Gas exchange in water and air: Revealing fundamental mechanisms underlying the development and control of the insect respiratory system

水和空气中的气体交换：揭示昆虫呼吸系统发育和控制的基本机制

• 批准号: RGPIN-2020-07089
• 负责人: Matthews, Philip
• 金额: $ 2.91万
• 依托单位: University of British Columbia
• 依托单位国家: 加拿大
• 项目类别: Discovery Grants Program - Individual
• 财政年份: 2021
• 资助国家: 加拿大
• 起止时间: 2021-01-01 至 2022-12-31
• 项目状态: 已结题
• 来源: https://www.nserc-crsng.gc.ca/ase-oro/Details-Detailles_eng.asp?id=741587
• 关键词: Gas; exchange; water; air; Revealing

Insects are the most numerous and diverse animals on the planet, representing 80% of all known species. Although they are an ancestrally air-breathing group, species from 11 orders have independently evolved the ability to live and breathe underwater as juveniles. This impressive respiratory flexibility underlies the global success of all insects, but fundamental details of how they breathe are still a mystery. The long-term goal of my research program is to reveal how insects sense and regulate their gas exchange in response to hypoxia, hypercapnia, and acid-base balance, and to understand how their gas-exchange system has evolved to function in a range of challenging respiratory environments. The research proposed here addresses two critical gaps in our understanding of insect respiratory physiology by determining 1) where and how insects sense internal levels of O2 and CO2, and 2) how they remove fluid from their tracheal system and replace it with air when they first hatch. My research program will harness the physiological traits of aquatic insects to uncover, for the first time, the mechanisms that underlie these vital processes. Aquatic dragonfly nymphs exhibit a clear ventilatory rhythm, allowing us to locate O2 and CO2-sensitive neurons by measuring the effect of focal stimulation on ventilation. The molecular mechanisms by which these neurons sense O2 or CO2 will then be revealed by chemical stimulation and inhibition. Developing terrestrial insects can pull air into their tracheal system through open spiracles as the tracheal fluid is drawn into their blood, but aquatic insects hatch underwater and possess a closed tracheal system. They must generate a bubble in their tracheal fluid by cavitation, and then expand its volume as the fluid is withdrawn. We aim to reveal how this occurs. Osmosis could drive cavitation and fluid removal, while CO2 production could support bubble expansion. Ion transport must underlie both processes, so using drugs to selectively inhibit ion pumps will show the transport pathways involved. Manipulating hydrostatic pressure to elicit or inhibit cavitation in developing insects will reveal the magnitude of the osmotic and gas pressures generated by the tracheal system. We will also explore the evolutionary plasticity of the insect respiratory system by studying a unique buoyancy control mechanism. Aquatic larvae of the genus Chaoborus have modified their tracheal system into a hydrostatic organ, comprising four air-filled sacs. We have discovered that the larvae do not pump gas into the sacs to regulate buoyancy. Instead they change the pH of bands of resilin protein in the sac wall, which expand and contract in response, thus changing the volume of the sac. Understanding this system will reveal how the ancestral tracheal machinery has been modified to produce this striking evolutionary innovation. All components of this program will rewrite our understanding of how the insect respiratory system functions.

昆虫是地球上数量最多、种类最多的动物，占所有已知物种的 80%。尽管它们是一个祖先呼吸空气的群体，但来自 11 个目的物种在幼年时期就独立进化出了在水下生活和呼吸的能力。这种令人印象深刻的呼吸灵活性是所有昆虫在全球取得成功的基础，但它们如何呼吸的基本细节仍然是个谜。我的研究计划的长期目标是揭示昆虫如何感知和调节其气体交换以应对缺氧、高碳酸血症和酸碱平衡，并了解它们的气体交换系统如何进化以在一系列具有挑战性的呼吸环境中发挥作用。这里提出的研究通过确定 1) 昆虫在何处以及如何感知 O2 和 CO2 的内部水平，以及 2) 当它们第一次孵化时，它们如何从气管系统中去除液体并用空气代替它，从而解决了我们对昆虫呼吸生理学理解中的两个关键差距。我的研究计划将利用水生昆虫的生理特征，首次揭示这些重要过程的机制。水生蜻蜓若虫表现出清晰的通气节律，使我们能够通过测量局部刺激对通气的影响来定位 O2 和 CO2 敏感神经元。这些神经元感知 O2 或 CO2 的分子机制将通过化学刺激和抑制来揭示。发育中的陆生昆虫可以通过开放的气门将空气吸入气管系统，因为气管液体被吸入血液中，但水生昆虫在水下孵化并拥有封闭的气管系统。它们必须通过空化作用在气管液体中产生气泡，然后随着液体的排出而扩大气泡的体积。我们的目的是揭示这是如何发生的。渗透可以促进空化和流体去除，而二氧化碳的产生可以支持气泡膨胀。离子运输必须是这两个过程的基础，因此使用药物选择性抑制离子泵将显示所涉及的运输途径。操纵静水压力来引发或抑制发育中的昆虫的空化现象将揭示气管系统产生的渗透压和气体压力的大小。我们还将通过研究独特的浮力控制机制来探索昆虫呼吸系统的进化可塑性。 Chaoborus 属的水生幼虫已将其气管系统改造为静水器官，由四个充气囊组成。我们发现幼虫不会将气体泵入囊中来调节浮力。相反，它们改变了囊壁中节肢弹性蛋白带的pH值，节肢蛋白带相应地膨胀和收缩，从而改变了囊的体积。了解这个系统将揭示祖先的气管机械是如何被改造以产生这种惊人的进化创新的。该计划的所有组成部分将改写我们对昆虫呼吸系统如何运作的理解。