Metabolic and regulatory responses involved in cold acclimation in Atlantic killifish, Fundulus heteroclitus

Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [ V V (mit,f)]. In fish, higher V V (mit,f) is typically associated with increased expression of nuclear respiratory factor 1 (Nrf1), a transcription factor that induces...

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Published in:Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology Vol. 187; no. 3; pp. 463 - 475
Main Authors: Healy, Timothy M., Chung, Dillon J., Crowther, Kyle G., Schulte, Patricia M.
Format: Journal Article
Language:English
Published: Berlin/Heidelberg Springer Berlin Heidelberg 01-04-2017
Springer Nature B.V
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Abstract Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [ V V (mit,f)]. In fish, higher V V (mit,f) is typically associated with increased expression of nuclear respiratory factor 1 (Nrf1), a transcription factor that induces expression of nuclear-encoded respiratory genes. To examine if nrf1 expression or the expression of other genes that regulate mitochondrial biogenesis contribute to changes in whole-organism metabolic rate during cold acclimation, we examined the time course of changes in the expression of these genes and in metabolic rate in Atlantic killifish, Fundulus heteroclitus . Cold acclimation rapidly decreased metabolic rate, but increased the expression of nrf1 more gradually, with a time course that depended on how rapidly the fish were transitioned to low temperature. Cold-induced nrf1 expression was not associated with increases in biochemical indicators of mitochondrial respiratory capacity, suggesting that cold-induced mitochondrial biogenesis may occur without increases in oxidative capacity in this species. These observations imply that changes in nrf1 expression and metabolic rate due to cold acclimation occur through different physiological mechanisms, and that increases in V V (mit,f) are likely not directly related to changes in metabolic rate with cold acclimation in this species. However, nrf1 expression differed between northern and southern killifish subspecies regardless of acclimation temperature, consistent with observed differences in metabolic rate and V V (mit,f) at 5 °C between these subspecies. Taken together, these results reveal substantial complexity in the regulation of V V (mit,f) and mitochondrial capacity with temperature in fish and the relationship of these parameters to metabolic rate.
AbstractList Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [V (mit,f)]. In fish, higher V (mit,f) is typically associated with increased expression of nuclear respiratory factor 1 (Nrf1), a transcription factor that induces expression of nuclear-encoded respiratory genes. To examine if nrf1 expression or the expression of other genes that regulate mitochondrial biogenesis contribute to changes in whole-organism metabolic rate during cold acclimation, we examined the time course of changes in the expression of these genes and in metabolic rate in Atlantic killifish, Fundulus heteroclitus. Cold acclimation rapidly decreased metabolic rate, but increased the expression of nrf1 more gradually, with a time course that depended on how rapidly the fish were transitioned to low temperature. Cold-induced nrf1 expression was not associated with increases in biochemical indicators of mitochondrial respiratory capacity, suggesting that cold-induced mitochondrial biogenesis may occur without increases in oxidative capacity in this species. These observations imply that changes in nrf1 expression and metabolic rate due to cold acclimation occur through different physiological mechanisms, and that increases in V (mit,f) are likely not directly related to changes in metabolic rate with cold acclimation in this species. However, nrf1 expression differed between northern and southern killifish subspecies regardless of acclimation temperature, consistent with observed differences in metabolic rate and V (mit,f) at 5 °C between these subspecies. Taken together, these results reveal substantial complexity in the regulation of V (mit,f) and mitochondrial capacity with temperature in fish and the relationship of these parameters to metabolic rate.
Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [V V(mit,f)]. In fish, higher V V(mit,f) is typically associated with increased expression of nuclear respiratory factor 1 (Nrf1), a transcription factor that induces expression of nuclear-encoded respiratory genes. To examine if nrf1 expression or the expression of other genes that regulate mitochondrial biogenesis contribute to changes in whole-organism metabolic rate during cold acclimation, we examined the time course of changes in the expression of these genes and in metabolic rate in Atlantic killifish, Fundulus heteroclitus. Cold acclimation rapidly decreased metabolic rate, but increased the expression of nrf1 more gradually, with a time course that depended on how rapidly the fish were transitioned to low temperature. Cold-induced nrf1 expression was not associated with increases in biochemical indicators of mitochondrial respiratory capacity, suggesting that cold-induced mitochondrial biogenesis may occur without increases in oxidative capacity in this species. These observations imply that changes in nrf1 expression and metabolic rate due to cold acclimation occur through different physiological mechanisms, and that increases in V V(mit,f) are likely not directly related to changes in metabolic rate with cold acclimation in this species. However, nrf1 expression differed between northern and southern killifish subspecies regardless of acclimation temperature, consistent with observed differences in metabolic rate and V V(mit,f) at 5 °C between these subspecies. Taken together, these results reveal substantial complexity in the regulation of V V(mit,f) and mitochondrial capacity with temperature in fish and the relationship of these parameters to metabolic rate.
Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [ V V (mit,f)]. In fish, higher V V (mit,f) is typically associated with increased expression of nuclear respiratory factor 1 (Nrf1), a transcription factor that induces expression of nuclear-encoded respiratory genes. To examine if nrf1 expression or the expression of other genes that regulate mitochondrial biogenesis contribute to changes in whole-organism metabolic rate during cold acclimation, we examined the time course of changes in the expression of these genes and in metabolic rate in Atlantic killifish, Fundulus heteroclitus . Cold acclimation rapidly decreased metabolic rate, but increased the expression of nrf1 more gradually, with a time course that depended on how rapidly the fish were transitioned to low temperature. Cold-induced nrf1 expression was not associated with increases in biochemical indicators of mitochondrial respiratory capacity, suggesting that cold-induced mitochondrial biogenesis may occur without increases in oxidative capacity in this species. These observations imply that changes in nrf1 expression and metabolic rate due to cold acclimation occur through different physiological mechanisms, and that increases in V V (mit,f) are likely not directly related to changes in metabolic rate with cold acclimation in this species. However, nrf1 expression differed between northern and southern killifish subspecies regardless of acclimation temperature, consistent with observed differences in metabolic rate and V V (mit,f) at 5 °C between these subspecies. Taken together, these results reveal substantial complexity in the regulation of V V (mit,f) and mitochondrial capacity with temperature in fish and the relationship of these parameters to metabolic rate.
Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [V sub(V)(mit,f)]. In fish, higher V sub(V)(mit,f) is typically associated with increased expression of nuclear respiratory factor 1 (Nrf1), a transcription factor that induces expression of nuclear-encoded respiratory genes. To examine if nrf1 expression or the expression of other genes that regulate mitochondrial biogenesis contribute to changes in whole-organism metabolic rate during cold acclimation, we examined the time course of changes in the expression of these genes and in metabolic rate in Atlantic killifish, Fundulus heteroclitus. Cold acclimation rapidly decreased metabolic rate, but increased the expression of nrf1 more gradually, with a time course that depended on how rapidly the fish were transitioned to low temperature. Cold-induced nrf1 expression was not associated with increases in biochemical indicators of mitochondrial respiratory capacity, suggesting that cold-induced mitochondrial biogenesis may occur without increases in oxidative capacity in this species. These observations imply that changes in nrf1 expression and metabolic rate due to cold acclimation occur through different physiological mechanisms, and that increases in V sub(V)(mit,f) are likely not directly related to changes in metabolic rate with cold acclimation in this species. However, nrf1 expression differed between northern and southern killifish subspecies regardless of acclimation temperature, consistent with observed differences in metabolic rate and V sub(V)(mit,f) at 5 degree C between these subspecies. Taken together, these results reveal substantial complexity in the regulation of V sub(V)(mit,f) and mitochondrial capacity with temperature in fish and the relationship of these parameters to metabolic rate.
Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [V V(mit,f)]. In fish, higher V V(mit,f) is typically associated with increased expression of nuclear respiratory factor 1 (Nrf1), a transcription factor that induces expression of nuclear-encoded respiratory genes. To examine if nrf1 expression or the expression of other genes that regulate mitochondrial biogenesis contribute to changes in whole-organism metabolic rate during cold acclimation, we examined the time course of changes in the expression of these genes and in metabolic rate in Atlantic killifish, Fundulus heteroclitus. Cold acclimation rapidly decreased metabolic rate, but increased the expression of nrf1 more gradually, with a time course that depended on how rapidly the fish were transitioned to low temperature. Cold-induced nrf1 expression was not associated with increases in biochemical indicators of mitochondrial respiratory capacity, suggesting that cold-induced mitochondrial biogenesis may occur without increases in oxidative capacity in this species. These observations imply that changes in nrf1 expression and metabolic rate due to cold acclimation occur through different physiological mechanisms, and that increases in V V(mit,f) are likely not directly related to changes in metabolic rate with cold acclimation in this species. However, nrf1 expression differed between northern and southern killifish subspecies regardless of acclimation temperature, consistent with observed differences in metabolic rate and V V(mit,f) at 5 °C between these subspecies. Taken together, these results reveal substantial complexity in the regulation of V V(mit,f) and mitochondrial capacity with temperature in fish and the relationship of these parameters to metabolic rate.
Author Crowther, Kyle G.
Schulte, Patricia M.
Healy, Timothy M.
Chung, Dillon J.
Author_xml – sequence: 1
  givenname: Timothy M.
  surname: Healy
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  givenname: Dillon J.
  surname: Chung
  fullname: Chung, Dillon J.
  organization: Department of Zoology, The University of British Columbia
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  givenname: Kyle G.
  surname: Crowther
  fullname: Crowther, Kyle G.
  organization: Department of Zoology, The University of British Columbia
– sequence: 4
  givenname: Patricia M.
  surname: Schulte
  fullname: Schulte, Patricia M.
  organization: Department of Zoology, The University of British Columbia
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27787665$$D View this record in MEDLINE/PubMed
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IsPeerReviewed true
IsScholarly true
Issue 3
Keywords Fish
Oxygen consumption
Temperature
Mitochondria
Mitochondrial biogenesis
Gene expression
Language English
LinkModel DirectLink
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Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
PMID 27787665
PQID 1878051129
PQPubID 54170
PageCount 13
ParticipantIDs proquest_miscellaneous_1888965139
proquest_miscellaneous_1835691083
proquest_journals_1878051129
crossref_primary_10_1007_s00360_016_1042_9
pubmed_primary_27787665
springer_journals_10_1007_s00360_016_1042_9
PublicationCentury 2000
PublicationDate 2017-04-01
PublicationDateYYYYMMDD 2017-04-01
PublicationDate_xml – month: 04
  year: 2017
  text: 2017-04-01
  day: 01
PublicationDecade 2010
PublicationPlace Berlin/Heidelberg
PublicationPlace_xml – name: Berlin/Heidelberg
– name: Germany
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PublicationSubtitle Biochemical, Systems, and Environmental Physiology
PublicationTitle Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology
PublicationTitleAbbrev J Comp Physiol B
PublicationTitleAlternate J Comp Physiol B
PublicationYear 2017
Publisher Springer Berlin Heidelberg
Springer Nature B.V
Publisher_xml – name: Springer Berlin Heidelberg
– name: Springer Nature B.V
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Snippet Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [ V V (mit,f)]. In fish,...
Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [V (mit,f)]. In fish, higher...
Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [V V(mit,f)]. In fish,...
Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [V sub(V)(mit,f)]. In fish,...
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SubjectTerms Acclimatization
Acclimatization - physiology
Animal Physiology
Animals
Biochemistry
Biomedical and Life Sciences
Biomedicine
Biosynthesis
Citrate (si)-Synthase - metabolism
Cold Temperature
Cytochrome
Fish Proteins - genetics
Fish Proteins - metabolism
Freshwater
Fundulidae - physiology
Fundulus heteroclitus
Gene Expression
Human Physiology
Life Sciences
Low temperature
Marine
Metabolism
Mitochondria, Muscle - metabolism
Muscles - metabolism
Nuclear Respiratory Factor 1 - genetics
Original Paper
Oxygen Consumption
Temperature
Zoology
Title Metabolic and regulatory responses involved in cold acclimation in Atlantic killifish, Fundulus heteroclitus
URI https://link.springer.com/article/10.1007/s00360-016-1042-9
https://www.ncbi.nlm.nih.gov/pubmed/27787665
https://www.proquest.com/docview/1878051129
https://search.proquest.com/docview/1835691083
https://search.proquest.com/docview/1888965139
Volume 187
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