Guangdong Provincial Key Laboratory of Water Quality Improvement and Ecological Restoration for Watersheds, School of Ecology, Environment and Resources, Guangdong University of Technology, Guangzhou, China.
Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China.
ISME J. 2023 May;17(5):712-719. doi: 10.1038/s41396-023-01383-3. Epub 2023 Feb 23.
Anaerobic reduction processes in natural waters can be promoted by dead microalgae that have been attributed to nutrient substances provided by the decomposition of dead microalgae for other microorganisms. However, previous reports have not considered that dead microalgae may also serve as photosensitizers to drive microbial reduction processes. Here we demonstrate a photoelectric synergistic linkage between dead microalgae and bacteria capable of extracellular electron transfer (EET). Illumination of dead Raphidocelis subcapitata resulted in two-fold increase in the rate of anaerobic bioreduction by pure Geobacter sulfurreducens, suggesting that photoelectrons generated from the illuminated dead microalgae were transferred to the EET-capable microorganisms. Similar phenomena were observed in NO reduction driven by irradiated dead Chlorella vulgaris and living Shewanella oneidensis, and Cr(VI) reduction driven by irradiated dead Raphidocelis subcapitata and living Bacillus subtilis. Enhancement of bioreduction was also seen when the killed microalgae were illuminated in mixed-culture lake water, suggesting that EET-capable bacteria were naturally present and this phenomenon is common in post-bloom systems. The intracellular ferredoxin-NADP-reductase is inactivated in the dead microalgae, allowing the production and extracellular transfer of photoelectrons. The use of mutant strains confirmed that the electron transport pathway requires multiheme cytochromes. Taken together, these results suggest a heretofore overlooked biophotoelectrochemical process jointly mediated by illumination of dead microalgae and live EET-capable bacteria in natural ecosystems, which may add an important component in the energetics of bioreduction phenomena particularly in microalgae-enriched environments.
自然水体中的厌氧还原过程可以被已死亡的微藻所促进，这些微藻的死亡归因于它们为其他微生物提供了分解所产生的营养物质。然而，以前的报告并没有考虑到死亡的微藻也可能作为光敏剂来驱动微生物的还原过程。在这里，我们展示了死亡的微藻与能够进行胞外电子传递（EET）的细菌之间存在光电协同联系。光照死亡的莱茵衣藻会使纯希瓦氏菌的厌氧生物还原速率提高一倍，这表明来自受光照的死亡微藻的光电子被转移到了具有 EET 能力的微生物。在受光照的死亡普通小球藻驱动的硝酸盐还原和活的希瓦氏菌的反应中以及在受光照的死亡莱茵衣藻驱动的六价铬还原和活的枯草芽孢杆菌的反应中都观察到了类似的现象。在混合培养的湖水光照死亡的微藻时也观察到了生物还原的增强，这表明具有 EET 能力的细菌自然存在，并且这种现象在藻类爆发后的系统中很常见。在死亡的微藻中，细胞内的铁氧还蛋白-NADP-还原酶失活，从而产生并进行了光电子的胞外转移。利用突变株证实了电子传递途径需要多血红素细胞色素。总的来说，这些结果表明，在自然生态系统中，光照死亡的微藻和具有 EET 能力的活细菌共同介导了一个以前被忽视的生物光电化学过程，这可能为生物还原现象的能量学增加了一个重要组成部分，特别是在富含微藻的环境中。
