Thapa Bhim Sen, Flynn Theodore M, Jensvold Zena D, Kemner Kenneth M, Sladek Margaret F, O'Loughlin Edward J, Marshall Christopher W
Department of Biological Sciences, Marquette University, Milwaukee, Wisconsin, USA.
Biosciences Division, Argonne National Laboratory, Lemont, Illinois, USA.
Appl Environ Microbiol. 2025 May 21;91(5):e0222224. doi: 10.1128/aem.02222-24. Epub 2025 Apr 25.
In many aquatic and terrestrial ecosystems, iron (Fe) reduction by microorganisms is a key part of biogeochemical cycling and energy flux. The presence of redox-active electron shuttles in the environment potentially enables a phylogenetically diverse group of microbes to use insoluble iron as a terminal electron acceptor. We investigated the impact that different electron shuttles had on respiration, microbial physiology, and microbial ecology. We tested eight different electron shuttles, seven quinones and riboflavin, with redox potentials between 0.217 and -0.340 V. Fe(III) reduction coupled with acetate oxidation was observed with all shuttles. Once Fe(III) reduction began to plateau, a rapid increase in acetate consumption was observed and coincided with the onset of methane production, except in the incubations with the shuttle 9,10-anthraquinone-2-carboxylic acid (AQC). The rates of iron reduction, acetate consumption, methanogenesis, and the microbial communities varied significantly across the different shuttles independent of redox potential. In general, shuttles appeared to reduce the overall diversity of the community compared to no shuttle controls, but certain shuttles were exceptions to this trend. Geobacteraceae were the predominant taxonomic family in all enrichments except in the presence of AQC or 1,2-dihydroxyanthraquinone (AQZ), but each shuttle enriched a unique community significantly different from the no shuttle control conditions. This suggests that the presence of different redox-active electron shuttles can have a large influence on the microbial ecology and total carbon flux in the environment.IMPORTANCEIron is the fourth most abundant element in the Earth's crust, and the reduction of iron by microbes is an important component of global biogeochemical cycles. A phylogenetically diverse group of microbes is capable of conserving energy with oxidized iron as a terminal electron acceptor, but the environmental conditions favoring certain taxonomic clades in iron-reducing environments are unclear. One complicating factor often overlooked in small-scale enrichments is the influence of soluble, redox-active electron shuttles on the rate and microbial ecology of iron reduction. We tested the effects of eight different electron shuttles on microbial physiology and ecology in iron-reducing enrichments derived from a local wetland. Each electron shuttle varied the microbial activity and enriched for a microbial community distinct from the no shuttle control condition. Therefore, in complex subsurface environments with many redox-active compounds present, we propose electron shuttles as a reason for the coexistence of multiple clades of iron-reducing bacteria.
在许多水生和陆地生态系统中，微生物介导的铁（Fe）还原是生物地球化学循环和能量通量的关键部分。环境中氧化还原活性电子穿梭体的存在可能使多种微生物能够利用不溶性铁作为末端电子受体。我们研究了不同电子穿梭体对呼吸作用、微生物生理学和微生物生态学的影响。我们测试了8种不同的电子穿梭体，7种醌类和核黄素，其氧化还原电位在0.217至-0.340V之间。所有穿梭体均观察到Fe（III）还原与乙酸氧化耦合。一旦Fe（III）还原开始趋于平稳，除了在添加9,10-蒽醌-2-羧酸（AQC）的培养物中外，乙酸消耗量迅速增加，并与甲烷产生的开始同时发生。不同穿梭体的铁还原率、乙酸消耗量、产甲烷率和微生物群落存在显著差异，与氧化还原电位无关。一般来说，与不添加穿梭体的对照相比，穿梭体似乎降低了群落的总体多样性，但某些穿梭体是这一趋势的例外。除了存在AQC或1,2-二羟基蒽醌（AQZ）的情况外，地杆菌科是所有富集培养物中的主要分类科，但每种穿梭体富集的独特群落与不添加穿梭体的对照条件有显著差异。这表明不同氧化还原活性电子穿梭体的存在会对环境中的微生物生态学和总碳通量产生很大影响。
铁是地壳中第四丰富的元素，微生物对铁的还原是全球生物地球化学循环的重要组成部分。多种微生物能够以氧化铁作为末端电子受体来保存能量，但在铁还原环境中有利于某些分类进化枝的环境条件尚不清楚。在小规模富集培养中经常被忽视的一个复杂因素是可溶性氧化还原活性电子穿梭体对铁还原速率和微生物生态学的影响。我们测试了8种不同电子穿梭体对源自当地湿地的铁还原富集培养中微生物生理学和生态学的影响。每种电子穿梭体都改变了微生物活性，并富集了与不添加穿梭体的对照条件不同的微生物群落。因此，在存在许多氧化还原活性化合物的复杂地下环境中，我们提出电子穿梭体是多种铁还原细菌进化枝共存的一个原因。
