Oxygen conserving mitochondrial adaptations in the skeletal muscles of breath hold divers

Thomas Kjeld; Nis Stride; Anders Gudiksen; Egon Godthaab Hansen; Henrik Christian Arendrup; Peter Frederik Horstmann; Bo Zerahn; Lars Thorbjørn Jensen; Nikolai Baastrup Nordsborg; Jacob Bejder; Jens Frey Halling

doi:10.1371/journal.pone.0201401

Oxygen conserving mitochondrial adaptations in the skeletal muscles of breath hold divers

Thomas Kjeld^*, Nis Stride, Anders Gudiksen, Egon Godthaab Hansen, Henrik Christian Arendrup, Peter Frederik Horstmann, Bo Zerahn, Lars Thorbjørn Jensen, Nikolai Baastrup Nordsborg, Jacob Bejder, Jens Frey Halling

^*Corresponding author for this work

5 Citations (Scopus)

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Abstract

Background: The performance of elite breath hold divers (BHD) includes static breath hold for more than 11 minutes, swimming as far as 300 m, or going below 250 m in depth, all on a single breath of air. Diving mammals are adapted to sustain oxidative metabolism in hypoxic conditions through several metabolic adaptations, including improved capacity for oxygen transport and mitochondrial oxidative phosphorylation in skeletal muscle. It was hypothesized that similar adaptations characterized human BHD. Hence, the purpose of this study was to examine the capacity for oxidative metabolism in skeletal muscle of BHD compared to matched controls.

Methods: Biopsies were obtained from the lateral vastus of the femoral muscle from 8 Danish BHD and 8 non-diving controls (Judo athletes) matched for morphometry and whole body VO₂max. High resolution respirometry was used to determine mitochondrial respiratory capacity and leak respiration with simultaneous measurement of mitochondrial H₂O₂ emission. Maximal citrate synthase (CS) and 3-hydroxyacyl CoA dehydrogenase (HAD) activity were measured in muscle tissue homogenates. Western Blotting was used to determine protein contents of respiratory complex I-V subunits and myoglobin in muscle tissue lysates.

Results: Muscle biopsies of BHD revealed lower mitochondrial leak respiration and electron transfer system (ETS) capacity and higher H₂O₂ emission during leak respiration than controls, with no differences in enzyme activities (CS and HAD) or protein content of mitochondrial complex subunits myoglobin, myosin heavy chain isoforms, markers of glucose metabolism and antioxidant enzymes.

Conclusion: We demonstrated for the first time in humans, that the skeletal muscles of BHD are characterized by lower mitochondrial oxygen consumption both during low leak and high (ETS) respiration than matched controls. This supports previous observations of diving mammals demonstrating a lower aerobic mitochondrial capacity of the skeletal muscles as an oxygen conserving adaptation during prolonged dives.

Original language	English
Article number	e0201401
Journal	P L o S One
Volume	13
Issue number	9
Pages (from-to)	1-13
Number of pages	13
ISSN	1932-6203
DOIs	https://doi.org/10.1371/journal.pone.0201401
Publication status	Published - 19 Sept 2018

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Kjeld et al_P L o S One_2018_Vol 13(9)_e0201401Final published version, 1.47 MBLicence: CC BY

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title = "Oxygen conserving mitochondrial adaptations in the skeletal muscles of breath hold divers",

abstract = "Background: The performance of elite breath hold divers (BHD) includes static breath hold for more than 11 minutes, swimming as far as 300 m, or going below 250 m in depth, all on a single breath of air. Diving mammals are adapted to sustain oxidative metabolism in hypoxic conditions through several metabolic adaptations, including improved capacity for oxygen transport and mitochondrial oxidative phosphorylation in skeletal muscle. It was hypothesized that similar adaptations characterized human BHD. Hence, the purpose of this study was to examine the capacity for oxidative metabolism in skeletal muscle of BHD compared to matched controls. Methods: Biopsies were obtained from the lateral vastus of the femoral muscle from 8 Danish BHD and 8 non-diving controls (Judo athletes) matched for morphometry and whole body VO2max. High resolution respirometry was used to determine mitochondrial respiratory capacity and leak respiration with simultaneous measurement of mitochondrial H2O2 emission. Maximal citrate synthase (CS) and 3-hydroxyacyl CoA dehydrogenase (HAD) activity were measured in muscle tissue homogenates. Western Blotting was used to determine protein contents of respiratory complex I-V subunits and myoglobin in muscle tissue lysates. Results: Muscle biopsies of BHD revealed lower mitochondrial leak respiration and electron transfer system (ETS) capacity and higher H2O2 emission during leak respiration than controls, with no differences in enzyme activities (CS and HAD) or protein content of mitochondrial complex subunits myoglobin, myosin heavy chain isoforms, markers of glucose metabolism and antioxidant enzymes.Conclusion: We demonstrated for the first time in humans, that the skeletal muscles of BHD are characterized by lower mitochondrial oxygen consumption both during low leak and high (ETS) respiration than matched controls. This supports previous observations of diving mammals demonstrating a lower aerobic mitochondrial capacity of the skeletal muscles as an oxygen conserving adaptation during prolonged dives.",

author = "Thomas Kjeld and Nis Stride and Anders Gudiksen and Hansen, {Egon Godthaab} and Arendrup, {Henrik Christian} and Horstmann, {Peter Frederik} and Bo Zerahn and Jensen, {Lars Thorbj{\o}rn} and Nordsborg, {Nikolai Baastrup} and Jacob Bejder and Halling, {Jens Frey}",

note = "CURIS 2018 NEXS 336",

year = "2018",

month = sep,

day = "19",

doi = "10.1371/journal.pone.0201401",

language = "English",

volume = "13",

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journal = "PLoS Computational Biology",

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T1 - Oxygen conserving mitochondrial adaptations in the skeletal muscles of breath hold divers

AU - Kjeld, Thomas

AU - Stride, Nis

AU - Gudiksen, Anders

AU - Hansen, Egon Godthaab

AU - Arendrup, Henrik Christian

AU - Horstmann, Peter Frederik

AU - Zerahn, Bo

AU - Jensen, Lars Thorbjørn

AU - Nordsborg, Nikolai Baastrup

AU - Bejder, Jacob

AU - Halling, Jens Frey

N1 - CURIS 2018 NEXS 336

PY - 2018/9/19

Y1 - 2018/9/19

N2 - Background: The performance of elite breath hold divers (BHD) includes static breath hold for more than 11 minutes, swimming as far as 300 m, or going below 250 m in depth, all on a single breath of air. Diving mammals are adapted to sustain oxidative metabolism in hypoxic conditions through several metabolic adaptations, including improved capacity for oxygen transport and mitochondrial oxidative phosphorylation in skeletal muscle. It was hypothesized that similar adaptations characterized human BHD. Hence, the purpose of this study was to examine the capacity for oxidative metabolism in skeletal muscle of BHD compared to matched controls. Methods: Biopsies were obtained from the lateral vastus of the femoral muscle from 8 Danish BHD and 8 non-diving controls (Judo athletes) matched for morphometry and whole body VO2max. High resolution respirometry was used to determine mitochondrial respiratory capacity and leak respiration with simultaneous measurement of mitochondrial H2O2 emission. Maximal citrate synthase (CS) and 3-hydroxyacyl CoA dehydrogenase (HAD) activity were measured in muscle tissue homogenates. Western Blotting was used to determine protein contents of respiratory complex I-V subunits and myoglobin in muscle tissue lysates. Results: Muscle biopsies of BHD revealed lower mitochondrial leak respiration and electron transfer system (ETS) capacity and higher H2O2 emission during leak respiration than controls, with no differences in enzyme activities (CS and HAD) or protein content of mitochondrial complex subunits myoglobin, myosin heavy chain isoforms, markers of glucose metabolism and antioxidant enzymes.Conclusion: We demonstrated for the first time in humans, that the skeletal muscles of BHD are characterized by lower mitochondrial oxygen consumption both during low leak and high (ETS) respiration than matched controls. This supports previous observations of diving mammals demonstrating a lower aerobic mitochondrial capacity of the skeletal muscles as an oxygen conserving adaptation during prolonged dives.

AB - Background: The performance of elite breath hold divers (BHD) includes static breath hold for more than 11 minutes, swimming as far as 300 m, or going below 250 m in depth, all on a single breath of air. Diving mammals are adapted to sustain oxidative metabolism in hypoxic conditions through several metabolic adaptations, including improved capacity for oxygen transport and mitochondrial oxidative phosphorylation in skeletal muscle. It was hypothesized that similar adaptations characterized human BHD. Hence, the purpose of this study was to examine the capacity for oxidative metabolism in skeletal muscle of BHD compared to matched controls. Methods: Biopsies were obtained from the lateral vastus of the femoral muscle from 8 Danish BHD and 8 non-diving controls (Judo athletes) matched for morphometry and whole body VO2max. High resolution respirometry was used to determine mitochondrial respiratory capacity and leak respiration with simultaneous measurement of mitochondrial H2O2 emission. Maximal citrate synthase (CS) and 3-hydroxyacyl CoA dehydrogenase (HAD) activity were measured in muscle tissue homogenates. Western Blotting was used to determine protein contents of respiratory complex I-V subunits and myoglobin in muscle tissue lysates. Results: Muscle biopsies of BHD revealed lower mitochondrial leak respiration and electron transfer system (ETS) capacity and higher H2O2 emission during leak respiration than controls, with no differences in enzyme activities (CS and HAD) or protein content of mitochondrial complex subunits myoglobin, myosin heavy chain isoforms, markers of glucose metabolism and antioxidant enzymes.Conclusion: We demonstrated for the first time in humans, that the skeletal muscles of BHD are characterized by lower mitochondrial oxygen consumption both during low leak and high (ETS) respiration than matched controls. This supports previous observations of diving mammals demonstrating a lower aerobic mitochondrial capacity of the skeletal muscles as an oxygen conserving adaptation during prolonged dives.

U2 - 10.1371/journal.pone.0201401

DO - 10.1371/journal.pone.0201401

M3 - Journal article

C2 - 30231055

AN - SCOPUS:85053594845

SN - 1932-6203

VL - 13

SP - 1

EP - 13

JO - PLoS Computational Biology

JF - PLoS Computational Biology

IS - 9

M1 - e0201401

ER -

Oxygen conserving mitochondrial adaptations in the skeletal muscles of breath hold divers

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