Photoelectron-promoted metabolism of sulphate-reducing microorganisms in substrate-depleted environments

IF 4.3 2区 生物学 Q2 MICROBIOLOGY
Chao Zhong, Anhuai Lu, Hailiang Dong, Shan Huang, Liang Shi, Yanan Shen, Yangjian Cheng, Yiran Dong, Xiangzhen Li, Jie Xu, Jinren Ni, Michael F. Hochella Jr, Juan Liu
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Abstract

Sulphate-reducing microorganisms, or SRMs, are crucial to organic decomposition, the sulphur cycle, and the formation of pyrite. Despite their low energy-yielding metabolism and intense competition with other microorganisms, their ability to thrive in natural habitats often lacking sufficient substrates remains an enigma. This study delves into how Desulfovibrio desulfuricans G20, a representative SRM, utilizes photoelectrons from extracellular sphalerite (ZnS), a semiconducting mineral that often coexists with SRMs, for its metabolism and energy production. Batch experiments with sphalerite reveal that the initial rate and extent of sulphate reduction by G20 increased by 3.6 and 3.2 times respectively under light conditions compared to darkness, when lactate was not added. Analyses of microbial photoelectrochemical, transcriptomic, and metabolomic data suggest that in the absence of lactate, G20 extracts photoelectrons from extracellular sphalerite through cytochromes, nanowires, and electron shuttles. Genes encoding movement and biofilm formation are upregulated, suggesting that G20 might sense redox potential gradients and migrate towards sphalerite to acquire photoelectrons. This process enhances the intracellular electron transfer activity, sulphur metabolism, and ATP production of G20, which becomes dominant under conditions of carbon starvation and extends cell viability in such environments. This mechanism could be a vital strategy for SRMs to survive in energy-limited environments and contribute to sulphur cycling.

Abstract Image

Abstract Image

底物贫乏环境中硫酸盐还原微生物的光电子促进新陈代谢。
硫酸盐还原微生物(SRMs)对有机物分解、硫循环和黄铁矿的形成至关重要。尽管硫酸盐还原微生物的新陈代谢能量低,与其他微生物的竞争也很激烈,但它们在通常缺乏足够底物的自然栖息地中繁衍生息的能力仍然是一个谜。本研究探讨了具有代表性的 SRM--脱硫弧菌 G20 如何利用细胞外闪锌矿(ZnS)的光电子进行新陈代谢和产生能量。用闪锌矿进行的分批实验表明,在不添加乳酸盐的情况下,与黑暗条件相比,G20 在光照条件下的硫酸盐还原初始速率和程度分别增加了 3.6 倍和 3.2 倍。对微生物光电化学、转录组和代谢组数据的分析表明,在没有乳酸盐的情况下,G20 通过细胞色素、纳米线和电子快车从细胞外闪锌矿中提取光电子。编码运动和生物膜形成的基因上调,表明 G20 可能感知氧化还原电位梯度,并向闪锌矿迁移以获取光电子。这一过程增强了 G20 的胞内电子传递活性、硫代谢和 ATP 生成,使其在碳饥饿条件下成为主导,并延长了细胞在这种环境中的存活时间。这种机制可能是 SRM 在能量有限的环境中生存并促进硫循环的重要策略。
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来源期刊
Environmental microbiology
Environmental microbiology 环境科学-微生物学
CiteScore
9.90
自引率
3.90%
发文量
427
审稿时长
2.3 months
期刊介绍: Environmental Microbiology provides a high profile vehicle for publication of the most innovative, original and rigorous research in the field. The scope of the Journal encompasses the diversity of current research on microbial processes in the environment, microbial communities, interactions and evolution and includes, but is not limited to, the following: the structure, activities and communal behaviour of microbial communities microbial community genetics and evolutionary processes microbial symbioses, microbial interactions and interactions with plants, animals and abiotic factors microbes in the tree of life, microbial diversification and evolution population biology and clonal structure microbial metabolic and structural diversity microbial physiology, growth and survival microbes and surfaces, adhesion and biofouling responses to environmental signals and stress factors modelling and theory development pollution microbiology extremophiles and life in extreme and unusual little-explored habitats element cycles and biogeochemical processes, primary and secondary production microbes in a changing world, microbially-influenced global changes evolution and diversity of archaeal and bacterial viruses new technological developments in microbial ecology and evolution, in particular for the study of activities of microbial communities, non-culturable microorganisms and emerging pathogens
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