Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii

Abstract Extreme environmental conditions at high altitude, such as hypobaric hypoxia, low temperature, and strong UV radiation, pose a great challenge to the survival of animals. Although the mechanisms of adaptation to high-altitude environments have attracted much attention for native plateau spe...

Full description

Bibliographic Details
Main Authors: Xuejing Zhang, Shengkang Men, Lun Jia, Xiaolong Tang, Kenneth B. Storey, Yonggang Niu, Qiang Chen
Format: Article
Language:English
Published: BMC 2023-11-01
Series:Frontiers in Zoology
Subjects:
Online Access:https://doi.org/10.1186/s12983-023-00513-z
_version_ 1827770380737052672
author Xuejing Zhang
Shengkang Men
Lun Jia
Xiaolong Tang
Kenneth B. Storey
Yonggang Niu
Qiang Chen
author_facet Xuejing Zhang
Shengkang Men
Lun Jia
Xiaolong Tang
Kenneth B. Storey
Yonggang Niu
Qiang Chen
author_sort Xuejing Zhang
collection DOAJ
description Abstract Extreme environmental conditions at high altitude, such as hypobaric hypoxia, low temperature, and strong UV radiation, pose a great challenge to the survival of animals. Although the mechanisms of adaptation to high-altitude environments have attracted much attention for native plateau species, the underlying metabolic regulation remains unclear. Here, we used a multi-platform metabolomic analysis to compare metabolic profiles of liver between high- and low-altitude populations of toad-headed lizards, Phrynocephalus vlangalii, from the Qinghai–Tibet Plateau. A total of 191 differential metabolites were identified, consisting of 108 up-regulated and 83 down-regulated metabolites in high-altitude lizards as compared with values for low-altitude lizards. Pathway analysis revealed that the significantly different metabolites were associated with carbohydrate metabolism, amino acid metabolism, purine metabolism, and glycerolipid metabolism. Most intermediary metabolites of glycolysis and the tricarboxylic acid cycle were not significantly altered between the two altitudes, but most free fatty acids as well as β-hydroxybutyric acid were significantly lower in the high-altitude population. This may suggest that high-altitude lizards rely more on carbohydrates as their main energy fuel rather than lipids. Higher levels of phospholipids occurred in the liver of high-altitude populations, suggesting that membrane lipids may undergo adaptive remodeling in response to low-temperature stress at high altitude. In summary, this study demonstrates that metabolic profiles differ substantially between high- and low-altitude lizard populations, and that these differential metabolites and metabolic pathways can provide new insights to reveal mechanisms of adaptation to extreme environments at high altitude.
first_indexed 2024-03-11T12:38:46Z
format Article
id doaj.art-8009270f4f454b03aa02681a7393b9fd
institution Directory Open Access Journal
issn 1742-9994
language English
last_indexed 2024-03-11T12:38:46Z
publishDate 2023-11-01
publisher BMC
record_format Article
series Frontiers in Zoology
spelling doaj.art-8009270f4f454b03aa02681a7393b9fd2023-11-05T12:25:29ZengBMCFrontiers in Zoology1742-99942023-11-0120111210.1186/s12983-023-00513-zComparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangaliiXuejing Zhang0Shengkang Men1Lun Jia2Xiaolong Tang3Kenneth B. Storey4Yonggang Niu5Qiang Chen6School of Life Sciences, Lanzhou UniversitySchool of Life Sciences, Lanzhou UniversitySchool of Life Sciences, Lanzhou UniversitySchool of Life Sciences, Lanzhou UniversityDepartment of Biology, Carleton UniversityDepartment of Life Sciences, Dezhou UniversitySchool of Life Sciences, Lanzhou UniversityAbstract Extreme environmental conditions at high altitude, such as hypobaric hypoxia, low temperature, and strong UV radiation, pose a great challenge to the survival of animals. Although the mechanisms of adaptation to high-altitude environments have attracted much attention for native plateau species, the underlying metabolic regulation remains unclear. Here, we used a multi-platform metabolomic analysis to compare metabolic profiles of liver between high- and low-altitude populations of toad-headed lizards, Phrynocephalus vlangalii, from the Qinghai–Tibet Plateau. A total of 191 differential metabolites were identified, consisting of 108 up-regulated and 83 down-regulated metabolites in high-altitude lizards as compared with values for low-altitude lizards. Pathway analysis revealed that the significantly different metabolites were associated with carbohydrate metabolism, amino acid metabolism, purine metabolism, and glycerolipid metabolism. Most intermediary metabolites of glycolysis and the tricarboxylic acid cycle were not significantly altered between the two altitudes, but most free fatty acids as well as β-hydroxybutyric acid were significantly lower in the high-altitude population. This may suggest that high-altitude lizards rely more on carbohydrates as their main energy fuel rather than lipids. Higher levels of phospholipids occurred in the liver of high-altitude populations, suggesting that membrane lipids may undergo adaptive remodeling in response to low-temperature stress at high altitude. In summary, this study demonstrates that metabolic profiles differ substantially between high- and low-altitude lizard populations, and that these differential metabolites and metabolic pathways can provide new insights to reveal mechanisms of adaptation to extreme environments at high altitude.https://doi.org/10.1186/s12983-023-00513-zHigh altitudeMetabolomicsAdaptationPhrynocephalus vlangalii
spellingShingle Xuejing Zhang
Shengkang Men
Lun Jia
Xiaolong Tang
Kenneth B. Storey
Yonggang Niu
Qiang Chen
Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii
Frontiers in Zoology
High altitude
Metabolomics
Adaptation
Phrynocephalus vlangalii
title Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii
title_full Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii
title_fullStr Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii
title_full_unstemmed Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii
title_short Comparative metabolomics analysis reveals high-altitude adaptations in a toad-headed viviparous lizard, Phrynocephalus vlangalii
title_sort comparative metabolomics analysis reveals high altitude adaptations in a toad headed viviparous lizard phrynocephalus vlangalii
topic High altitude
Metabolomics
Adaptation
Phrynocephalus vlangalii
url https://doi.org/10.1186/s12983-023-00513-z
work_keys_str_mv AT xuejingzhang comparativemetabolomicsanalysisrevealshighaltitudeadaptationsinatoadheadedviviparouslizardphrynocephalusvlangalii
AT shengkangmen comparativemetabolomicsanalysisrevealshighaltitudeadaptationsinatoadheadedviviparouslizardphrynocephalusvlangalii
AT lunjia comparativemetabolomicsanalysisrevealshighaltitudeadaptationsinatoadheadedviviparouslizardphrynocephalusvlangalii
AT xiaolongtang comparativemetabolomicsanalysisrevealshighaltitudeadaptationsinatoadheadedviviparouslizardphrynocephalusvlangalii
AT kennethbstorey comparativemetabolomicsanalysisrevealshighaltitudeadaptationsinatoadheadedviviparouslizardphrynocephalusvlangalii
AT yonggangniu comparativemetabolomicsanalysisrevealshighaltitudeadaptationsinatoadheadedviviparouslizardphrynocephalusvlangalii
AT qiangchen comparativemetabolomicsanalysisrevealshighaltitudeadaptationsinatoadheadedviviparouslizardphrynocephalusvlangalii