Global significance of light-driven proton pumps in eukaryotic marine phytoplankton

阳光是我们星球上的终极能源，从单细胞微生物到多细胞生物体，光的有效捕获和利用是一个在所有生命王国中微妙进化的过程。除了利用光作为生长的能源外，它也是环境信息的重要来源。微生物进化出了特别多样化的系统，利用光产生能量，避开恶劣的环境，并确定适合营养和生长的环境。生物体将光能转化为生长所需的化学能的代谢模式被称为光养(源自希腊语中的“light”和[trohe]中的“营养素”)。地球上为光营养提供动力的最重要的生物过程是氧合光合作用，它利用含有叶绿素色素的多亚单位蛋白质复合体，称为光系统，并产生我们呼吸的氧气。这些光系统在捕捉和利用光方面效率很高，但严重依赖铁来发挥作用。此外，第二个独立于光系统的机械上不同的过程也可以为光营养提供动力，并使用称为视紫红质的膜嵌入光感受器。视紫红质是由视蛋白膜蛋白组成的分子，它结合了视网膜色素，但与光系统不同的是，它不需要铁来发挥作用。它们的工作原理是基于它们的单一、简单的性质。与使用由多个基因编码的复杂光系统不同，视紫红素将光吸收和能量守恒的任务结合到由单个基因编码的单个蛋白质中。当吸收光时，视网膜色素的化学结构发生变化，并在分子内引发一连串的结构变化。视紫红质感受器首先在古老的原核生物(无核和膜结合细胞器的细胞)中被发现，但后来也在非常遥远的亲缘关系的细菌中被发现。海洋环境中细菌视紫红质的高度丰富表明，基于视紫红质的光营养是海洋中一个具有全球意义的微生物过程。令人惊讶的是，最近在单细胞真核生物(有核和核膜包裹遗传物质的生物体)中也发现了视紫红质，包括光合作用的海洋浮游植物。然而，真核生物视紫红质在更节能的光系统中的功能仍然令人费解。在初步研究中，我们提供了第一个实验证据，即编码视紫红质的基因在铁限制的浮游植物中高度上调。它们在铁有限的海洋中也更为丰富，这些海洋约占全球海洋表面的三分之一。这些发现为我们的研究假设提供了第一个直接的证据，即海洋浮游植物中的视紫红质为依赖铁的光合作用提供了一种以前未知的后备机制，当铁缺乏时，依赖铁的光系统可以促进化学能的产生和生长。这一新的机制特别令人感兴趣，因为最近的研究表明，由于人为二氧化碳溶解增加而导致的海洋酸化可以减少浮游植物对铁的可获得性，这可能会改变海洋中浮游植物的多样性，并有利于在铁浓度降低的情况下具有竞争优势的物种(例如，通过基于视紫红质的光营养)。在我们的研究项目中，我们将使用新的分子遗传学方法来检验我们的研究假设，并进一步探索视紫红素在全球重要的海洋浮游植物中的细胞作用和环境意义。我们的结果将为海洋浮游植物如何利用视紫红质提供基本的新见解。这将引起科学界的极大兴趣，因为浮游植物涉及许多不同的学科，从海洋和气候科学到材料科学和可再生能源。

Sunlight is the ultimate source of energy on our planet and the efficient capture and use of light is an exquisitely evolved process across all kingdoms of life, ranging from unicellular microbes to multicellular organisms. In addition to use of light as an energy source for growth, it is also an important source of environmental information. Microbes have evolved particularly diverse systems to use light to generate energy, avoid hostile environments and identify suitable environments for nutrition and growth. The metabolic mode in which organisms convert light energy into chemical energy for growth is called phototrophy (from Greek [photo-], "light" and [trophe], "nourishment"). The most important biological process on earth to power phototrophy is oxygenic photosynthesis, which employs multisubunit protein complexes containing chlorophyll pigments known as photosystems and produces the oxygen we breathe. These photosystems are highly-efficient in capturing and using light, but heavily-depend on iron to function.Additionally, a second mechanistically distinct process, which is independent from photosystems, can also power phototrophy and employs membrane-embedded photoreceptors called rhodopsins. Rhodopsins are molecules composed of opsin membrane proteins, which bind the pigment retinal but unlike photosystems do not need iron to function. Their operating principle is based on their unitary simple nature. Instead of employing complex photosystems, which are encoded by multiple genes, rhodopsins combine the tasks of light absorption and energy-conservation into a single protein encoded by a single gene. Upon absorption of light, the chemical structure of retinal pigment changes and triggers a cascade of structural changes within the molecule. Rhodopsin photoreceptors were first discovered in ancient prokaryotic (cells lacking a nucleus and membrane-bound organelles) archaebacteria, but later also in very distantly related bacteria. The high abundance of bacterial rhodopsins in marine environments has shown that rhodopsin-based phototrophy is a globally significant microbial process in the ocean. Surprisingly, rhodopsins have recently also been identified in unicellular eukaryotes (organisms with nucleus and nuclear envelope enclosing the genetic material) including photosynthetic marine phytoplankton. However, the function of eukaryotic rhodopsins in the presence of more energy-efficient photosystems remains puzzling. In a preliminary study, we provided first experimental evidence, that genes encoding for rhodopsins are highly up-regulated in iron-limited phytoplankton. They were also more abundant in iron-limited oceans, which cover about one third of the global ocean surface. These findings provide first direct evidence for our research hypothesis that rhodopsins in marine phytoplankton provide a previously unknown backup mechanism for iron-dependent chlorophyll-based photosynthesis, to enhance production of chemical energy and growth when iron is lacking for iron-dependent photosystems. This new mechanism is of particular interest, because recent research has shown that ocean acidification due to increased dissolution of anthropogenic carbon dioxide can decrease the iron availability to phytoplankton, which probably will alter phytoplankton diversity in the oceans and favor species that have a competitive advantage (e.g. by rhodopsin-based phototrophy) under reduced iron concentrations. In our research project we will use new molecular genetic methods to test our research hypothesis and further explore the cellular role and environmental significance of rhodopsins in globally important marine phytoplankton. Our results will provide fundamental new insights into how marine phytoplankton use rhodopsins. It will be of great interest to the scientific community, because phytoplankton are subject to many different disciplines, from marine and climate science to material science and renewable energy.