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Fuel source shift or cost reduction: Context-dependent adaptation strategies in closely related Neodon fuscus and Lasiopodomys brandtii against hypoxia

Xiu-Juan Li Cong-Cong Qiao Bo-Jian Chen Meng-Yang Li Peng Chen Mao-Lin Huang Chun-Xiao Chen Yan Liu Han Cheng Meng-Wan Jiang Lu-Ye Shi Zhen-Long Wang

Xiu-Juan Li, Cong-Cong Qiao, Bo-Jian Chen, Meng-Yang Li, Peng Chen, Mao-Lin Huang, Chun-Xiao Chen, Yan Liu, Han Cheng, Meng-Wan Jiang, Lu-Ye Shi, Zhen-Long Wang. Fuel source shift or cost reduction: Context-dependent adaptation strategies in closely related Neodon fuscus and Lasiopodomys brandtii against hypoxia. Zoological Research, 2022, 43(4): 497-513. doi: 10.24272/j.issn.2095-8137.2022.011
Citation: Xiu-Juan Li, Cong-Cong Qiao, Bo-Jian Chen, Meng-Yang Li, Peng Chen, Mao-Lin Huang, Chun-Xiao Chen, Yan Liu, Han Cheng, Meng-Wan Jiang, Lu-Ye Shi, Zhen-Long Wang. Fuel source shift or cost reduction: Context-dependent adaptation strategies in closely related Neodon fuscus and Lasiopodomys brandtii against hypoxia. Zoological Research, 2022, 43(4): 497-513. doi: 10.24272/j.issn.2095-8137.2022.011

供能来源转换或降低能量消耗:青海田鼠与布氏田鼠低氧下的适应策略比较研究

doi: 10.24272/j.issn.2095-8137.2022.011

Fuel source shift or cost reduction: Context-dependent adaptation strategies in closely related Neodon fuscus and Lasiopodomys brandtii against hypoxia

Funds: This work was supported by the National Natural Science Foundation of China (U2004152), Zhongyuan Science and Technology Innovation Leading Talent Project (224200510001), and China Postdoctoral Science Foundation (2020M672264)
More Information
  • 摘要: 氧气对于大多数生物来说都是必不可少的。氧气供应不足会破坏机体平衡甚至危及生命,缺氧引起的心血管衰竭对包括人类在内的许多动物来说都是致命的。值得注意的是,自然界中的一些生物已经适应了低氧环境,这使它们成为研究低氧环境下心血管系统调控机制的良好模型。青海田鼠(Neodon fuscus)由于长期生活于高海拔环境中而适应低氧,而其近缘物种布氏田鼠(Lasiopodomys brandtii)则经历由洞道集群带来的间歇性低氧环境。为了探讨不同生活史低氧适应物种心血管系统的应对机制,该研究以昆明小鼠(Mus musculus)作为对照,比较了青海田鼠和布氏田鼠在低氧(10% O2,48 h)和常氧(20.9% O2,48 h)条件下心血管系统的生理和分子响应机制。通过组织学和血液学分析发现,青海田鼠和布氏田鼠对低氧具有较强的耐受性,而暴露于低氧环境下的昆明小鼠心肌组织明显损伤,血液循环阻力增加。另一方面,比较转录组学分析发现,青海田鼠和布氏田鼠在低氧环境下的氧运输能力有所提高,但存在一定的策略差异。具体来说,在暴露于低氧环境时,青海田鼠上调了与心脏收缩和血管生成相关的基因,而布氏田鼠上调了与红细胞生成相关的基因。相同的是,这两个物种都上调了与血红蛋白合成相关的基因。此外,我们还发现了两种田鼠在低氧环境下心脏代谢策略的差异:青海田鼠心脏的能量供应发生了由脂肪酸氧化到葡萄糖氧化的转变,从而实现更高效的氧气利用;而布氏田鼠同时降低了脂肪酸氧化、葡萄糖氧化和心率,采用了较为保守的方式应对低氧。综上所述,这些研究结果表明了青海田鼠和布氏田鼠的心血管系统已经进化出不同的适应策略,以帮助它们在低氧条件下增强氧气运输和保存能量。
    #Authors contributed equally to this work
  • Figure  1.  Changes in heart tissue morphology, collagen fiber content, and erythrocyte system before and after hypoxia treatment

    A–F: H&E staining of N. fuscus (A, D), L. brandtii (B, E), and M. musculus hearts (C, F). Heart tissue morphology of three species under normoxia (A, B, C) and hypoxia (D, E, F). 200× magnification. G: Changes in collagen fiber content (%) in N. fuscus, L. brandtii, and M. musculus hearts in response to normoxia and hypoxia. H–J: Erythrocyte system parameters in N. fuscus (H), L. brandtii (I), and M. musculus (J) under normoxic and hypoxic conditions. RBC, red blood cells (1012/L); HGB, hemoglobin (g/L); HCT, hematocrit (%); MCV, mean corpuscular volume (fL); MCH, mean red blood cell hemoglobin (pg); MCHC, mean red blood cell hemoglobin concentration (g/L); RDW, red blood cell distribution width (%). *: P<0.05; **: P<0.01.

    Figure  2.  GO enrichment, KEGG enrichment, and PPI results for up-regulated and down-regulated DEGs in N. fuscus

    A, B: Different colors represent number of genes significantly enriched in GO terms (see color key) and font size represents P-value significance level (larger font indicates smaller P). Top 30 significantly enriched GO terms in up-regulated DEGs are shown in Figure A, and all significantly enriched GO terms are presented in Supplementary Table S7. C, D: Different-colored circles represent different biological classifications (see color key) and numbers in circles represent number of genes significantly enriched in KEGG pathways. E: Red and blue circles represent proteins encoded by up-regulated and down-regulated DEGs, respectively. Circle size represents number of other proteins in network that interact with that protein, with larger circles indicating greater number of proteins interacting with protein in question. Thickness of line connecting circles indicates strength of interaction between two proteins, with wider lines indicating stronger interaction.

    Figure  3.  GO enrichment, KEGG enrichment, and PPI results for up-regulated and down-regulated DEGs in L. brandtii

    A, B: Different colors represent number of genes significantly enriched in GO terms (see color key) and font size represents P-value significance level (larger font indicates smaller P). C, D: Different-colored circles represent different biological classifications (see color key) and numbers in circles represent number of genes significantly enriched in KEGG pathways. E: Red and blue circles represent proteins encoded by up-regulated and down-regulated DEGs, respectively. Circle size represents number of other proteins in network that interact with that protein, with larger circles indicating greater number of proteins that interact with protein in question. Thickness of line connecting circles indicates strength of interaction between two proteins, with wider lines indicating stronger interaction.

    Figure  4.  GO enrichment, KEGG enrichment, and PPI results for up-regulated and down-regulated DEGs in M. musculus

    A, B: Different colors represent number of genes significantly enriched in GO terms (see color key) and font size represents P-value significance level (larger font indicates smaller P). C, D: Different-colored circles represent different biological classifications (see color key) and numbers in circles represent number of genes significantly enriched in KEGG pathways. E: Red and blue circles represent proteins encoded by up-regulated and down-regulated DEGs, respectively. Circle size represents number of other proteins in network that interact with that protein, with larger circles indicating greater number of proteins that interact with protein in question. Thickness of line connecting circles indicates strength of interaction between two proteins, with wider lines indicating stronger interaction.

    Figure  5.  Gene expression levels measured by qRT-PCR and RNA-seq methods

    A, B: Relative expression levels of Hba (A) and Alas2 (B) in N. fuscus, L. brandtii, and M. musculus. C–F: Gene expression trends (C) and correlations (D–F) of six genes between qRT-PCR and RNA-seq in N. fuscus, L. brandtii, and M. musculus.

    Figure  6.  Dynamic deduction of oxygen transport regulation in N. fuscus and L. brandtii under hypoxic conditions

    Figure  7.  Cardiac energy metabolism pathways activated under hypoxic environments

    A: N. fuscus. B: L. brandtii. C: M. musculus. Black arrow represents direction of biochemical reaction, and gene names in red and blue italics represent up-regulated and down-regulated DEGs, respectively.

    Table  1.   Transcriptome assembly metrics and assessment results in N. fuscus, L. brandtii, and M. musculus

    Assembly metricN. fuscusL. brandtiiM. musculus
    Total number of Trinity transcripts (n)528 549471 494471 657
    Total assembled bases of transcripts (bp)453 677 736415 739 886407 973 875
    Mean length of transcripts (bp)858.35881.75864.98
    N50 of transcripts (bp)2 4832 5662 530
    GC content of transcripts (%)47.6947.8247.80
    Mapping rate to transcripts (%)92.54–93.7892.61–93.5592.16–93.81
    Total number of unigenes (n)153 192132 299137 036
    Total assembled bases of unigenes (bp)168 920 719152 170 285152 428 218
    Mean length of unigenes (bp)1 102.671 150.201 112.32
    N50 of unigenes (bp)1 7481 9151 847
    GC content of unigenes (%)46.9047.1247.07
    Mapping rate to unigenes (%)88.36–90.1988.61–89.3387.09–88.84
    BUSCO completeness of unigenes (%)80.479.280.8
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  • 收稿日期:  2022-03-07
  • 录用日期:  2022-05-05
  • 网络出版日期:  2022-05-11
  • 刊出日期:  2022-07-18

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