn lethal, long after the return to normal conditions. Thermotolerance, which is the capacity of an organism to withstand relatively extreme temperatures, is influenced by the response during stress exposure, as well as the recovery process afterwards. While heat-shock response mechanisms have been studied intensively, predicting thermal tolerance remains a challenge.Results: Here, we use the nematode Caenorhabditis elegans to measure transcriptional resilience to heat stress and predict thermotolerance. Using principal component analysis in combination with genome-wide gene expression profiles collected in three high-resolution time series during control, heat stress, and recovery conditions, we infer a quantitative scale capturing the extent of stress-induced transcriptome dynamics in a single value. This scale provides a basis for evaluating transcriptome resilience, defined here as the ability to depart from stress-expression dynamics during recovery. Independent replication across multiple highly divergent genotypes reveals that the transcriptional resilience parameter measured after a spike in temperature is quantitatively linked to long-term survival after heat stress.Conclusion: Our findings imply that thermotolerance is an intrinsic property that pre-determines long-term outcome of stress and can be predicted by the transcriptional resilience parameter. Inferring the transcriptional resilience parameters of higher organisms could aid in evaluating rehabilitation strategies after stresses such as disease and trauma.",
author = "Katharina Jovic and Jacopo Grilli and Sterken, {Mark G.} and Snoek, {Basten L.} and Riksen, {Joost A.G.} and Stefano Allesina and Kammenga, {Jan E.}",
year = "2019",
month = "12",
day = "10",
doi = "10.1186/s12915-019-0725-6",
language = "English",
volume = "17",
journal = "BMC Biology",
issn = "1741-7007",
publisher = "Springer Verlag",
number = "1",

}

Transcriptome resilience predicts thermotolerance in Caenorhabditis elegans. / Jovic, Katharina; Grilli, Jacopo; Sterken, Mark G.; Snoek, Basten L.; Riksen, Joost A.G.; Allesina, Stefano; Kammenga, Jan E.

In: BMC Biology, Vol. 17, No. 1, 102, 10.12.2019.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Transcriptome resilience predicts thermotolerance in Caenorhabditis elegans

AU - Jovic, Katharina

AU - Grilli, Jacopo

AU - Sterken, Mark G.

AU - Snoek, Basten L.

AU - Riksen, Joost A.G.

AU - Allesina, Stefano

AU - Kammenga, Jan E.

PY - 2019/12/10

Y1 - 2019/12/10

N2 - The detrimental effects of a short bout of stress can persist and potentially turn lethal, long after the return to normal conditions. Thermotolerance, which is the capacity of an organism to withstand relatively extreme temperatures, is influenced by the response during stress exposure, as well as the recovery process afterwards. While heat-shock response mechanisms have been studied intensively, predicting thermal tolerance remains a challenge.Results: Here, we use the nematode Caenorhabditis elegans to measure transcriptional resilience to heat stress and predict thermotolerance. Using principal component analysis in combination with genome-wide gene expression profiles collected in three high-resolution time series during control, heat stress, and recovery conditions, we infer a quantitative scale capturing the extent of stress-induced transcriptome dynamics in a single value. This scale provides a basis for evaluating transcriptome resilience, defined here as the ability to depart from stress-expression dynamics during recovery. Independent replication across multiple highly divergent genotypes reveals that the transcriptional resilience parameter measured after a spike in temperature is quantitatively linked to long-term survival after heat stress.Conclusion: Our findings imply that thermotolerance is an intrinsic property that pre-determines long-term outcome of stress and can be predicted by the transcriptional resilience parameter. Inferring the transcriptional resilience parameters of higher organisms could aid in evaluating rehabilitation strategies after stresses such as disease and trauma.

AB - The detrimental effects of a short bout of stress can persist and potentially turn lethal, long after the return to normal conditions. Thermotolerance, which is the capacity of an organism to withstand relatively extreme temperatures, is influenced by the response during stress exposure, as well as the recovery process afterwards. While heat-shock response mechanisms have been studied intensively, predicting thermal tolerance remains a challenge.Results: Here, we use the nematode Caenorhabditis elegans to measure transcriptional resilience to heat stress and predict thermotolerance. Using principal component analysis in combination with genome-wide gene expression profiles collected in three high-resolution time series during control, heat stress, and recovery conditions, we infer a quantitative scale capturing the extent of stress-induced transcriptome dynamics in a single value. This scale provides a basis for evaluating transcriptome resilience, defined here as the ability to depart from stress-expression dynamics during recovery. Independent replication across multiple highly divergent genotypes reveals that the transcriptional resilience parameter measured after a spike in temperature is quantitatively linked to long-term survival after heat stress.Conclusion: Our findings imply that thermotolerance is an intrinsic property that pre-determines long-term outcome of stress and can be predicted by the transcriptional resilience parameter. Inferring the transcriptional resilience parameters of higher organisms could aid in evaluating rehabilitation strategies after stresses such as disease and trauma.

U2 - 10.1186/s12915-019-0725-6

DO - 10.1186/s12915-019-0725-6

M3 - Article

VL - 17

JO - BMC Biology

JF - BMC Biology

SN - 1741-7007

IS - 1

M1 - 102

ER -