Unveiling the adaptive evolution of halotolerant aceticlastic methanogenesis: Multi-scale responses and energy partition

IF 12.8 1区环境科学与生态学 Q1 ENGINEERING, ENVIRONMENTAL

Water Research Pub Date : 2026-04-15 Epub Date: 2026-02-11 DOI:10.1016/j.watres.2026.125552

Huiyuan Guo , Qing Liu , Hexing Han , Weichao Xu , Wansheng Shi , Mingxing Zhao , Xin Xiao , Jianwei Liu , Tinggang Li

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Abstract

The high concentration of salt ions in saline organic wastewater poses significant challenges for wastewater treatment technologies, particularly impacting the stability of anaerobic digesters. Aceticlastic methanogenesis is a crucial pathway for converting acetate into methane through methanoarchaea whose metabolism is adversely impacted by salt stress. To address this, long-term adaptive laboratory evolution (ALE) was conducted to cultivate halotolerant aceticlastic methanoarchaea, incorporating metagenomics, metatranscriptomic sequencing, metabolomics, and metabolic modeling to delineate genetic and metabolic responses. The evolved microbiome achieved a substantial increase in methanogenic activity at 5 % sodium chloride, reaching 82.25 % theoretical conversion of acetate to methane, significantly outperforming the original microbiome. This ALE process overcame the natural scarcity of aceticlastic methanogens in hypersaline environments. Key adaptation mechanisms were confirmed at the transcriptional level, primarily involving the upregulation of genes for inorganic ion transport, compatible solute uptake, and de novo biosynthesis. Horizontal gene transfer also contributed significantly through the transfer of osmoregulation genes, particularly those for compatible solute transport, suggesting an energy-efficient adaptation strategy of accumulating rather than synthesizing solutes. Metabolic flux analysis revealed that adjustments in energy distribution under salt stress are driven by the energetic cost of synthesizing compatible solutes, which highlights the importance of solute transporters for energy conservation. This study elucidates the complex interplay between metabolic reprogramming and gene transfer in enhancing microbial resilience under salt stress, thereby deepening our understanding of microbial adaptations in extreme environments and advancing biotechnological approaches for saline wastewater treatment.

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揭示耐盐醋酸制甲烷的适应性进化：多尺度响应和能量分配

含盐有机废水中的高浓度盐离子对废水处理技术提出了重大挑战，特别是影响厌氧沼气池的稳定性。醋酸裂解产甲烷是甲烷古菌将乙酸转化为甲烷的重要途径，而甲烷古菌的代谢受到盐胁迫的不利影响。为了解决这一问题，研究人员进行了长期适应性实验室进化（ALE），培养耐盐醋酸甲烷古菌，结合元基因组学、元转录组测序、代谢组学和代谢模型来描述遗传和代谢反应。进化后的微生物组在5%氯化钠条件下的产甲烷活性显著提高，乙酸酯转化为甲烷的理论转化率达到82.25%，显著优于原始微生物组。这种ALE过程克服了高盐环境中醋酸产甲烷菌的自然稀缺。关键的适应机制在转录水平上得到证实，主要涉及无机离子运输、相容溶质摄取和新生生物合成基因的上调。水平基因转移也通过渗透调节基因的转移发挥了重要作用，特别是那些兼容溶质运输的基因，这表明一种积累而不是合成溶质的节能适应策略。代谢通量分析表明，盐胁迫下能量分布的调整是由合成相容溶质的能量成本驱动的，这凸显了溶质转运体对能量节约的重要性。本研究阐明了代谢重编程和基因转移在提高盐胁迫下微生物恢复力中的复杂相互作用，从而加深了我们对极端环境下微生物适应的理解，并推进了含盐废水处理的生物技术方法。

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来源期刊

Water Research 环境科学-工程：环境

CiteScore

20.80

自引率

9.40%

发文量

1307

审稿时长

38 days

期刊介绍： Water Research, along with its open access companion journal Water Research X, serves as a platform for publishing original research papers covering various aspects of the science and technology related to the anthropogenic water cycle, water quality, and its management worldwide. The audience targeted by the journal comprises biologists, chemical engineers, chemists, civil engineers, environmental engineers, limnologists, and microbiologists. The scope of the journal include: •Treatment processes for water and wastewaters (municipal, agricultural, industrial, and on-site treatment), including resource recovery and residuals management; •Urban hydrology including sewer systems, stormwater management, and green infrastructure; •Drinking water treatment and distribution; •Potable and non-potable water reuse; •Sanitation, public health, and risk assessment; •Anaerobic digestion, solid and hazardous waste management, including source characterization and the effects and control of leachates and gaseous emissions; •Contaminants (chemical, microbial, anthropogenic particles such as nanoparticles or microplastics) and related water quality sensing, monitoring, fate, and assessment; •Anthropogenic impacts on inland, tidal, coastal and urban waters, focusing on surface and ground waters, and point and non-point sources of pollution; •Environmental restoration, linked to surface water, groundwater and groundwater remediation; •Analysis of the interfaces between sediments and water, and between water and atmosphere, focusing specifically on anthropogenic impacts; •Mathematical modelling, systems analysis, machine learning, and beneficial use of big data related to the anthropogenic water cycle; •Socio-economic, policy, and regulations studies.