Eliani-Russak Efrat, Tik Zohar, Uzi-Gavrilov Shaked, Meijler Michael M, Sivan Orit
Department of Earth and Environmental Sciences, Ben-Gurion University of the Negev, Be'er Sheva, Israel.
Department of Chemistry, Ben-Gurion University of the Negev, Be'er Sheva, Israel.
Front Microbiol. 2023 Jul 20;14:1197299. doi: 10.3389/fmicb.2023.1197299. eCollection 2023.
Microbial dissimilatory iron reduction is a fundamental respiratory process that began early in evolution and is performed in diverse habitats including aquatic anoxic sediments. In many of these sediments microbial iron reduction is not only observed in its classical upper zone, but also in the methane production zone, where low-reactive iron oxide minerals are present. Previous studies in aquatic sediments have shown the potential role of the archaeal methanogen Methanosarcinales in this reduction process, and their use of methanophenazines was suggested as an advantage in reducing iron over other iron-reducing bacteria. Here we tested the capability of the methanogenic archaeon to reduce three naturally abundant iron oxides in the methanogenic zone: the low-reactive iron minerals hematite and magnetite, and the high-reactive amorphous iron oxide. We also examined the potential role of their methanophenazines in promoting the reduction. Pure cultures were grown close to natural conditions existing in the methanogenic zone (under nitrogen atmosphere, N:CO, 80:20), in the presence of these iron oxides and different electron shuttles. Iron reduction by was observed in all iron oxide types within 10 days. The reduction during that time was most notable for amorphous iron, then magnetite, and finally hematite. Importantly, the reduction of iron inhibited archaeal methane production. When hematite was added inside cryogenic vials, thereby preventing direct contact with , no iron reduction was observed, and methanogenesis was not inhibited. This suggests a potential role of methanophenazines, which are strongly associated with the membrane, in transferring electrons from the cell to the minerals. Indeed, adding dissolved phenazines as electron shuttles to the media with iron oxides increased iron reduction and inhibited methanogenesis almost completely. When was incubated with hematite and the phenazines together, there was a change in the amounts (but not the type) of specific metabolites, indicating a difference in the ratio of metabolic pathways. Taken together, the results show the potential role of methanogens in reducing naturally abundant iron minerals in methanogenic sediments under natural energy and substrate limitations and shed new insights into the coupling of microbial iron reduction and the important greenhouse gas methane.
微生物异化铁还原是一种基本的呼吸过程，在进化早期就已出现，在包括水生缺氧沉积物在内的多种生境中都有发生。在许多这类沉积物中，微生物铁还原不仅在其典型的上部区域被观察到，在存在低活性氧化铁矿物的甲烷生成区也能观察到。先前对水生沉积物的研究表明，古菌产甲烷菌甲烷八叠球菌在这一还原过程中具有潜在作用，并且它们利用甲烷吩嗪被认为是相较于其他铁还原细菌在还原铁方面的一个优势。在此，我们测试了产甲烷古菌在甲烷生成区还原三种天然丰度较高的氧化铁的能力：低活性铁矿物赤铁矿和磁铁矿，以及高活性无定形氧化铁。我们还研究了它们的甲烷吩嗪在促进还原过程中的潜在作用。在这些氧化铁和不同电子穿梭体存在的情况下，纯培养物在接近甲烷生成区自然存在的条件下（在氮气氛围中，N:CO，80:20）生长。在10天内，所有类型的氧化铁都观察到了由该古菌引起的铁还原。在此期间，无定形铁的还原最为显著，其次是磁铁矿，最后是赤铁矿。重要的是，铁的还原抑制了古菌的甲烷生成。当在低温小瓶中加入赤铁矿，从而防止其与该古菌直接接触时，未观察到铁还原，且甲烷生成也未受到抑制。这表明与膜紧密相关的甲烷吩嗪在将电子从细胞传递到矿物方面具有潜在作用。事实上，向含有氧化铁的培养基中添加溶解的吩嗪作为电子穿梭体，增加了铁还原并几乎完全抑制了甲烷生成。当该古菌与赤铁矿和吩嗪一起培养时，特定代谢物的量（但不是类型）发生了变化，表明代谢途径的比例存在差异。综上所述这些结果表明，在自然能量和底物限制条件下，产甲烷菌在还原甲烷生成沉积物中天然丰度较高的铁矿物方面具有潜在作用，并为微生物铁还原与重要温室气体甲烷的耦合提供了新的见解。
