周伟华, 廖健祖, 3, 郭亚娟, 3, 袁翔城, 黄 晖, 刘 胜, 李 涛



溶解有机物的光降解及其对浮游细菌和浮游植物的影响

周伟华1, 2, 廖健祖1, 2, 3, 郭亚娟1, 2, 3, 袁翔城1, 2, 黄 晖1, 2, 刘 胜1, 2, 李 涛1, 2

(1. 中国科学院南海海洋研究所热带海洋生物资源与生态重点实验室, 广东广州510301; 2. 中国科学院海南热带海洋生物实验站, 海南三亚572000; 3. 中国科学院大学, 北京100049)

作为海洋中最大的动态有机碳储库, 溶解有机物的光降解(主要是紫外波段)对生源要素的生物地球化学循环以及海洋生态系统的结构和功能具有重要的影响。本文探讨了影响溶解有机物光降解的环境因素、其光化学过程和产物, 并重点阐述了溶解有机物的光降解对浮游细菌和浮游植物的影响。溶解有机物的来源和成分复杂, 其光降解在不同海区有不同的生态效应, 为了能更准确地把握其生态效应, 需要更全面和深入的研究。

溶解有机物; 光降解; 紫外线; 浮游细菌; 浮游植物

溶解有机物(Dissolved organic matter, DOM)是自然界中普遍存在的一类复杂的混合物。目前, 大多数的海洋DOM分离方法使用孔径为0.7 µm的玻璃纤维膜进行过滤, 它包括通过滤膜而且之后用于实验分析过程中不因蒸发丢失的有机物质部分, 以及在过滤过程中没有被截留的胶体颗粒[1]。

作为海洋中最大的动态有机碳储库(约662 Gt碳), 海洋中DOM的生物地球化学行为对碳循环以及全球气候变化有着重要的作用[2]。DOM根据其生物可利用性可分为: 活性DOM(Liable DOM, LDOM)、半活性DOM(Semi-Liable DOM, SLDOM)和惰性DOM(Recalcitrant DOM, RDOM)。其中RDOM的含量最高, 约占海洋DOM的95%(约624Gt碳), 与大气中的CO2的碳量(约750 Gt碳)相当, 是一个巨大的碳汇。由于其难降解, 在海洋中有极长的停留时间, 焦念志等[3]认为RDOM是海洋重要的储碳物质, 并提出“微型生物碳泵(Microbial carbon pump, MCP)”的概念, 即有机质在微型生物的作用下形成RDOM的过程。经过MCP过程而形成的RDOM有较高的碳: 氮: 磷(3511: 202: 1)[4], 从而使碳以有机物的形态长期保存在海洋中, 而氮, 磷则以无机的形态被生产者重新吸收利用。因而, MCP不仅有储碳的作用, 且能促进营养盐的循环和生产力。

工业革命以来, 受人类活动的影响, 臭氧层被削薄使得更多的紫外线(Ultraviolet radiation, UV)能达到地球的表面。近年来, 甚至在一些热带地区也出现了臭氧洞, UV对水生生态系统的影响越来越突出, 特别是紫外线B波段(UV-B)[5-7]。Kieber等[8]在《Nature》上报道了海洋中高分子量的RDOM在紫外线作用下能发生光化学反应, 生成分子质量更小且具有生物活性的光降解产物, 可被浮游生物吸收利用, 从而影响海洋中碳的转移以及浮游生物食物链传递动力学。因此, 紫外线对DOM的光降解作用可对MCP的慢速循环过程进行内容补充[3]。国内也有研究指出, DOM的光降解可以延长蓝藻水华的持续时间[9]。可见DOM的光降解在海洋中元素的循环和海洋生态过程中均起着重要的作用。

在全球气候变化的大环境下, 因紫外辐射的增强而导致的生态效应无疑是一个亟需研究的科学问题。生态系统中作为基础生物的浮游细菌和浮游植物无疑对紫外线辐射增强引起的反应最为敏感, 为了加深了解DOM的光降解对浮游生物生态系统的影响, 很有必要对DOM光降解的基本过程、产物以及对浮游生物的影响进行详细阐述。

1 影响DOM光降解的环境因素

由于人类活动引起的全球气候变化(如: 紫外线增强、海水温度升高、海洋酸化等), 使海洋生态环境遭受严重影响。海洋中DOM的光降解势必也会受到这些环境因素变化的影响。1)近年来, 河口区的铁含量呈升高的趋势[10], 铁含量的增加有助于DOM吸收UV, 海水pH的降低和铁浓度增加均能提高DOM的光降解速率, 而pH的降低对DOM光降解的影响更为显著。Molot等[11]指出: 在pH低于7时, 光降解过程主要是由羟基自由基所激发。2)在盐度高的水体中, 陆源DOM光降解产生溶解无机碳(Dissolvedinorganic carbon, DIC)的速率减慢, 光漂白作用减弱[12],但光铵化以及DOM中UV254-发色团的光降解速率提升, 从而改变了DOM在光降解过程中的光吸收特性[13-14]。3)室内受控培养实验表明: 在氧饱和浓度下, DOM光降解产生DIC的速率加快, 光漂白作用增强[15-16], 这与直接光降解过程需要氧有关[17]。4)不同波长的紫外线, 其所含的能量不同, 对DOM光降解的影响也不同。Wang等[16]报道了UV-B、UV-A和可见光三个波段对DOM光降解产生溶解无机物(Dissolved inorganic matter, DIM)的贡献分别为31.8%、32.6%、25.6%。此外, 在不同季节和不同海区, UV辐射强度存在很大差异, 这无疑对DOM的光降解产生很大的影响。5)Shirokova等[18]认为在异常高温的水域中溶解有机碳(Dissolved organic carbon, DOC)的浓度降低了30%, 很可能是DOM光降解速率加快的缘故。Porcal等[19]探讨了DOM光降解产生DIC的两种可能途径, 包括DOM直接光降解产生DIC以及DOM先降解产生颗粒有机碳(Particulate organic carbon, POC)等中间产物, 再降解成DIC, 前者受低温控制, 而后者受高温控制并起到主要作用。Ren等[20]也指出了水温升高在很大程度上影响着DOM光降解产生CO的速率。此外, 海水的温度上升还会使混合层变浅, 温跃层更加明显, 上下层海水垂直混合更加困难, 导致上层海水将接收更多的太阳辐射, 使得DOM光降解和光漂白将更加剧烈[21-22]。

2 DOM的主要光降解过程和产物

2.1 DOM的主要光降解过程

DOM的主要光降解过程可分为: 直接光降解、间接光降解和Fe3+-DOM复合物的光降解[23]。

2.1.1 直接光降解

直接光降解是一种较为简单的光化学反应, 指的是DOM自身作为主要的发色团, 其直接吸收光而进行的化学反应, 其初级产物芳香性降低[24], 并能进行二次分解反应生成分子质量更小的物质[25-26]。DOM是否通过直接光降解途径取决于DOM的化学组成及其来源。有研究指出: 陆源DOM比藻源DOM展示出更强的光反应活性, 而且陆源DOM在光降解过程中产生更多具有生物活性的DOC[27-28]。

2.1.2 间接光降解

间接光降解比直接光降解常见, 指的是DOM自身不能作为发色团而直接吸收光, 需要水体中存在的天然物质(如: 腐殖质或微生物等)被光激发后, 将激发态的能量转移给化合物而导致的分解反应。其中一个重要的途径是通过羟基自由基激发[29]。由于间接光降解能改变自然水体中阻碍光降解的化学物质的分子结构, 因此它在水体中有着特别重要的作用和意义。

2.1.3 Fe3+-DOM复合物的光降解

指的是在富含铁元素的表层水中, Fe3+-DOM的羧酸盐复合体通过配体到金属的电荷转移而形成的分解反应[27, 30]。反应包括了Fe3+到Fe2+的转化和脱羧过程, 可见DOM光降解过程对铁离子的氧化还原反应有重要影响[15]。

2.2 主要光解产物

水体中的DOM光降解改变了其原有的物理性质和化学组成, 如: 芳香性降低[31]、pH值下降[32]、疏水性[33]、吸收光谱性质[34]以及分子质量大小的改变[32]。其主要的产物可以分成以下3类[35]: 1)最为常见的一类产物就是含碳气体, 包括: CO2、CO、CH4、DIC等[36-37]。2)低分子质量的有机化合物, 包括: 氨基酸、尿素、甲醛、乙醛、丙酮酸等[38-39]。3)氮和磷等无机盐, 包括: NH4+、NO2–、PO43–等[40-41]。

3 DOM光降解对浮游细菌的影响

3.1 DOM光降解对浮游细菌生长的促进与抑制作用

DOM具有吸收UV的特性, 因而富含DOM的水域无疑更能阻碍UV在水层中的穿透[42]。一方面, 高浓度的DOM可以对UV敏感的浮游细菌起到保护作用; 另一方面, UV辅射引起的DOM光化学反应可产生活性物质, 同时光漂白作用又改变加剧了UV在水域中的穿透深度。可见, DOM的光降解从多方面影响浮游细菌的群落结构和功能。UV促进了细菌生长的可能机制是在一定程度上, DOM光降解产生的活性物质在促进生长方面抵消了UV对细菌的损伤作用[8, 43]。接种在事先用UV处理过的海水中的浮游细菌可以达到更高的丰度, 表明细菌吸收利用了DOM的光化学分解产物[44]。在表层海水, 由于较高强度的UV辐射使得细菌活动受到严重的抑制, 在深5 m的表层沿岸海水, 细菌活动抑制率达到40%左右; 在贫营养盐的大洋水域, 抑制作用延伸到10 m以上, 因而UV辐射使表层海水富含活性有机物质[45]。当随着深度的增加或者通过垂直(或湍流)混合等使水层UV强度减弱, 且UV对浮游细菌的损伤由UV-A诱导的酶促反应得以修复时, 浮游细菌便能更有效地吸收光降解产物而得到更好的生长[44, 46]。

光化学转化能使DOM转化为更具活性的物质, 但也会产生相反的效应。研究表明, DOM光化学转化产生的羰基化合物, 如: 羰酸, 成为细菌分解代谢的底物[47]。此外, DOM光降解还能产生具有生物活性的NH4+-N[48]。然而, Keil和Kirchman[49]发现DOM在太阳光的照射下, 加速了活性蛋白的“老化”, 即转化为难降解的状态。UV加速“老化”的报道在藻源DOM上出现较多, 这无疑对浮游细菌的生长起到抑制作用[50]。此外, Kramer和Herndl[51]指出浮游细菌在培养过程中产生RDOM, 这种RDOM的光降解产物仍然不具生物活性, 二次培养不会促进浮游细菌的生长。一般来说, 在呈弱酸性、离子强度和叶绿素含量低、腐殖质含量高的水域, 由UV诱导的DOM光降解对细菌的生长起促进作用[52]。

由DOM的光化学转化造成营养物质结构的改变不仅影响细菌的生理功能, 还会改变细菌的群落结构[53-54]。总的来说, DOM的光降解可以改变微食物环的物质循环和能量流动, 进而影响食物链的结构与功能。

Chrost和Faust[55]指出在伯利兹珊瑚礁保护区中, 由于DOM光降解, 浮游细菌的生长率和二次生产得到提高。在北冰洋的边缘海—波弗特海, DOM光降解产生的DIM可达细菌呼吸消耗量的10%, 由于冰川的融化, DOM的光降解作用将更加显著[56]。在波罗的海, 平均每年DOC的光降解量超过了河流输入的具有光活性的DOC量, 其中用于支持浮游细菌生物量的活性光反应产物占DOC光降解产物的20%, 表明波罗的海光降解作用是陆源DOC的汇[14]。然而, 国内虽有见对DOM与污染物、抗生素和重金属化合物毒性的报道[57-58], 却鲜有DOM光降解与浮游细菌耦合的报道。

3.2 DOM光降解影响浮游细菌生长的机理

由于DOM中含有光化学和生物活性成分, 光化学和生物过程对DOM的降解起到了竞争作用。Obernosterer等[28]指出了由于富含糖类物质, 藻源DOM(以培养过程中的产物为主)比陆源DOM(以腐殖质为主)更具生物活性, 而陆源DOM则含有丰富的芳香性碳, 更具光化学活性。在陆源DOM的光转化反应过程中, 生物活性DOC含量提高了7%, 而藻源DOM没有产生生物活性DOC。此外, 生物和光对DOM的降解也有互利的作用, Amado等[59]报道了在富含腐殖酸的泻湖中, 细菌矿化作用使DOM光降解效率提高了13%, 而光降解可使细菌矿化效率提高300%。他认为在这个过程中起关键功能的物质为富含电子的氨基酸(如: 组氨酸、蛋氨酸、酪氨酸、色氨酸和半胱氨酸等)[60]。Amado等[60]还提出了新的模型: DOM光降解对细菌生长的影响除了与DOM的来源有关之外, 还与DOM的浓度有关。DOM在光降解过程中会产生一些强氧化性物质, 如: 单线态氧(Singlet oxygen), 其生成量与DOM的浓度成正相关[61-62], 而且有研究指出水域中单线态氧的含量处于被低估的状态[63]。单线态氧可以反过来降解氨基酸和其他DOM分子, 影响DOM的组成结构并抑制细菌的生长[60-61, 64]。单线态氧对浮游细菌还有毒性作用并影响细菌代谢及其种群动力学[65]。

4 DOM光降解对浮游植物的影响

普遍认为大洋区的浮游植物初级生产力表现为氮限制, 在贫营养盐的东地中海, 光铵化速率约为40 mmol/(m2·a), 与该海区大气氮沉降量相近, 可提供新生产力氮需求的12%[66]。Morell和Corredor[67]发现近海叶绿素浓度的增加与DOM的光降解有着密切的联系, 在富含DOM的河口区, 光降解过程释放大量的铵盐, 为浮游植物的生长提供了丰富的无机氮, 他们估计由光铵化作用产生的氮盐可达到浮游植物需氮量的50%。在波罗的海, 由RDOM光降解产生的生物活性氮可支持浮游植物1.2%的新生产力和3.6%需氮量[68]。而在智利中部上升流区的研究表明: 在春、夏季, 光铵化产物能支持50%~178%的浮游植物NH4+需求量[69]。可见, DOM光降解是对海洋营养盐动力学起着极其重要的作用, 特别是在贫营养盐的大洋区, 是海洋中的无机氮重要的来源之一。在光铵化对浮游植物生长的影响方面, 有学者[68]把波罗的海原有的浮游植物接种到DOM完全光降解的海水中培养发现, 受氮限制影响的浮游植物生物量得到提高。通过模型计算得出, 夏季DOM光降解产生活性氮的速率为22~26 µmol/(m2·d), 使海区叶绿素含量提高12~14 µg/(m2·d)。同时, DOM的光降解产物DIC(CO2、HCO3–、CO32–)也可以促进浮游植物的生产力。当形成藻类水华时, DOM的光降解生成DIC的速率降低, 其产量仅能支持小于3%的生产力。但研究人员认为在藻华过程中产生的DOM(即藻源DOM)更具有光化学活性, 由于海水平流交换使外源DOM成为主要成分才导致了降解速率的降低[70]。很明显, 这与目前的主流相悖, 因而在DOM光降解的耦合机制上还亟待更系统和深入的研究。此外, DOM光降解产生的活性氧产物也会对浮游植物产生损伤作用[71]。

近年来, 有害藻华、底层缺氧等水域生态灾害频繁发生, 严重地影响水域生态系统结构的稳定性, 污染水域环境, 最终危害人类健康。长期以来, 人类活动所造成的水体富营养化被认为是引起蓝藻水华的最主要因素。而且, 由于水温上升导致的跃层的扩大、风速的减弱、光照强度和时间的增加均有助于蓝藻水华的爆发[72]。有研究指出, DOM的光降解也会延长蓝藻水华的持续时间[9]。一方面, 相对于其他藻类, 蓝藻对于太阳光辐射具有更强的耐受性[73], 另一方面, 在适应不断恶化的生态环境过程中, 蓝藻已形成一定的自我保护机制, 如: 迁移到更深的水层避开高强度的辐射[74]; 超氧化物歧化酶(Superoxide Dismutase, SOD)、过氧化氢酶(Catalase, CAT)等抗氧化机制清除细胞内的过氧化合物[75-76]; 合成细胞外多糖[77]; 分泌具有吸收UV作用的化学物质, 如: 类菌胞素氨基酸(Mycosporine-like amino acids, MAAs)[78-79]以及伪枝藻素(Scytonemin, SCY)[80]; 通过修复和更新损伤的DNA和蛋白质, 如: 切除修复[81-82]、SOS反应[83]、光合系统II(PSII)蛋白的重新合成[84]; 通过细胞凋亡清除损伤严重的细胞[85]等。

5 DOM光降解对食物网的影响

浮游植物和浮游细菌作为海洋生态系统中的主要生产者和分解者, DOM光降解对其生物量和群落产生的变化必然会通过食物网传递影响上级营养级。这方面的研究报道先见于湖泊, De Lange等[86]通过培养实验表明: 由紫外线造成的DOC光降解提高了微食物环中浮游细菌、低级的异养以及兼养生物的生物量。但其用于培养实验的浮游生物来源于实验室, 因此不能很好地指示自然环境状态。Daniel等[87]研究了湖泊DOM光降解产物对异养微食物环的影响, 其研究发现DOM光降解提高了湖泊中总的浮游细菌、原生以及后生浮游动物的生物量。对于富营养盐的水体, DOM光降解没有引起明显的群落变化, 但对于腐殖质水体, 鞭毛虫、轮虫、无节幼体以及枝角类的生物量有显著提高。而在海洋方面的报道, Vähätalo等[88]研究了波罗的海近岸海域DOM光降解对浮游细菌为起点的三个营养级的影响, 其研究也表明了DOM光降解的促进作用。Stepanauskas等[89]在圣华金河口三角洲的研究指出, 由于具有生物活性DOC的含量够低, 以DOC为基础的微食物网每年仅能支持小于0.6×109g C的原生动物生产力, 相当于17×109g C的初级生产力, 即使DOC的光降解使其生物活性降低40%也不会对浮游动物以及鱼类的营养需求产生重要的影响。目前, 人类活动所导致的污染物质过多排放、冰川和冻土的融化、极端气候现象发生频率的升高等提高了河流和海洋中的DOM含量[90-92]。DOM光降解对水域生态系统功能和结构的影响将更加显著, 特别是沿岸海域。然而, DOM光降解对浮游植物食物网以及更高营养级的影响的研究仍然很缺乏。

6 研究展望

一方面, 由于全球气候变化和人类活动的影响, 使河流以及海洋中DOM的浓度不断升高; 另一方面, 由于臭氧层的削薄, 使更多的紫外线能达到地球表面。紫外线使DOM发生的光降解反应在碳、磷等生源要素的生物地球化学循环以及海洋生态过程有着越来越重要的影响。国外学者在这方面开展的研究相对较多, 主要包括: DOM光降解与浮游细菌和浮游植物的耦合及其对海洋生产力以及微食物网结构的影响、DOM光降解机理和产物、还有在污水处理方面的应用等[93]。然而国内相关的工作较少, 多见于DOM与污染物和重金属化合物的毒性以及陆地土壤DOM迁移、转化方面的报道。近年来, 国内虽有对水域生态系统中, DOM光降解产物、降解速率、对藻华的影响以及利用三维荧光光谱分析手段对DOM光降解特征和动力学方面的研究[94-95], 但仍有不少问题亟待进一步研讨:

(1) 由于DOM的成分复杂, 对于来源与化学组成不同的DOM, 其光降解过程不同, 产物也不一致。此外, DOM的光降解过程与环境因素直接相关, 而且环境因子对于DOM的光降解是联合起作用的。因此, 需要对DOM的来源和组成成分进行分类、对影响DOM的光降解的环境因子进行整合, 筛选主要环境因子, 构建其反应过程模型。

(2) 需要针对典型海区开展DOM光降解及其生态效应研究(如: 热带珊瑚礁海区)。DOM具有吸收UV的作用可以减轻珊瑚礁生态系统的环境压力, 同时活性光降解产物为其带来营养物质, 通过食物网的传递促进其生产力。DOM的光降解作用可为珊瑚礁生态系统“低营养盐, 高生产力和生物多样性”的特征研究提供新思路。

(3) 以往的研究着重于对不同来源DOM的光化学反应, 很少有考虑到水体中DOM浓度的变化。然而, 由于人类活动和全球气候变化使淡水流域中DOM浓度升高, 进而随着江河流入海洋, 对海洋DOM的含量和组成成分有重要影响。因此, 有必要对陆源的DOM进行精确的成分分析, 并对DOM浓度升高和光降解对水域生态系统的影响进行研究。

(4) 对DOM的光降解进行长期观察和大尺度的研究, 从而更准确地把握其生态效应和对水域生态系统响应的预测。

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Photodegradation of dissolved organic matter and its effect on bacterioplankton and phytoplankton

ZHOU Wei-hua1, 2, LIAO Jian-zu1, 2, 3, GUO Ya-juan1, 2, 3, YUAN Xiang-cheng1, 2, HUANG Hui1, 2, LIU Sheng1, 2, LI Tao1, 2

(1. Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China; 2. Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences, Sanya 572000, China; 3. University of Chinese Academy of Sciences, Beijing 100049, China)

As the largest dynamic reservoir of organic carbon in the ocean, photodegradation of dissolved organic matter (DOM) under ultraviolet radiation (UV) has important effects on the biogeochemical cycles of biogenic elements, as well as on the structure and function of the marine ecosystem. This article summarizes the environmental factors that affect the photodegradation processes and products of DOM. In addition, the effects of photodegradation of DOM on bacterioplankton and phytoplankton are discussed. Owing to the different sources and complex compositions of DOM, the ecological effects of photodegradation are spatially different. Hence, further comprehensive studies are crucially needed to evaluate the ecological effects of photodegradation of DOM in different sea areas.

dissolved organic matter; photodegradation; ultraviolet radiation; bacterioplankton; phytoplankton

P76

A

1000-3096(2017)02-0136-09

10.11759/hykx20151214003

2015-12-14;

2016-04-17

国家自然科学基金(No.31370500, No.40806050, No.31370499)

周伟华(1976-), 男, 浙江东阳人, 博士, 研究员, 主要从事海洋生态环境研究, 电话, 020-89023225, Email: whzhou@scsio.ac.cn

Dec. 14, 2015

[National Natural Science Foundation of China, No. 31370500, No. 40806050, No. 31370499]

(本文编辑: 康亦兼)