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Metagenomic insights into the metabolism of microbial communities that mediate iron and methane cycling in Lake Kinneret sediments
Biogeosciences ( IF 4.9 ) Pub Date : 2020-09-10 , DOI: 10.5194/bg-2020-329
Michal Elul , Maxim Rubin-Blum , Zeev Ronen , Itay Bar-Or , Werner Eckert , Orit Sivan

Abstract. Complex microbial communities facilitate iron and methane transformations in anoxic ‎methanic sediments of freshwater lakes, such as Lake Kinneret (The Sea of Galilee, Israel). The ‎phylogenetic and functional diversity of these consortia are not fully understood, and it is not ‎clear which lineages perform iron reduction, anaerobic oxidation of methane (AOM) or both ‎‎(Fe-AOM). Here, we investigated microbial communities from both natural Lake Kinneret ‎sediments and iron-amended slurry incubations using metagenomics, focusing on functions ‎associated with iron reduction and methane cycling. Analyses of the phylogenetic and ‎functional diversity indicate that consortia of archaea (mainly Bathyarchaeia, ‎Methanomicrobia, Thermoplasmata, and Thermococci) and bacteria (mainly Chloroflexi ‎‎(Chloroflexota), Nitrospirae (Nitrospirota) and Proteobacteria) perform key metabolic ‎reactions such as amino acid uptake and dissimilation, organic matter fermentation, and ‎methanogenesis. The intrinsic Deltaproteobacteria, especially Desulfuromondales ‎‎(Desulfuromonadota), have the potential to transfer electrons extracellularly either to iron ‎mineral particles or to microbial syntrophs, including methanogens. This is likely via ‎transmembrane cytochromes, outer membrane hexaheme c-type cytochrome (OmcS) in ‎particular, or pilin monomer, PilA, which were attributed to this lineage. The bonafide ‎anaerobic oxidizers of methane (ANME) and denitrifying methanotrophs Methylomirabilia ‎‎(NC10) were scarce, and we consider the role of the lineage Methanothrix (Methanothrichales) ‎in Fe-AOM. We show that putative aerobes, such as methane-oxidizing bacteria Methylomonas ‎and their methylotrophic synthrophs Methylotenera are found among the anaerobic lineages in ‎Lake Kinneret iron amended slurries and can be involved in the oxidation of methane or its ‎intermediates, as suggested previously. We propose a reaction model for metabolic interactions ‎in the lake sediments, linking the potential players that interact via intricate metabolic ‎tradeoffs and direct electron transfer between species. Our results highlight the metabolic ‎complexity of microbial communities in an energy-limited environment, where aerobe and ‎anaerobe communities may co-exist and facilitate Fe-AOM as one strategy for survival.‎

中文翻译:

介导Kinneret湖沉积物中铁和甲烷循环的微生物群落代谢的元基因组学见解

摘要。复杂的微生物群落促进淡水湖(如以色列的加利利海)的淡水湖的缺氧甲烷化沉积物中的铁和甲烷转化。这些财团的系统发育和功能多样性尚不完全清楚,尚不清楚哪些谱系进行铁还原,甲烷厌氧氧化(AOM)或两者兼而有之(Fe-AOM)。在这里,我们使用宏基因组学研究了天然的Kinneret湖沉淀物和铁修饰的泥浆培养物的微生物群落,重点研究了与铁还原和甲烷循环相关的功能。对系统发育和功能多样性的分析表明,古细菌(主要为Bathyarchaeia,Methanomicrobia,Thermoplasmata和Thermococci)和细菌(主要为Chloroflexi(Chloroflexota),硝化螺旋菌(Nitrospirota)和变形杆菌(Proteobacteria)执行关键的代谢反应,例如氨基酸吸收和异化,有机物发酵和甲烷生成。固有的Deltaproteobacteria,特别是Desulfuromondales(Desulfuromonadota),具有将电子从细胞外转移到铁矿物质颗粒或微生物合成菌(包括产甲烷菌)的潜力。这可能是通过跨膜细胞色素,特定的外膜六血红素c型细胞色素(OmcS)或菌毛素单体PilA引起的,这归因于该谱系。真正的甲烷厌氧氧化剂(ANME)和反硝化甲烷氧化甲基甲烷(NC10)稀缺,我们考虑了血统的作用 和甲烷生成。固有的Deltaproteobacteria,特别是Desulfuromondales(Desulfuromonadota),具有将电子从细胞外转移到铁矿物质颗粒或微生物合成菌(包括产甲烷菌)的潜力。这可能是通过跨膜细胞色素,特定的外膜六血红素c型细胞色素(OmcS)或菌毛素单体PilA引起的,这归因于该谱系。真正的甲烷厌氧氧化剂(ANME)和反硝化甲烷氧化甲基甲烷(NC10)稀缺,我们考虑了血统的作用 和甲烷生成。固有的Deltaproteobacteria,特别是Desulfuromondales(Desulfuromonadota),具有将电子从细胞外转移到铁矿物质颗粒或微生物合成菌(包括产甲烷菌)的潜力。这可能是通过跨膜细胞色素,特定的外膜六血红素c型细胞色素(OmcS)或菌毛素单体PilA引起的,这归因于该谱系。真正的甲烷厌氧氧化剂(ANME)和反硝化甲烷氧化甲基甲烷(NC10)稀缺,我们考虑了血统的作用 这可能是通过跨膜细胞色素,特定的外膜六血红素c型细胞色素(OmcS)或菌毛素单体PilA引起的,这归因于该谱系。真正的甲烷厌氧氧化剂(ANME)和反硝化甲烷氧化甲基甲烷(NC10)稀缺,我们考虑了血统的作用 这可能是通过跨膜细胞色素,特定的外膜六血红素c型细胞色素(OmcS)或菌毛素单体PilA引起的,这归因于该谱系。真正的甲烷厌氧氧化剂(ANME)和反硝化甲烷氧化甲基甲烷(NC10)稀缺,我们考虑了血统的作用Methanothrix(Methanothrichales)在Fe-AOM中。我们表明,假定需氧菌,如甲烷氧化菌甲基单和他们的甲基synthrophs Methylotenera在基内雷特湖铁修正泥浆厌氧谱系中发现的和可参与甲烷或中间体的氧化,如先前建议。我们提出了一种用于湖泊沉积物中新陈代谢相互作用的反应模型,将潜在的参与者通过复杂的新陈代谢权衡和物种之间的直接电子转移进行相互作用。我们的研究结果突出了在能量受限的环境中微生物群落的代谢复杂性,其中需氧菌和厌氧菌群落可以共存并促进Fe-AOM的生存。
更新日期:2020-09-10
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