水稻土丁酸互营产甲烷菌群的砷甲基化特征及机制解析

doi:10.16258/j.cnki.1674-5906.2024.10.010

生态环境学报 ›› 2024, Vol. 33 ›› Issue (10): 1580-1589.DOI: 10.16258/j.cnki.1674-5906.2024.10.010

• 研究论文【环境科学】 • 上一篇下一篇

水稻土丁酸互营产甲烷菌群的砷甲基化特征及机制解析

刘苏杰¹^,²^,³(), 刘传平³, 方利平³, 陈冠虹³^,^*(), 李芳柏³

1.中国科学院广州地球化学研究所，广东广州 510640
2.中国科学院大学，北京 100049
3.广东省科学院生态环境与土壤研究所/华南土壤污染控制与修复国家地方联合工程研究中心/广东省农业环境综合治理重点实验室，广东广州510650

收稿日期:2024-02-15 出版日期:2024-10-18 发布日期:2024-11-15
通讯作者: *陈冠虹。E-mail: ghchen@soil.gd.cn
作者简介:刘苏杰（1998年生），男，硕士研究生，研究方向为土壤砷污染控制。E-mail: liusujie21@mails.ucas.ac.cn
基金资助:
国家重点研发计划项目(2023YFD1901300);国家自然科学基金项目(42377395);国家茶叶产业岗位专家项目(CARS-19);“十四五”广东省农业科技创新十大主攻方向“揭榜挂帅”项目(2022SDZG08);韶关市省科技专项资金项目(220716096270196);韶关市省科技创新战略专项项目(230225176275072)

Arsenic Methylation Process and the Associated Microbial Mechanisms in Paddy Soil Butyrate-degrading Methanogenic Communities

LIU Sujie¹^,²^,³(), LIU Chuanping³, FANG Liping³, CHEN Guanhong³^,^*(), LI Fangbai³

1. Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, P. R. China
2. University of Chinese Academy of Sciences, Beijing, 100049, P. R. China
3. Institute of Eco-environmental and Soil Sciences, Guangdong Academy of Sciences/National-Regional Joint Engineering Research Center for Soil Pollution Control and Remediation in South China/Guangdong Key Laboratory of Integrated Agro-environmental Pollution Control and Management, Guangzhou, 510650, P. R. China

Received:2024-02-15 Online:2024-10-18 Published:2024-11-15

摘要/Abstract

摘要：

短链脂肪酸互营产甲烷是厌氧有机质分解过程中的关键限速步骤，互营产甲烷菌群砷抗性机制是其适应砷胁迫的重要途径，然而它们的砷转化特征和抗性策略尚不清楚。丁酸是有机质分解产甲烷过程中生成的重要中间产物，丁酸产甲烷菌群的砷甲基化能力及对砷胁迫的耐受机制对于理解厌氧微生物砷转化过程至关重要。利用丁酸为唯一碳源和无机As(III)或有机三价砷MMAs(III)为砷底物分别富集稻田土壤源产甲烷菌群，发现丁酸产甲烷富集物能够将As(III)转化为一甲基砷（MMAs）、二甲基砷（DMAs）和三甲基砷（TMAsO），也能将MMAs(III)转化为DMAs和TMAsO。通过细菌、古菌和功能微生物群落分子解析技术，结果表明共养单胞菌科Syntrophomonadaceae作为丁酸互营氧化功能菌是富集物中主要的细菌类群，甲烷八叠球菌属Methanosarcina和甲烷杆菌属Methanobacterium是主要的产甲烷古菌，它们协同驱动了砷胁迫下的丁酸氧化产甲烷过程。不同砷胁迫条件下的关键微生物类群对比结果显示，MMAs(Ⅲ)胁迫条件进一步富集了Syntrophomonadaceae（55.2%－61.0%）和Methanobacterium（49.0%－55.7%），并且这两种类群中存在潜在砷甲基化微生物，它们可能通过砷甲基化来耐受环境中的砷胁迫。所以，短链脂肪酸互营氧化产甲烷菌群中互营细菌和产甲烷古菌成员可能利用砷甲基化进行解毒，以适应厌氧环境中的高毒性三价无机砷或甲基砷，是其耐受砷胁迫的重要生存策略。研究结果可为理解厌氧微生物类金属耐受机制及其参与的碳砷元素耦合转化过程提供新视角。

关键词: 水稻土, 短链脂肪酸, 互营产甲烷, 砷甲基化微生物, 砷抗性

Abstract:

Syntrophic fatty acid oxidation is a rate-limiting step during the methanogenic degradation of organic matter, and arsenic(As) resistance strategies are important for the activities of syntrophic methanogenic communities under As stress. However, their As-transforming abilities and the underlying mechanisms remain unknown. Butyrate is a key intermediate in the degradation of organic matter to methane. The As-methylating ability of butyrate-degrading methanogenic communities and their As resistance mechanisms are essential for understanding the anaerobic microbial As transformation processes. In this study, butyrate-degrading methanogenic enrichment was obtained from paddy soils using butyrate as the sole carbon source and As(III) or MMAs(III) as the As substrate. It was found that the enrichments could methylate As(III) to MMAs, DMAs, and TMAsO, and methylate MMAs(III) to DMAs and TMAsO. Syntrophomonadaceae, known as the key butyrate oxidizer, was the main bacterial taxon in the enrichment. Methanosarcina and Methanobacterium are the main methanogenic archaea, which may be in syntrophic association with butyrate oxidizers, thereby driving the methanogenesis under As stress. A comparison of key microbial groups under different As stresses revealed that Syntrophomonadaceae (55.2%‒61.0%) and Methanobacterium (49.0%‒55.7%) were enriched under MMAs(III) conditions. Potential As-methylating microorganisms were further identified in these two taxa, indicating that their ability to methylate As may confer resistance to As toxicity in the environment. Therefore, syntrophic bacteria and methanogenic archaea may perform As methylation to detoxify highly toxic trivalent inorganic or methylated As species in anoxic environments, which may play a role in their survival strategies under As stress. This study provides new insights into metalloid resistance mechanisms adopted by anaerobic microorganisms and the coupled process of carbon and arsenic cycling.

Key words: paddy soil, short-chain fatty acid, syntrophic methanogenesis, arsenic-methylating microorganisms, arsenic resistance

中图分类号:

X171.5
X172

刘苏杰, 刘传平, 方利平, 陈冠虹, 李芳柏. 水稻土丁酸互营产甲烷菌群的砷甲基化特征及机制解析[J]. 生态环境学报, 2024, 33(10): 1580-1589.

LIU Sujie, LIU Chuanping, FANG Liping, CHEN Guanhong, LI Fangbai. Arsenic Methylation Process and the Associated Microbial Mechanisms in Paddy Soil Butyrate-degrading Methanogenic Communities[J]. Ecology and Environment, 2024, 33(10): 1580-1589.

图/表 8

表1 基础盐培养基组分

Table 1 The component of medium used in this study

组分	量值	单位
1,4-哌嗪二乙磺酸 (PIPES)	3.024	g·L⁻¹
NH₄Cl	0.535	g·L⁻¹
NaHCO₃	0.420	g·L⁻¹
KH₂PO₄	0.136	g·L⁻¹
MgCl₂·6H₂O	0.1017	g·L⁻¹
CaCl₂	0.055	g·L⁻¹
维生素溶液	1	mL·L⁻¹
微量元素溶液	1	mL·L⁻¹
超纯水	1	L·L⁻¹
pH	7.0	‒

表2 实时荧光定量PCR分析所用引物及扩增条件

Table 2 Lists of primer pairs and thermal cycling parameters for real-time quantitative PCR

目的基因	引物名称	引物序列 (5'-3')	长度/bp	扩增程序	参考文献
细菌16S rRNA	515F	GTGYCAGCMGCCGCGGTAA	280	95 ℃ 30 s; 94 ℃ 20 s, 55 ℃ 20 s, 72 ℃ 30 s, 40个循环	Einen et al., 2008
细菌16S rRNA	806R	GGACTACNVGGGTWTCTAAT	280	95 ℃ 30 s; 94 ℃ 20 s, 55 ℃ 20 s, 72 ℃ 30 s, 40个循环	Einen et al., 2008
古菌16S rRNA	Arch519F	CAGCCGCCGCGGTAA	400	95 ℃ 30 s; 95 ℃ 30 s, 57 ℃ 30 s, 72 ℃ 50 s, 40个循环	Coolen et al., 2004
古菌16S rRNA	Arch915R	GTGCTCCCCCGCCAATTCCT	400	95 ℃ 30 s; 95 ℃ 30 s, 57 ℃ 30 s, 72 ℃ 50 s, 40个循环	Coolen et al., 2004
arsM	arsMF1	TCYCTCGGCTGCGGCAAYCCVAC	350	95 ℃ 30 s; 95 ℃ 30 s, 57 ℃ 30 s, 72 ℃ 1 min, 40个循环	Jia et al., 2013
arsM	arsMR2	CGWCCGCCWGGCTTWAGYACCCG	350	95 ℃ 30 s; 95 ℃ 30 s, 57 ℃ 30 s, 72 ℃ 1 min, 40个循环	Jia et al., 2013
mcrA	mlas-mod-F	GGYGGTGTMGGDTTCACMCARTA	469	95 ℃ 30 s; 95 ℃ 15 s, 58 ℃ 30 s, 72 ℃ 30 s, 40个循环	Angel et al., 2012
mcrA	mcrA-rev-R	CGTTCATBGCGTAGTTVGGRTAGT	469	95 ℃ 30 s; 95 ℃ 15 s, 58 ℃ 30 s, 72 ℃ 30 s, 40个循环	Angel et al., 2012

图1 BI和BM富集物中甲基砷物质的量浓度随时间变化和物种组成（以单位生物量计） *：P<0.05。下同

Figure 1 Evolution of methylated arsenic concentration and the composition of methylated arsenic species in BI and BM (normalized by OD600)

图2 BI和BM富集物中甲烷、丁酸和乙酸物质的量浓度随时间变化（以单位生物量计）

Figure 2 Evolution of methane, butyrate and acetate concentration in BI and BM (normalized by OD600)

图3 培养第30天时BI和BM富集物中砷甲基化和产甲烷功能基因相对丰度

Figure 3 Relative abundance of arsenic methylation and methanogenic functional genes in BI and BM

图4 BI和BM富集物细菌群落结构特征对比 **：P<0.01

Figure 4 Differences in the properties of the bacterial community between BI and BM

图5 BI和BM富集物古菌群落结构特征对比

Figure 5 Differences in the properties of archaeal community between BI and BM

图6 基于富集物中菌群arsM核酸序列构建的Neighbor-Joining系统发育树

Figure 6 Phylogenetic tree of arsM nucleotide sequences retrieved from enrichments

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水稻土丁酸互营产甲烷菌群的砷甲基化特征及机制解析

Arsenic Methylation Process and the Associated Microbial Mechanisms in Paddy Soil Butyrate-degrading Methanogenic Communities

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