Marc Arderiu Romero , Manon Guille-Collignon , Benjamin Bailleul , Frédéric Lemaître
{"title":"Analytical fingerprint of the interactions between quinones and bioenergetic membranes in Chlamydomonas reinhardtii","authors":"Marc Arderiu Romero , Manon Guille-Collignon , Benjamin Bailleul , Frédéric Lemaître","doi":"10.1016/j.electacta.2024.144597","DOIUrl":null,"url":null,"abstract":"<div><p>The use of intact photosynthetic organisms (e.g. microalgae or cyanobacteria) for biotechnological approaches is a promising avenue to extract sustainable energy from oxygenic photosynthesis. More particularly, exogenous quinones can act as electron shuttles to reroute part of the photosynthetic electron flow of living cells to an outer collecting electrode. This encouraging approach is however hampered by reported poisoning or side-effects of exogenous quinones on the cell bioenergetics. In order to contribute to understand those effects, we investigated the modes and sites of interaction of two model quinones (2,6-DCBQ and 2,6-DMBQ) with the respiratory and photosynthetic electron transfer chains of the green alga <em>Chlamydomonas reinhardtii</em>. By considering different analytical tools (chlorophyll <em>a</em> fluorescence, transient absorption spectrometry, O<sub>2</sub> consumption rate), the two exogenous quinones are shown to hamper the photosynthetic electron transfer from photosystem II (PSII) to the cytochrome <em>b</em><sub>6</sub><em>f</em> and, at longer term, PSII damage. In addition, the investigated quinones initiate the suppression of mitochondrial respiration, illustrated by the decrease of O<sub>2</sub> consumption. This results in the diminution of the ATP exchanges between mitochondrion and chloroplast responsible for the generation of the proton motive force across the thylakoid in darkness, and in turn affects the performances of the CF1FO ATPase. For all those effects, 2,6-DCBQ was more effective than 2,6-DMBQ in agreement with its higher redox potential and partition coefficient values. This work provides a new framework for the study of biophotovoltaic devices using photosynthetic organisms and quinones as mediators and could be extended to find the best candidates combining efficient bioelectricity production and limited toxicity.</p></div>","PeriodicalId":305,"journal":{"name":"Electrochimica Acta","volume":null,"pages":null},"PeriodicalIF":5.5000,"publicationDate":"2024-06-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Electrochimica Acta","FirstCategoryId":"88","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0013468624008375","RegionNum":3,"RegionCategory":"材料科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ELECTROCHEMISTRY","Score":null,"Total":0}
引用次数: 0
Abstract
The use of intact photosynthetic organisms (e.g. microalgae or cyanobacteria) for biotechnological approaches is a promising avenue to extract sustainable energy from oxygenic photosynthesis. More particularly, exogenous quinones can act as electron shuttles to reroute part of the photosynthetic electron flow of living cells to an outer collecting electrode. This encouraging approach is however hampered by reported poisoning or side-effects of exogenous quinones on the cell bioenergetics. In order to contribute to understand those effects, we investigated the modes and sites of interaction of two model quinones (2,6-DCBQ and 2,6-DMBQ) with the respiratory and photosynthetic electron transfer chains of the green alga Chlamydomonas reinhardtii. By considering different analytical tools (chlorophyll a fluorescence, transient absorption spectrometry, O2 consumption rate), the two exogenous quinones are shown to hamper the photosynthetic electron transfer from photosystem II (PSII) to the cytochrome b6f and, at longer term, PSII damage. In addition, the investigated quinones initiate the suppression of mitochondrial respiration, illustrated by the decrease of O2 consumption. This results in the diminution of the ATP exchanges between mitochondrion and chloroplast responsible for the generation of the proton motive force across the thylakoid in darkness, and in turn affects the performances of the CF1FO ATPase. For all those effects, 2,6-DCBQ was more effective than 2,6-DMBQ in agreement with its higher redox potential and partition coefficient values. This work provides a new framework for the study of biophotovoltaic devices using photosynthetic organisms and quinones as mediators and could be extended to find the best candidates combining efficient bioelectricity production and limited toxicity.
利用完整的光合生物(如微藻或蓝藻)进行生物技术研究,是从含氧光合作用中提取可持续能源的一条大有可为的途径。特别是,外源醌可以作为电子穿梭器,将活细胞光合作用的部分电子流重新引向外部收集电极。然而,外源醌类化合物对细胞生物能的毒害或副作用却阻碍了这一令人鼓舞的方法。为了帮助理解这些影响,我们研究了两种模式醌(2,6-DCBQ 和 2,6-DMBQ)与绿藻类衣藻的呼吸链和光合电子传递链的相互作用模式和部位。通过采用不同的分析工具(叶绿素 a 荧光、瞬时吸收光谱、氧气消耗率),研究表明这两种外源醌会阻碍光合作用电子从光合系统 II(PSII)向细胞色素 b6f 的转移,并在较长时期内对 PSII 造成破坏。此外,所研究的醌还会抑制线粒体呼吸,表现为氧气消耗量的减少。这导致线粒体和叶绿体之间的 ATP 交换减少,而 ATP 交换负责在黑暗条件下产生质子动力穿过类囊体,进而影响 CF1FO ATP 酶的性能。在所有这些影响中,2,6-DCBQ 比 2,6-DMBQ 更有效,这与其较高的氧化还原电位和分配系数值一致。这项工作为研究以光合生物和醌类化合物为媒介的生物光电设备提供了一个新的框架,并可扩展到寻找兼具高效生物发电和有限毒性的最佳候选物质。
期刊介绍:
Electrochimica Acta is an international journal. It is intended for the publication of both original work and reviews in the field of electrochemistry. Electrochemistry should be interpreted to mean any of the research fields covered by the Divisions of the International Society of Electrochemistry listed below, as well as emerging scientific domains covered by ISE New Topics Committee.