李平
, 谭添, 刘韩, 王和林 中国地质大学(武汉)生物地质与环境地质国家重点实验室, 湖北 武汉 430074
收稿日期：2020-10-04；修回日期：2021-01-25；网络出版日期：2021-02-24
基金项目：国家自然科学基金（91851115）
作者简介：李平，博士，研究员(教授)，博士生导师，主要从事地质微生物方面的研究。先后承担和参与包括自然科学基金重大研究计划项目等在内的多项国家及省部级科研项目。以第一作者或通讯作者在Water Research、Science of the Total Environment、Frontiers in Microbilogy、International Biodeterioration & Biodegradation、Chemosphere等重要国际SCI期刊上发表论文30多篇.
*通信作者：李平, Tel: +86-27-67883456;E-mail: pli@cug.edu.cn.
摘要：地下水系统是地球关键带的重要组成部分，为微生物提供了特殊的栖息环境和复杂的生存条件，进而演化出复杂的生物地球化学过程。随着多技术、多学科的交叉融合及发展，近几十年地下水微生物功能群及生物地球化学循环研究取得了引人瞩目的重要进展。本文从地下水中的微生物群功能分区、微生物介导的地球化学元素循环、污染与修复中的生物地球化学过程，以及生物地球化学过程数值模拟等方面对国内外相关研究进展进行了综述，并对地下水系统中微生物"暗物质、暗过程"、微生物修复、地下水医学地质学，以及地下水多学科交叉融合等研究方向和前景进行了展望。
关键词：地下水微生物功能分区生态位生物地球化学循环生物修复微生物数值模拟
Functional microbial communities and the biogeochemical cycles in groundwater
Li Ping
, Tan Tian, Liu Han, Wang Helin State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, Hubei Province, China
Received: 4 October 2020; Revised: 25 January 2021; Published online: 24 February 2021
*Corresponding author: Ping Li, Tel: +86-27-67883456;E-mail: pli@cug.edu.cn.
Foundation item: Supported by the National Natural Science Foundation of China (91851115)
Abstract: As the important part of earth's critical zone, groundwater system provides special habitat environment and complex conditions for microorganisms, which further evolves complicated biogeochemical processes. In the last decades, with the developing and inter-crossing of new technologies and multi-discipline, important progresses have been obtained in the fields of microbial functional communities and biogeochemical cycle in groundwater. This review mainly describes the ecological niche of functional microbial communities, introduces the new findings in microbially-mediated geochemical cycling, microbial remediation and numerical simulation of the biogeochemical processes in groundwater system, including the discovery of new species, the coupling of various element cycles, and the latest technology of in-situ remediation of contaminated groundwater. This work also prospects the related future research direction including the microbial "dark matters" and "dark processes", bioremediation, medical geology, and multidisciplinary integration in groundwater system.
Keywords: groundwatermicrobial functional communitiesecological nichebiogeochemical cyclesbioremediationmicrobial numerical simulation
地下水系统是地球关键带的重要组成部分，是连接地表生物圈-深部地下生物圈的桥梁和纽带。世界范围内有超过三分之二的饮用水来自地下水，我国60%以上的城市开采利用地下水[1-2]。随着人类活动日益频繁，地下水污染逐渐加剧，地下水可持续安全供给受到空前挑战。微生物是地下水生态系统的重要组成部分，是地下水系统物质循环和能量流动的控制器。地下水低温、缺氧、低有机质和黑暗等特点为微生物提供了特殊的栖息环境[3]；地下水系统的非均质性和水文地质过程的非线性又为微生物提供了极其复杂的生存条件，进而演化出复杂的微生物功能群和生物地球化学过程。开展地下水微生物功能群及生物地球化学循环的研究有助于我们深入了解地下水水质的演化过程，为地下水资源保护和地下水污染修复提供科学依据。
随着科学技术的不断革新，近年来地下水微生物功能群及生物地球化学过程的研究呈现快速增长态势。特别是随着近10年来多学科技术的飞速发展，分子生物学、多组学、同位素、地球化学分析和数值模拟等多种技术方法、多学科的交叉融合与应用，地下水微生物功能群及生物地球化学循环研究取得了一系列引人瞩目的重要进展，主要有以下几个方面：(1) 地下水微生物功能群及功能分区；(2) 地下水微生物介导的地球化学元素循环；(3) 地下水污染与修复的生物地球化学过程；(4) 地下水生物地球化学过程数值模拟。本文将从这些方面对近年来国内外相关研究进展进行综述，并对其未来发展方向进行展望。
1 主要研究进展 1.1 地下水系统中微生物功能群及功能分区 地下水环境复杂的地球化学条件为微生物提供了多样的栖息环境，进而演化出了复杂的微生物功能群。研究地下水中的微生物功能群及其相互影响，能够更清楚地了解氧化还原条件变化过程中微生物群落的演替，为厘清地下水微生物与地球化学的协同关系提供依据。
有研究表明，地球上约40%的原核生物都栖息在地下含水层这一特殊环境中[4]，大量的微生物新种群还未被发现。研究者们通过16S rRNA扩增子测序和宏基因组学等技术对多个国家的地下水水体和沉积物以及岩溶地下水中的微生物群落及其功能进行了研究，发现了惊人的微生物多样性以及大量的新种；微生物介导的碳、氮、硫循环代谢活动相互依存，呈“流水线”式有序协作完成[5-7]；地下水微生物菌群功能多样，几乎占据了所有可能的菌群生态位。目前发现的地下水微生物可能参与有机物降解、产甲烷和甲烷氧化、硫氧化还原、铁氧化还原、氨化、固氮、硝化和反硝化等多种代谢活动[8-10]。
由于地下水流速缓慢，微生物长期累积并作用于碳、氮、铁、硫等元素的循环和迁移转化，从而改变了地下水的化学组分以及氧化还原电位(Eh)。从地下水补给区到排泄区，随着Eh的逐渐降低，地下水系统呈现了不同的生态位以及微生物功能群分区。这些微生物功能群在不同的Eh条件下分别进行有机物分解、硝酸盐还原、铁还原、硫酸盐还原和产甲烷等过程[11-17] (图 1)。例如，微生物进行硫酸盐还原时要求氧化还原电位Eh低于–100 mV[18]，而产甲烷菌只有在氧化还原电位小于–330 mV的条件下才能产甲烷[19]。
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| 图 1 地下水环境中主要微生物功能分区 Figure 1 The different ecological niches in groundwater. From the recharge zone to discharge zone of groundwater, with Eh decreasing, the function of the dominated microbial communities changed in turn of organic decomposition, nitrate reduction, iron reduction, sulfate reduction and methane production. |
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1.2 地下水微生物介导的地球化学元素循环 地下水中微生物介导多种元素的地球化学循环，包括氮、碳、铁、硫和砷等。这些元素循环之间也相互影响。如碳循环过程中的厌氧甲烷氧化过程与氮循环中的硝酸盐还原耦合[20-25]；化能厌氧铁氧化过程也需要硝酸盐的参与[26-27]；而厌氧氨氧化过程中产生大量电子，也可以与其它元素的还原反应如铁还原耦合，即厌氧铁还原氨氧化过程(Fe reduction coupled with ammonium oxidization，Feammox)[28-30]；硫酸盐还原过程中也会耦合铁和砷还原等[31-33]。
地下水系统是地球氮素循环的源和汇。近年来学界相关的研究主要集中在地下水系统氮的来源与转化过程，以及地下水系统对全球氮循环的贡献等方面。研究发现微生物矿化产氨与硝酸盐异化产氨(dissimilatory nitrate reduction to ammonium，DNRA)以及地表氮输入是高氨地下水形成的主要成因[34-35]，微生物固氮也可能是高氨地下水形成的重要原因[36-37] (图 2)。此外，厌氧氨氧化(anaerobic ammonia oxidation，Anammox)是近年来地下水氮循环中新发现的途径及研究热点[38]，地下水-土壤界面是Anammox反应热区，Anammox菌群是地下含水层氮素衰减的主要推手[39-40]。大量研究表明反硝化菌在地下水氮循环中起重要作用，反硝化过程可能贡献地下水中溶解N2的25%[41-45]。介导地下水中好氧氨氧化作用的菌群受氨浓度影响较大，在低氨地下水中以好氧氨氧化古菌为主，而在高氨地下水中好氧氨氧化细菌占主导地位[46-47]。
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| 图 2 高砷地下水中氮循环基因的相对变化[36] Figure 2 The relative change of detected nitrogen cycling genes from the high arsenic group samples[36]. Arrows in orange indicate ammonium source processes, arrows in green indicate ammonium utilization processes. Percentages indicate the normalized total intensity of the functional genes in groundwaters. |
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目前，人们对地下水系统中微生物介导的碳循环过程的研究主要集中在碳固定、有机质降解和产甲烷等。在自然界中已发现的6种微生物固碳途径中，目前地下水系统中发现了4种，包括卡尔文循环、还原型三羧酸循环、还原乙酰辅酶A途径和3-羟基丙酸循环/4-羟基丁酸循环[48-51]。有研究发现地下水中有机物的微生物降解可促进铁的氢氧化物还原溶解，进而促进固相中砷的释放[52]，而微生物介导的产甲烷过程也可能与砷的迁移转化密切相关[53]。此外，有研究表明地下水-地表水混合区域是微生物有机碳降解的热区，微生物的异养呼吸作用改变了该区域的有机碳组成[54]。
地下水环境中也普遍存在铁循环过程，它可以控制pH值以及营养物和污染物的流动性[55-56]。如有研究发现地下水环境中含有大量的铁氧化细菌参与成矿[57-58]；另外，地下水环境中还发现并分离出多种铁还原菌，这些微生物有不同的代谢特征[59]。如1株在1.7 km深的地下水中分离获得的发酵型铁还原菌Tepidibacillus decaturensis，能以H2或有机碳作为电子供体，还原铁等多种金属元素[60]。而从高砷地下水中分离得到的几株厌氧呼吸型铁还原菌——克雷伯氏菌属(Klebsiella)和希瓦氏菌属(Shewanella)，能以葡萄糖为电子供体还原铁，同时导致砷的迁移；这些铁还原菌由于分泌的胞外聚合物(EPS)组分不同而释放含砷矿物中的砷，或二次成矿再次固定砷[61]。
硫酸盐还原菌(sulfate reducing bacteria，SRB)是一种通过异化作用将硫酸盐作为电子受体进行硫酸盐还原的严格厌氧菌，地下水低温低氧的特殊环境为SRB提供了适宜的生长环境。目前地下水中已发现多种SRB类群，如脱硫肠状菌属(Desulfotomaculum)，脱硫球茎菌属(Desulfobulbus)，脱硫八叠球菌属(Desulfosarcina)和脱硫橄榄状菌属(Desulfobacca)，这些菌群通常具有较低丰度[62]。但有研究发现在硫酸盐污染的地下水中，SRB在原核生物群落中占有明显优势[63]。已有研究表明，硫酸盐、有机碳和铁等元素可促进地下水中SRB菌群的活性，进而形成了生物硫铁矿纳米颗粒[64]。另外，有研究发现地下深部微生物还可参与硫的氧化过程[65]。
砷(As)是一种有毒污染物，广泛存在于全球范围内的地下水环境中，对人类健康造成威胁[66-67]。在富砷水环境中，许多微生物被发现耐砷和/或利用砷进行呼吸代谢，能介导砷的还原、氧化、甲基化和去甲基化等过程[68-72]。这些微生物对不同碳源表现出不同的代谢能力，对砷的生物地球化学循环起重要作用[73]。目前已在地下水环境中发现了多种砷氧化还原微生物，包括副梭菌(Paraclostridium)、柠檬酸杆菌属(Citrobacter)、克雷伯氏菌属(Klebsiella)和芽孢杆菌属(Bacillus)等[74-77]。
微生物介导的地下水系统各元素循环之间常常相互影响，协同发生。如人们对硫、铁和砷的循环过程研究发现：微生物介导的硫酸盐还原促进了地下水系统中含砷铁氧化物的非生物还原，硫酸盐还原作用对含水层中铁循环和砷迁移过程起关键作用[78]；沉积物中释放的砷还可以通过与硫酸盐还原作用形成硫化铁矿物共沉淀或被吸附固定[79]。最近也有研究表明，地下水系统中Feammox作用可能是导致砷释放到地下水中的重要过程[80-81]。地下水中微生物介导的碳循环过程也被发现和其它元素地球化学过程相耦合，如有研究发现地下水沉积物衍生的溶解性腐殖酸可以通过电子穿梭促进铁还原，进而影响砷迁移[82]。同时，有机碳作为微生物代谢的主要能量来源，可通过增强微生物活性来促进铁的氢氧化物还原性溶解，从而导致砷释放[83-86]。
1.3 地下水污染与修复中的生物地球化学过程 地下水污染问题日益严重，除石油烃等有机污染物外，地下水污染还包括铜、铁、砷、锰、锌等重/类金属污染[87]。由于地下水污染整体特征表现为污染源多、污染面广、污染途径隐蔽和污染源滞后等[88-89]，再加上地下水的埋藏性和系统复杂性，使得地下水污染防治和修复工作困难重重。早期的异位修复或物理化学修复方法成本高，困难大，因此微生物修复逐渐成为现在的研究热点。微生物修复技术主要通过地下水微生物对污染物的降解和固定来实现地下水污染物的去除，主要包括原位修复法和生物反应器法。如Michalsen等[90]采用原位修复法成功使用两株菌I-C和KTR9将地下水中的环三次甲基三硝基胺快速降解；Zhang等[91]利用S(0)或Fe(0)自养生物和异养微生物之间的生物氧化去除地下水中的钒(V)；Gibert等[92]利用渗透反应屏障(PRB)在原位去除地下水中的硝酸盐，通过PRB中的活性物质为反硝化细菌提供碳源，成功地去除地下水中浓度高达280 mg/L的NO3–。由于地下水流速低，隔水层渗透性差，这使得微生物原位修复和PRB修复法容易受到制约。而采用地下循环井的方法则可增强地下水的流动性，进而大大促进微生物修复效率。如Pierro等[93]在修复氯代烃污染的地下水过程中，使用循环井加快了微生物所需碳源(3-羟基丁酸盐)的输送，极大程度地促进了修复效果。
1.4 地下水生物地球化学过程的数值模拟 地下水环境的复杂性，以及水文地质过程的非线性，使得地下水中的生物地球化学过程极其复杂，实验室条件下难以模拟，因此数值模拟作为一种定量化且经济的方法被应用到地下水生物地球化学过程的研究中。利用数值模拟的方法对微生物作用进行评估，并且预测其功能和过程，已逐渐成为近年来相关研究的热点[94]。早在20世纪80年代，有研究就提出了关于潜流带生物地球化学过程的数学模型，如OTIS (One-dimensional transport with inflow and storage)模型、RTD (residence time distribution)模型、ASP (advective storage path)模型、TSM (transient storage model)模型等[95-97]。之后，越来越多的地下水、地表水数值模型也被应用到研究中。如Shapiro等[98]利用基因组数据预测自然环境中微生物代谢速率，通过模拟含水层中产甲烷菌预测该类菌体代谢过程中的生化反应速率，明确跟踪了产甲烷过程中碳和能量的细胞通量。Shi等[99]建立了微生物介导砷还原和铁氧化物转化的耦合动力学模型，并根据砷还原基因arrA的表达模式对砷还原速率进行了量化。又如Lai等[100]建立了数学模型来评估纳米零价铁(NZVI)微生物脱氮去除地下水硝酸盐技术的性能。Valsala等[101]通过建立有限差分模型的数值模拟方法，探究了胶体和微生物共存对地下水中BTEX (苯、甲苯、乙苯、二甲苯)迁移的影响。目前，微生物数值模拟方面的研究还处于初步阶段，大量的地下水“微生物暗过程”还有待采用数值模拟的办法进行预测和探究。
2 问题和展望 随着(宏)基因/转录组学、代谢组学、宏表型组学等技术的快速发展以及各种分析手段的不断革新，学界对地下水系统中生物地球化学循环的了解更加全面深入，同时也对地下水微生物功能群及生物地球化学循环研究提出更高的要求。未来地下水微生物功能群及生物地球化学循环的研究亟待围绕以下几个方面展开。
地下水微生物介导的元素地球化学循环过程亟待进一步深入，这些过程中的能量转换和代谢新途径及其调控机制还有待大量深入研究。随着各种研究手段的革新，围绕地下水中微生物作用的微观机制及其宏观生态效应，深入探索地下水微生物介导的元素地球化学循环过程中多元素多过程的耦合关系，以及它们在地球“水圈”、“岩石圈”和“大气圈”中作用的研究将成为未来的热点。
修复理论方法和技术创新将成为地下水可持续安全供给的基石。地下水修复的生物地球化学理论研究、生物技术应用研究及生物修复工程化方面还比较薄弱，还缺乏对地下水微生物功能群演化和生物地球化学过程的完整识别。另外由于地下水环境不同于地表，复杂多变且不可见，地下水修复微生物功能群及其地球化学过程的原位检测和野外长期监测是难点。未来地下水修复的重点研究方向需要多头并进：开发原位模拟方法和长期监测技术，微生物修复与植物修复、电化学修复等多技术联合。
地下水与人类生活关系密切，直接影响人类身体健康。因此，全面深入理解地下水微生物作用与地质成因和人为活动影响下各种致畸致癌等有害物质的迁移转化过程及其健康风险，对保证国家供水安全和维护公共健康起着十分重要的作用。近年来医学地质学的提出将面临新的重大社会需求，人类在谋求人与自然和谐发展的进程中，“同一健康”概念(one health concept)下的地下水医学地质学的重要性将与日俱增[102]，将是今后的一个重要研究方向。
微生物是地球上最丰富多样的细胞生命形式，占据了所有可能的生态位。而绝大部分微生物都不能通过纯培养获得，即被称为“微生物暗物质”。地下水系统中大量未知的微生物类群以及“微生物暗物质”亟待学界进一步挖掘[103]。通过纯培养技术获得地下水微生物可培养信息与资源方面的研究，或通过不依赖纯培养且具有高分辨率的单细胞技术，如纳米二次离子质谱(NanoSIMS)和单细胞拉曼光谱等获得微生物细胞共代谢信息，将是今后的又一个重要研究方向[104-106]。
随着科学技术的发展，分子生物学、多组学、生物信息学、同位素地球化学、微区地球化学分析、高分辨率电镜技术、数值模拟等多种技术方法、多学科的交叉融合将应用到地下水微生物的研究中，这些必将成为今后研究的有力工具，在很大程度上拓展我们对地下水认知的深度和广度，为地下水科学的发展以及地下水的安全供给提供广阔空间。
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