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 |
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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 fullname: Healy, Timothy M. email: healy@zoology.ubc.ca organization: Department of Zoology, The University of British Columbia – sequence: 2 givenname: Dillon J. surname: Chung fullname: Chung, Dillon J. organization: Department of Zoology, The University of British Columbia – sequence: 3 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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Keywords | Fish Oxygen consumption Temperature Mitochondria Mitochondrial biogenesis Gene expression |
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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 |
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