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 They must generate a bubble in their tracheal fluid by cavitation, and then expand its volume as the fluid is withdrawn.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%。尽管它们是一个原始的呼吸空气的物种，但来自11个目的物种在青少年时期独立地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一个谜。我的研究计划的长期目标是揭示昆虫如何感知和调节它们的气体交换，以应对缺氧、高二氧化碳和酸碱平衡，并了解它们的气体交换系统是如何进化出来的，在一系列具有挑战性的呼吸环境中发挥作用。这里提出的这项研究通过确定1)昆虫在哪里以及如何感知内部O2和CO2的水平，以及2)它们如何从气管系统中清除液体并在刚孵化时将其替换为空气，来解决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背后的机制。水生蜻蜓若虫表现出清晰的呼吸节律，使我们能够通过测量局部刺激对通风的影响来定位对O2和CO2敏感的神经元。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。发育中的陆栖昆虫可以通过开放的气孔将空气吸入它们的气管系统，因为气管液体被吸入它们的血液中，但水生昆虫在水下孵化，拥有一个封闭的气管系统。他们必须通过空化在他们的气管液体中产生一个气泡，然后随着液体的抽出而扩大其体积。我们的目标是揭示这是如何发生的。渗透作用可以驱动空化和液体去除，而二氧化碳的产生可以支持气泡的膨胀。离子传输必须是这两个过程的基础，所以使用药物选择性地抑制离子泵将显示涉及的传输路径。操纵静水压力以在发育中的昆虫中引发或抑制空化，将揭示由气管系统产生的渗透压力和气体压力的大小。我们还将通过研究一种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属的水生幼虫已经将它们的气管系统改造成一个流体静压器官，由四个充满空气的囊组成。我们已经发现，幼虫不会将气体输送到囊中来调节浮力。相反，它们改变了囊壁中Resilin蛋白条带的pH值，这些条带的反应是膨胀和收缩，从而改变了囊的体积。了解这一系统将揭示祖先的气管机械是如何被修改以产生这一惊人的进化创新的。这个项目的所有组成部分都将改写我们对昆虫呼吸系统功能的理解。