葉琳琳，孔繁翔,史小麗，陽(yáng) 振，閆德智，張 民

(1. 南通大學(xué)地理科學(xué)學(xué)院，南通 226000；2. 中國(guó)科學(xué)院南京地理與湖泊研究所湖泊與環(huán)境國(guó)家重點(diǎn)實(shí)驗(yàn)室，南京 210008)

富營(yíng)養(yǎng)化湖泊溶解性有機(jī)碳生物可利用性研究進(jìn)展

葉琳琳1，孔繁翔2，*,史小麗2，陽(yáng) 振2，閆德智1，張 民2

(1. 南通大學(xué)地理科學(xué)學(xué)院，南通 226000；2. 中國(guó)科學(xué)院南京地理與湖泊研究所湖泊與環(huán)境國(guó)家重點(diǎn)實(shí)驗(yàn)室，南京 210008)

富營(yíng)養(yǎng)化湖泊溶解性有機(jī)碳(DOC)包括內(nèi)源和外源性碳源，不同來(lái)源碳源在物質(zhì)化學(xué)結(jié)構(gòu)組成和分子量級(jí)等方面具有顯著差異，進(jìn)而影響到對(duì)細(xì)菌的生物可利用性和碳素在食物網(wǎng)中的傳遞效率。根據(jù)國(guó)內(nèi)外文獻(xiàn)，綜述了內(nèi)外源DOC在碳穩(wěn)定同位素值域上的顯著差異，建議通過(guò)對(duì)DOC碳穩(wěn)定同位素的分析來(lái)識(shí)別富營(yíng)養(yǎng)化湖泊中DOC的主要來(lái)源；通過(guò)對(duì)比內(nèi)外源DOC在碳水化合物、結(jié)合態(tài)中性糖和腐殖質(zhì)含量上的差異，并結(jié)合細(xì)菌生長(zhǎng)參數(shù)如細(xì)菌二級(jí)生產(chǎn)力、細(xì)菌呼吸作用及細(xì)菌生長(zhǎng)效率來(lái)分析內(nèi)外源DOC對(duì)細(xì)菌的生物可利用性。從富營(yíng)養(yǎng)化湖泊DOC來(lái)源的角度探討其生物可利用性和碳素傳遞效率，有助于了解富營(yíng)養(yǎng)化湖泊食物網(wǎng)中碳素循環(huán)特征，加強(qiáng)對(duì)湖泊生態(tài)學(xué)的認(rèn)識(shí)，為湖泊環(huán)境治理與保護(hù)提供科學(xué)依據(jù)。

富營(yíng)養(yǎng)化湖泊; 溶解性有機(jī)碳; 來(lái)源; 生物可利用性; 綜述

溶解性有機(jī)碳(DOC)在水體中主要以溶解性有機(jī)物(DOM)形式存在，是浮游細(xì)菌生長(zhǎng)的重要碳源。通過(guò)細(xì)菌的呼吸作用(BR)，部分DOC以二氧化碳的形式被釋放。另一部分DOC通過(guò)細(xì)菌吸收利用合成二級(jí)生產(chǎn)力(BP)，所形成的細(xì)胞顆粒通過(guò)浮游動(dòng)物的攝食再進(jìn)入傳統(tǒng)食物鏈[1- 2]。研究人員用細(xì)菌生長(zhǎng)效率(BGE=BP/[BP+BR])來(lái)表征DOC中碳源通過(guò)浮游細(xì)菌傳遞到更高營(yíng)養(yǎng)級(jí)別的效率[3- 4]。但是，DOC的來(lái)源、生物化學(xué)結(jié)構(gòu)組成及形態(tài)存在顯著差異，進(jìn)而影響其降解程度及細(xì)菌對(duì)其吸收利用途徑[5]。

DOC的生物可利用性一直是生態(tài)系統(tǒng)研究的重點(diǎn)與熱點(diǎn)。S?ndergaard 和 Middelboe[6]系統(tǒng)總結(jié)了湖泊，河流和海洋中126項(xiàng)DOC的研究表明，DOC中可利用組分與DOC總濃度顯著正相關(guān)，其中湖泊中DOC可利用組分所占比例為14%。Yokokawa 和 Nagata[7- 8]在日本Otsuchi 灣研究發(fā)現(xiàn)，DOC到浮游細(xì)菌的碳通量為23μg C L-1d-1，所形成的細(xì)菌二級(jí)生產(chǎn)力再被浮游動(dòng)物攝食，產(chǎn)生的碳通量為7μg C L-1d-1。Carpenter等[9]對(duì)不同營(yíng)養(yǎng)級(jí)別的湖泊研究發(fā)現(xiàn)，在貧營(yíng)養(yǎng)湖泊中，DOC來(lái)源以外源輸入為主，外源性DOC在湖泊中的降解常數(shù)為0.0001—0.01/d[10]。在亞馬遜河Batata湖研究發(fā)現(xiàn)，高水位期間，水體DOC以外源性為主，低水位期間，DOC以?xún)?nèi)源性為主，而低水位期間細(xì)菌BGE值要高于高水位期間[11]。但是，外源性DOC對(duì)細(xì)菌二級(jí)生產(chǎn)力的貢獻(xiàn)率，DOC分子量級(jí)的高低及腐殖質(zhì)含量對(duì)其生物可利用性的影響至今還存在分歧[12- 15]。因此，本文從DOC來(lái)源的角度綜述了內(nèi)外源DOC生物可利用性及其在碳素代謝途徑和效率方面的顯著差異，為今后深入研究富營(yíng)養(yǎng)化湖泊生態(tài)系統(tǒng)中碳素循環(huán)機(jī)理和湖泊環(huán)境保護(hù)提供參考依據(jù)。

1 溶解性有機(jī)碳的來(lái)源與區(qū)分

利用碳穩(wěn)定同位素技術(shù)可以追溯有機(jī)物的來(lái)源，但目前的溯源研究主要集中在顆粒態(tài)有機(jī)物(POM)方面[16- 18]。Gu 等[19]對(duì)32個(gè)淡水湖泊δ13CPOM進(jìn)行統(tǒng)計(jì)分析，研究結(jié)果表明，δ13CPOM年變化值域中最大值與湖泊富營(yíng)養(yǎng)化參數(shù)(總氮、總磷、葉綠素)顯著正相關(guān)。Heligings等[16]在比利時(shí)Scheldt河口研究發(fā)現(xiàn)，夏季POM的主要來(lái)源為浮游植物，而冬季以陸源輸入為主。曾慶飛[20]在太湖研究發(fā)現(xiàn)，夏季POM的主要來(lái)源為藍(lán)藻，并且δ13C浮游動(dòng)物與δ13CPOM大量重疊，表明浮游動(dòng)物攝食了部分藍(lán)藻。但是以碳穩(wěn)定同位素特征值為工具對(duì)富營(yíng)養(yǎng)化湖泊DOC進(jìn)行溯源，繼而深入研究其生物可利用性的研究還較少。

DOC按其來(lái)源可分為內(nèi)源性和外源性DOC。內(nèi)源性DOC主要來(lái)源于浮游植物光合作用產(chǎn)物的釋放以及內(nèi)源性碎屑物質(zhì)的分解[21]。研究發(fā)現(xiàn)，淡水湖泊藻類(lèi)的碳穩(wěn)定同位素δ13C在-35‰—-25‰[22]。外源性DOC主要來(lái)源于陸源的流域輸入，而多數(shù)陸生植物的光合作用主要通過(guò)C3途徑把大氣中CO2(δ13C≈-7‰)合成有機(jī)物，其δ13C為-27‰[23]。因此，不同來(lái)源有機(jī)物δ13C存在差異且值域重疊少，通過(guò)碳穩(wěn)定同位素特征值可以追溯有機(jī)物的來(lái)源，這為區(qū)分內(nèi)外碳源對(duì)有機(jī)物的貢獻(xiàn)提供了有力保障[24- 25]。

在日本富營(yíng)養(yǎng)化淺水湖泊霞浦湖研究發(fā)現(xiàn)，δ13CDOM變化范圍為-25.9‰—-24.2‰，并且春季δ13CDOM值高于秋季，表明DOC來(lái)源存在季節(jié)性變化規(guī)律，春季藻類(lèi)水華期間DOC主要來(lái)源是內(nèi)源性碳[26]。在美國(guó)威斯康辛州Northern Highland湖區(qū)的32個(gè)湖泊研究發(fā)現(xiàn)，δ13CDOM變化范圍為-22.9‰—-29.3‰，部分湖泊δ13CDOM與陸源C3植物碳穩(wěn)定同位素特征值(-27‰)相似，表明其DOC主要來(lái)源為外源輸入，內(nèi)源性DOC所占比例低于25%，而在δ13CDOM與δ13CPOM(顆粒態(tài)有機(jī)物)值域接近的湖泊中，內(nèi)源性碳對(duì)DOC的貢獻(xiàn)較高[27- 28]。但是也有研究發(fā)現(xiàn)有無(wú)藻類(lèi)水華，法國(guó)Rohemel 水庫(kù)δ13CDOM(-28.1‰—-28.6‰)與外源性δ13CDOM(-28.6‰)相似，DOC來(lái)源以外源性碳為主[29]。在蘇格蘭Loch Lomond湖泊研究發(fā)現(xiàn)，內(nèi)源性DOC的形成不足以改變水體中DOC的碳穩(wěn)定同位素特征值，雖然δ13CDOM在6—9月期間有顯著增長(zhǎng)趨勢(shì)，變化范圍為-29.0‰—-28.4‰，但是仍然屬于外源性DOC碳穩(wěn)定同位素值域，表明外源性DOC是水體中DOC的主要來(lái)源[30]。因此，通過(guò)DOC碳穩(wěn)定同位素特征值的變化特征，可以區(qū)分水體中DOC的主要來(lái)源途徑。

2 溶解性有機(jī)碳的化學(xué)結(jié)構(gòu)組成對(duì)其生物可利用性的影響

2.1 溶解性有機(jī)碳中碳水化合物含量對(duì)其生物可利用性的影響

DOC物質(zhì)結(jié)構(gòu)組成復(fù)雜，研究人員對(duì)其中部分物質(zhì)的化學(xué)結(jié)構(gòu)還不清楚，但溶解性總碳水化合物(TCHO)在目前可識(shí)別的DOC組分中所占比例最高，是細(xì)菌生長(zhǎng)代謝的重要物質(zhì)基礎(chǔ)，與顯色劑2,4,6-反式2-吡啶基三嗪(2,4,6-tripyridyl-s-triazine, TPTZ)可生成紫色絡(luò)合產(chǎn)物，通過(guò)紫外分光光度計(jì)在595nm處測(cè)定[31- 34]。在匈牙利富營(yíng)養(yǎng)化湖泊，TCHO在DOC中比例為15%—20%[35]。有研究發(fā)現(xiàn)，TCHO/DOC可以表征DOC生物可利用性[36- 37]。在印度Mandovi河口，細(xì)菌數(shù)量與TCHO/DOC顯著負(fù)相關(guān)，表明細(xì)菌通過(guò)分解碳水化合物來(lái)提供其物質(zhì)代謝的主要碳源[38]。而有研究發(fā)現(xiàn)，在浮游植物水華過(guò)程中，溶解性結(jié)合態(tài)中性糖(DCNS)在碳水化合物中比例高達(dá)54%，能為細(xì)菌生長(zhǎng)提供重要碳源[39- 40]。

2.2 溶解性有機(jī)碳的分子量級(jí)對(duì)其生物可利用性的影響

DOC按其分子量級(jí)可分為高分子溶解性有機(jī)碳(HMWDOC)和低分子量溶解性有機(jī)碳(LMWDOC)。但對(duì)于不同量級(jí)組分生物利用性的認(rèn)識(shí)，還一直存在爭(zhēng)議。Amon 和 Benner[14,41]認(rèn)為HMWDOC生物可利用性要高于LMWDOC。在墨西哥灣Saint Louis河口，研究發(fā)現(xiàn)HMWDOC組分容易被細(xì)菌分解利用，TCHO在HMWDOC所占比例(53%—73%)要顯著高于在DOC中比例(10%—31%)[42]。但也有研究認(rèn)為L(zhǎng)MWDOC具有較高生物活性，細(xì)菌對(duì)LMWDOC組分中TCHO利用效率(76%)要顯著高于HMWDOC組分(46%)[33,43- 44]。

2.3 溶解性有機(jī)碳中腐殖質(zhì)含量對(duì)其生物可利用性的影響

腐殖質(zhì)(HS)也是DOC中重要的物質(zhì)組成，其所占比例可高達(dá)80%[45]。在匈牙利Balaton湖的入湖河流River Zala和湖區(qū)東部，HS在DOC中所占比例分別為75%和50%[46]。一般認(rèn)為，腐殖質(zhì)物質(zhì)不容易被細(xì)菌分解利用[15,47]。美國(guó)卡羅來(lái)納L湖，HS在DOC所占比例為50%，對(duì)細(xì)菌生產(chǎn)力的貢獻(xiàn)為22%[48]。在挪威Kjels?sputten湖，細(xì)菌對(duì)DOC中的HS吸收利用效率低于10%[49]。研究發(fā)現(xiàn)在德國(guó)富含腐殖質(zhì)的湖泊(Schwarze kuhle)和清水湖(Sch?hsee)，DOC中生物活性組分的含量沒(méi)有顯著差異，約為15%—22%[50]。 但近來(lái)有研究發(fā)現(xiàn)，HS濃度對(duì)其生物可利用性具有重要影響[51- 52]，在匈牙利Balaton湖，HS濃度與DOC中生物活性組分濃度之間顯著正相關(guān)[53]。在波蘭富營(yíng)養(yǎng)化湖泊Jeziorak，添加HS濃度為25 mg/L 時(shí)細(xì)菌數(shù)量達(dá)到最大值[54]。James[55]也研究發(fā)現(xiàn)，在富含HS的湖泊中，HS濃度不超過(guò)20 mg/L，其對(duì)細(xì)菌生長(zhǎng)具有促進(jìn)作用。

3 內(nèi)源性溶解性有機(jī)碳生物可利用性及其對(duì)浮游植物水華生消的響應(yīng)

有研究認(rèn)為，富營(yíng)養(yǎng)化湖泊比寡營(yíng)養(yǎng)和中度富營(yíng)養(yǎng)化湖泊中DOC含量高[56- 59]，其原因是富營(yíng)養(yǎng)化湖泊中，浮游植物水華過(guò)程會(huì)導(dǎo)致DOC濃度顯著升高。在日本富營(yíng)養(yǎng)化湖泊Nakanuma春季水華暴發(fā)期間，DOC的產(chǎn)生速率是2.8 μmol L-1d-1[60]。在丹麥富營(yíng)養(yǎng)化湖泊Frederiksborq Slotss?春季硅藻水華消亡期間，DOC的產(chǎn)生速率是9 μ L-1d-1[61]。德國(guó)中富營(yíng)養(yǎng)化湖泊康士坦茨湖硅藻水華暴發(fā)時(shí)DOC濃度達(dá)到峰值，表明有新的DOC形成[62]。有研究發(fā)現(xiàn)在超富營(yíng)養(yǎng)化湖泊太湖的貢湖灣湖區(qū)，春夏季藍(lán)藻水華期間，DOC濃度升高，并與葉綠素濃度顯著正相關(guān)[63]。以上研究結(jié)果表明，浮游植物水華生消過(guò)程中，DOC濃度會(huì)顯著增加，并且主要是來(lái)源于內(nèi)源性DOC的形成。

有研究發(fā)現(xiàn)，浮游植物細(xì)胞內(nèi)碳水化合物含量為13%—35%，在浮游植物水華過(guò)程中，由于藻細(xì)胞的胞外釋放、被浮游動(dòng)物攝食和細(xì)胞自然裂解，細(xì)胞內(nèi)碳水化合物會(huì)釋放到水體中從而改變DOC中碳水化合物含量[64- 65]。在富營(yíng)養(yǎng)化湖泊巢湖夏季藍(lán)藻水華期間，TCHO在DOC中比例為26%[66]。在圍格內(nèi)模擬硅藻水華，新產(chǎn)生的DOC中有16%是由DCNS組成[67]。在美國(guó)Delaware河口春季水華過(guò)后的4—5月間，DCNS濃度在DOC中所占比例為4%—12%[68]。

此外，浮游植物水華過(guò)程會(huì)對(duì)DOC的分子量級(jí)產(chǎn)生影響[63,69- 70]。Gobler和 Saudo-Wilhelmy[71]在美國(guó)Pecomic河口研究發(fā)現(xiàn)浮游植物暴發(fā)期間，HMWDOC含量顯著增加，LMWDOC含量基本保持不變，而在水華消亡過(guò)程中，LMWDOC成為水體中有機(jī)碳主要組分。孫小靜等[72]通過(guò)室內(nèi)模擬實(shí)驗(yàn)研究發(fā)現(xiàn)，藍(lán)藻水華在降解的過(guò)程中會(huì)釋放大量的HMWDOC。Hama等[73]通過(guò)碳穩(wěn)定同位素示蹤研究發(fā)現(xiàn)，浮游植物經(jīng)過(guò)光合作用后，在黑暗中釋放的DOC產(chǎn)物主要以HMWDOC為主。

相對(duì)于外源性DOC來(lái)說(shuō)，新產(chǎn)生的內(nèi)源性DOC富含碳水化合物，因此轉(zhuǎn)化周期短，可以很快被細(xì)菌分解利用，從而參與到微食物網(wǎng)中碳素傳遞過(guò)程[74- 77]。TCHO和DCNS都是細(xì)菌生長(zhǎng)代謝的重要碳源，在德國(guó)中富營(yíng)養(yǎng)化康士坦茨湖研究發(fā)現(xiàn)，春季水華暴發(fā)和消亡期，細(xì)菌對(duì)TCHO的利用效率最高[78]。此外，實(shí)驗(yàn)?zāi)M的水華產(chǎn)生的DCNS有70%—80%能在35d內(nèi)被降解[79]。另有研究發(fā)現(xiàn)，浮游植物水華產(chǎn)生的DCNS有91%能在15 d內(nèi)被降解[80]。在羅斯海，浮游植物水華暴發(fā)期間，DCNS濃度增加了3倍，在DOC易降解組分中所占比例達(dá)到50%[40]。在內(nèi)源性DOM的降解實(shí)驗(yàn)中發(fā)現(xiàn)，30%的DOC被細(xì)菌分解利用，DCNS在DOC中比例從實(shí)驗(yàn)初期的14%降低到實(shí)驗(yàn)結(jié)束后的5%[81]。此外，有研究發(fā)現(xiàn)，浮游植物水華過(guò)程中產(chǎn)生的內(nèi)源性HMWDOC生物可利用性高，比LMWDOC轉(zhuǎn)化速率快[71,73]。綜上所述，浮游植物水華生消過(guò)程會(huì)改變DOC濃度、物質(zhì)結(jié)構(gòu)組成及分子量級(jí)，進(jìn)而改變其生物可利用性。

在比利時(shí)富營(yíng)養(yǎng)化淺水湖泊Blankaart，浮游細(xì)菌生長(zhǎng)主要以?xún)?nèi)源性DOC為主[82]。有研究發(fā)現(xiàn)13%的內(nèi)源性DOC支持了30%—65%的細(xì)菌生長(zhǎng)代謝活動(dòng)[79]。在太湖研究發(fā)現(xiàn)，浮游植物降解產(chǎn)生的內(nèi)源性DOC可能是細(xì)菌生長(zhǎng)的重要碳源[83]。在波蘭馬祖里湖區(qū)，對(duì)深水的中度富營(yíng)養(yǎng)化湖泊Kuc、富營(yíng)養(yǎng)化湖泊Ryńskie和超富營(yíng)養(yǎng)化淺水湖泊Szymon進(jìn)行調(diào)查，研究發(fā)現(xiàn)DOC主要來(lái)源于內(nèi)源性DOC，細(xì)菌生產(chǎn)力和葉綠素濃度顯著正相關(guān)(表1)，結(jié)果表明細(xì)菌生長(zhǎng)的碳源主要來(lái)源于內(nèi)源性DOC[84]。有研究發(fā)現(xiàn)，進(jìn)行營(yíng)養(yǎng)鹽添加增大湖泊初級(jí)生產(chǎn)力，有利于提高微生物對(duì)內(nèi)源性DOC的利用份額。在添加了氮磷營(yíng)養(yǎng)鹽的Peter湖，內(nèi)源性DOC對(duì)異養(yǎng)生物呼吸的貢獻(xiàn)從60%增大到88%[85]。在芬蘭中腐殖質(zhì)湖泊 P??j?rvi，夏季浮游植物水華過(guò)程中釋放的內(nèi)源性DOC含有較高生物可利用性組分，細(xì)菌BGE達(dá)到26%[86]。綜上所述，浮游植物水華過(guò)程中產(chǎn)生的內(nèi)源性DOC富含碳水化合物，結(jié)合態(tài)中性糖，具有較高生物可利用性，在湖泊微食物網(wǎng)碳素循環(huán)中具有重要作用。

但內(nèi)源性DOC中也有部分組分不易降解[52,87]。在日本富營(yíng)養(yǎng)化淺水湖泊霞浦湖湖心區(qū)域，內(nèi)源性DOC中不易降解組分濃度從秋季到冬季有所增長(zhǎng)[88]。有研究發(fā)現(xiàn)，部分內(nèi)源性DOC能在水里保留1a以上不降解[89]。在添加了營(yíng)養(yǎng)鹽進(jìn)行的圍格實(shí)驗(yàn)中，研究發(fā)現(xiàn)實(shí)驗(yàn)46d后，新產(chǎn)生的內(nèi)源性DOC中有32%難以降解[80]。實(shí)驗(yàn)?zāi)M產(chǎn)生的水華形成的內(nèi)源性DOC中有25%—30%在2.5a后，仍難以被礦化和利用[87]。研究還發(fā)現(xiàn)在淡水圍格中，硅藻水華形成階段，難降解DOC組分含量較高[77]。此外，浮游植物水華在消亡過(guò)程中受到磷元素的限制作用，也會(huì)產(chǎn)生大量難降解的DOC組分[90]。

表1 不同營(yíng)養(yǎng)級(jí)別湖泊中葉綠素，溶解性有機(jī)碳和細(xì)菌生產(chǎn)力的變化

4 外源性溶解性有機(jī)碳的生物可利用性

在貧營(yíng)養(yǎng)的湖泊中，外源性DOC含量要顯著高于內(nèi)源性DOC[9,91]。Carpenter等[9]在2001年和2002年選取威斯康辛州Paul、Peter和Tutesday湖為研究對(duì)象，研究結(jié)果見(jiàn)表2。Bade[28]也發(fā)現(xiàn)沒(méi)有進(jìn)行營(yíng)養(yǎng)鹽添加的湖泊，80%—90%的DOC來(lái)源于外源性DOC。Cole 等[92]通過(guò)C13示蹤，發(fā)現(xiàn)在富含腐殖質(zhì)的美國(guó)East Long湖泊中，外源性DOC在總有機(jī)碳中所占比例高達(dá)90%。綜上所述，在貧營(yíng)養(yǎng)和富含腐殖質(zhì)的湖泊中，外源性DOC所占比例高。

表2 不同營(yíng)養(yǎng)級(jí)別湖泊中外源性DOC貢獻(xiàn)率

2001年沒(méi)有對(duì)Paul 和Peter湖添加營(yíng)養(yǎng)鹽；2002年對(duì)Peter 湖添加營(yíng)養(yǎng)鹽；Tuesday湖為貧營(yíng)養(yǎng)湖泊

以往的研究認(rèn)為外源性DOC主要以腐殖質(zhì)物質(zhì)存在，分子量高，氮磷比低，具有芳香性，不易被微生物所利用[93- 94]。有研究發(fā)現(xiàn)，在德國(guó)貧營(yíng)養(yǎng)湖泊Groβe Fuchskuhle西部湖區(qū)，DOC以外源性為主，其中HS所占比例達(dá)到58%[95]。在日本富營(yíng)養(yǎng)化淺水湖泊霞浦湖湖心，外源性DOC是DOC中不易降解組分的主要來(lái)源[88]。在芬蘭富含腐殖質(zhì)的Mekkoj?rvi湖研究發(fā)現(xiàn)95%的外源性DOC不能被細(xì)菌分解利用[86]。

但近來(lái)有研究發(fā)現(xiàn)，很多湖泊屬于異養(yǎng)型，整個(gè)湖泊生態(tài)系統(tǒng)的呼吸作用(R)大于總初級(jí)生產(chǎn)力(GPP)。因此，外源性有機(jī)碳是湖泊物質(zhì)代謝過(guò)程中的重要補(bǔ)充[96- 98]。有研究發(fā)現(xiàn)，在未添加營(yíng)養(yǎng)鹽的湖泊中，外源性有機(jī)碳對(duì)浮游動(dòng)物碳源的貢獻(xiàn)率為22%—75%[8]。在營(yíng)養(yǎng)不良的Tuesday湖，外源性DOC對(duì)異養(yǎng)生物呼吸的貢獻(xiàn)率達(dá)到68%[86]。在挪威中腐殖質(zhì)湖泊Kjels?sputten[49]和瑞典?rtr?sket湖[99]，90%的細(xì)菌生產(chǎn)力來(lái)源于外源性DOC。在瑞典12個(gè)湖泊中研究發(fā)現(xiàn)，細(xì)菌二級(jí)生產(chǎn)力和呼吸作用均與外源性DOC顯著正相關(guān)(圖1)，但其中90%的DOC是用于細(xì)菌呼吸作用，因此BGE較低[100]。在East Long湖研究發(fā)現(xiàn)DOC以外源性為主，細(xì)菌BGE僅為4%[92]。有研究發(fā)現(xiàn)，內(nèi)源性DOC營(yíng)養(yǎng)價(jià)值高，碳氮比值約為12∶1，而外源性DOC碳氮比值約為50∶1[101]，不同來(lái)源DOC營(yíng)養(yǎng)價(jià)值的差異會(huì)影響細(xì)菌的生長(zhǎng)效率BGE, 有研究表明BGE與生長(zhǎng)基質(zhì)中碳氮比值具有負(fù)相關(guān)性[102]。因此，以外源性DOC為碳源，細(xì)菌生長(zhǎng)效率低[11- 12,17]。Kritzberg等[12]研究發(fā)現(xiàn)在異養(yǎng)型湖泊中，細(xì)菌的二級(jí)生產(chǎn)力和內(nèi)源性DOC具有顯著相關(guān)性，表明被細(xì)菌吸收的外源性DOC不可能被傳遞到上一層消費(fèi)者，在食物網(wǎng)中碳素傳遞效率低。

圖1 瑞典12個(gè)湖泊中細(xì)菌二級(jí)生產(chǎn)力BP、呼吸量BR與外源性溶解性有機(jī)碳的變化趨勢(shì)Fig.1 The variation of bacteria production, bacteria respiration and allochthonous dissolved organic carbon in twelve lakes in Sweden

此外有研究發(fā)現(xiàn)，外源性DOC分子量級(jí)組成對(duì)BGE具有顯著影響[103- 104]。Berggren等[13]研究發(fā)現(xiàn)，外源性DOC中LMWDOC對(duì)細(xì)菌、原生動(dòng)物和后生動(dòng)物二級(jí)生產(chǎn)力的貢獻(xiàn)分別為80%、54%和23%，通過(guò)攝食浮游細(xì)菌，這部分碳源可被有效地傳遞到更高營(yíng)養(yǎng)級(jí)別。在瑞典的溪流和湖泊中，研究發(fā)現(xiàn)細(xì)菌BGE隨著外源性DOC中LMWDOC濃度的升高而增大[105]。新的外源性DOC中，細(xì)菌的BGE高達(dá)50%，陳年的外源性DOC中BGE只有10%，可能是其中LMWDOC組分耗竭所致[106- 108]。但在芬蘭富含腐殖質(zhì)的Mekkoj?rvi Lake，細(xì)菌吸收利用了外源性DOC中30%的LMWDOC，BGE只有3%，而吸收利用4%的HMWDOC，BGE達(dá)到26%，表明外源性DOC中HMWDOC組分比LMWDOC組分營(yíng)養(yǎng)價(jià)值高[86]。 綜上所述，外源性DOC也是湖泊食物網(wǎng)中碳循環(huán)的重要補(bǔ)充，但其分子量級(jí)對(duì)其生物可利用性具有重要影響。

5 結(jié)論與展望

DOC是湖泊生態(tài)系統(tǒng)食物網(wǎng)的重要做成部分。目前，國(guó)內(nèi)就富營(yíng)養(yǎng)化湖泊中浮游植物水華過(guò)程對(duì)DOC濃度和形態(tài)等方面開(kāi)展了大量的工作[69,109]，張運(yùn)林等利用三維熒光對(duì)太湖溶解性有機(jī)碳的來(lái)源也進(jìn)行了分析[110- 111]，并取得了豐富的研究成果。但從DOC來(lái)源的角度，探索其生物可利用性、碳素代謝途徑和效率以及DOC-細(xì)菌-浮游植物相互關(guān)系的研究較少。

隨著人們對(duì)湖泊生態(tài)系統(tǒng)中碳循環(huán)機(jī)理的深入研究，有關(guān)DOC來(lái)源及生物可利用性對(duì)浮游植物水華過(guò)程的響應(yīng)急需得到進(jìn)一步加強(qiáng)。通過(guò)碳穩(wěn)定同位素技術(shù)，可以明確富營(yíng)養(yǎng)化湖泊中DOC的主要來(lái)源。通過(guò)對(duì)不同來(lái)源DOC中碳水化合物、溶解性結(jié)合態(tài)中性糖、分子量級(jí)和腐殖質(zhì)的分析，并結(jié)合細(xì)菌生長(zhǎng)參數(shù)，可以明確不同來(lái)源DOC生物可利用性的顯著差異，及其在湖泊食物網(wǎng)碳循環(huán)中作用和碳傳遞效率，為今后深入研究湖泊生態(tài)系統(tǒng)碳素循環(huán)機(jī)制和生態(tài)系統(tǒng)穩(wěn)定性提供參考依據(jù)。

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The bioavailability of dissolved organic carbon in the eutrophic lakes

YE Linlin1, KONG Fanxiang2,*, SHI Xiaoli2, YANG Zhen2, YAN Dezhi1, ZHANG Min2

1GeographicalSciencesCollege,NantongUniversity,Nantong226000 2StateKeyLaboratoryofLake&EnvironmentalScience,NanjingInstituteofGeographyandLimnology,ChineseAcademyofSciences,Nanjing210008,China

The dissolved organic carbon (DOC) pool is composed of both autochthonous and allochthonous DOC, and its concentration in lakes generally increases with the trophic status. Accumulation of the autochthonous DOC was observed in the eutrophic lake, and the allochthonous DOC was highest in the dystrophic lake. Carbohydrates constitute a large component of the DOC, the consumption of DOC by heterotrophic bacteria is one of the largest fluxes of carbon in most aquatic ecosystems, but the bioavailability and the efficiency of carbon transfer in lakes food web is affected by the distribution of molecular weight and chemical composition. The DOC can be separated into high and low molecular weight DOC fractions by cross-flow ultrafiltration, but which fraction is more bioreactive is still in dispute.

Stable carbon isotope can be used to trace the origins of organic carbon, and the approach depends on the fact that DOC from different origins has different stable isotopic compositions. The riverine DOC has a δ13C value of -27‰, which is different from freshwater phytoplankton, with a range from -35‰ to -25‰. This paper reviewed the researches on the stable carbon isotope ratio of the autochthonous and allochthonous DOC, suggesting that the main sources of DOC in eutrophic lakes can be identified by using natural stable carbon isotope ratio of DOC; the difference on the total dissolved carbohydrates (TCHO) and dissolved combined neutral sugar (DCNS) concentrations, as well as the humic substances (HS) was compared between the autochthonous and allochthonous DOC. Net increases in TCHO and DCNS were observed in the autochthonous DOC during phytoplankton blooms, whereas the HS fraction was quantitatively important in the allochthonous DOC. Many studies have reported the bacterial availability of TCHO and DCNS, and the ratio of TCHO/DOC is used to characterize the bioavailability of DOC, whereas HS can also increase bacterial secondary production and support bacterial growth if labile substrates are abundant.

Furthermore, to elucidate the bioavailability of the two sources of DOC, the bacterial secondary production, bacterial respiration and bacteria growth efficiency (BGE) was analyzed together. The DOC can be either transformed to bacterial secondary production or respired to inorganic carbon. BGE is the fraction of assimilated organic carbon that supports growth. The source of DOC and its chemical composition could be a key regulator of BGE. Traditionally, the autochthonous DOC has been considered to be the main source for bacterial as well as other secondary production, the allochthonous DOC was long considered relatively recalcitrant to bacterial degradation. However, in lakes which are both humic-rich and oligotrophic, the ecosystem respiration exceeds gross primary production, suggesting that the allochthonous DOC can be incorporated into the bacteria biomass and makes a significant carbon and energy subsidy for lakes food web, but little of the allochthonous carbon assimilated by bacteria is likely to reach higher consumers. Recent studies suggest that bacterial BGE increases with the concentration of the low molecular weight DOC in allochthonous DOC.

Discussing the bioavailability and efficiency of carbon transfer in the food web from the sources of DOC, will be helpful to investigate the characterization of carbon cycling in the eutrophic lakes, enhance our understanding of the lake ecology and to provide scientific references for the lake management and protection.

eutrophic lake; dissolved organic carbon; source; bioavailability; review

國(guó)家自然科學(xué)基金資助項(xiàng)目(41201076, 31270507, 31070420);湖泊與環(huán)境國(guó)家重點(diǎn)實(shí)驗(yàn)室開(kāi)放基金資助項(xiàng)目(2012SKL006)

2012- 09- 24;

2013- 03- 21

10.5846/stxb201209241349

*通訊作者Corresponding author.E-mail: fxkong@niglas.ac.cn

葉琳琳，孔繁翔,史小麗，陽(yáng)振，閆德智，張民.富營(yíng)養(yǎng)化湖泊溶解性有機(jī)碳生物可利用性研究進(jìn)展.生態(tài)學(xué)報(bào),2014,34(4):779- 788.

Ye L L, Kong F X, Shi X L, Yang Z, Yan D Z, Zhang M.The bioavailability of dissolved organic carbon in the eutrophic lakes.Acta Ecologica Sinica,2014,34(4):779- 788.