楊海水, 熊艷琴, 王　琪, 郭　伊, 戴亞軍, 許明敏

南京農業(yè)大學農學院, 南京　210095

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AM真菌物種多樣性：生態(tài)功能、影響因素及維持機制

楊海水*, 熊艷琴, 王琪, 郭伊, 戴亞軍, 許明敏

南京農業(yè)大學農學院, 南京210095

摘要:AM真菌物種多樣性是土壤生態(tài)系統(tǒng)生物多樣性的重要組分之一。盡管對AM真菌多樣性已有多年研究，但是，已有研究絕大多數僅停留在對AM真菌群落種屬解析層面上，對AM真菌物種多樣性生態(tài)功能及維持機制方面的認識較淺。從生態(tài)功能、影響因素及維持機制3個方面系統(tǒng)地綜述了近年來AM真菌多樣性領域的研究進展。認為AM真菌多樣性對植物群落生產力的調控機制及結合理論與實踐解析AM真菌多樣性維持機制是該領域未來的重點研究方向。

關鍵詞：叢枝菌根真菌；多樣性；生態(tài)功能；生態(tài)位；中性過程

叢枝菌根 (arbuscular mycorrhiza, AM) 真菌是一類分布廣泛、異常豐富的土壤微生物[1]。AM真菌隸屬于球囊菌門 (Glomeromycota)，能與80%以上的陸生植物根系形成共生關系[2]。在這一共生關系中，寄主植物為AM真菌提供碳源，而AM真菌為其寄主提供礦質養(yǎng)分。與此同時，還能促進寄主抵御環(huán)境脅迫。幾乎所有陸地生境均有AM真菌分布，除了森林、農田及草地等常見生境之外，甚至一些極端生境中依然有AM真菌存在，包括沙漠、濕地、極地、高寒草甸及紅樹林生態(tài)系統(tǒng)等[3]。這表明，AM真菌具有豐富的物種多樣性。劉潤進 等[4]已對2010年之前不同生態(tài)系統(tǒng)中AM真菌多樣性的研究狀況進行了詳細的綜述分析。近年來，AM真菌物種多樣性研究領域取得了諸多開創(chuàng)性成果，尤其在AM真菌物種多樣性的生態(tài)功能和維持機制方面。針對AM真菌的物種多樣性，本文分別從生態(tài)功能、影響因素及形成機制三個方面進行分析，旨在為AM真菌多樣性的未來研究方向提供參考依據。

1 AM真菌物種多樣性的生態(tài)功能

1.1促進植物群落多樣性

研究發(fā)現，AM真菌物種多樣性能夠促進植物群落的物種多樣性。van der Heijden 等[5]發(fā)現，AM真菌多樣性是維持植物群落多樣性的重要決定因子之一。在北美棄荒地草地生態(tài)系統(tǒng)，植物群落多樣性與AM真菌物種豐度顯著正相關。然而，這一現象背后的潛在機制并清楚。Urcelay和Diaz[6]對此提出了理論假設，認為這一現象是由植物的菌根依賴性決定。如果優(yōu)勢種的菌根依賴性較高，AM真菌促進優(yōu)勢種群進一步增加而降低植物群落多樣性；如果從屬種的菌根依賴性較高，AM真菌則增加植物群落多樣性。而在此之前，O′Connor等[7]已經通過實驗證實，在草地群落中，施加苯菌靈抑制菌根活性后，菌根依賴性較高的Medicagominima數量降低，菌根依賴性較低的Salviaverbenaca數量增加，而對非菌根植物Carrichteraannua無影響?；谇叭搜芯浚谔囟ōh(huán)境中，一種植物對某些AM真菌具有一定的偏好性[8- 9]?？梢詫rcelay和Diaz 的理論假設進一步擴展。隨著AM真菌物種多樣性增加，植物群落的從屬種遇到各自偏好的AM真菌的可能性增大，從而擴大各自的種群，進而增加整個植物群落的多樣性。Bever[8]將AM真菌的多樣性與寄主植物多樣性的關系歸因于正、負反饋。如果AM真菌與某種植物正反饋互作，則促進該種植物的生長而降低植物群落多樣性；反之，如果為負反饋，則促進不同植物的共存而增加植物的多樣性。針對Bever的“負反饋促進寄主植物共存”的理論，因此，這可能是由寄主植物選擇特異的AM真菌群落引起[10]。Vandenkoornhuyse等[9]發(fā)現，共存植物根內AM真菌群落組成是完全不同的。兩組不同的AM真菌群落，可能會利用完全不同的土壤空間資源，從而造成兩種寄主植物的資源生態(tài)位分化。這種菌根介導的生態(tài)位分化減少了寄主植物間的資源競爭，從而促進了互惠共存。因此，隨著AM真菌物種多樣性增加，植物群落從屬種構建與之共生的特異性AM真菌群落的可能性增加，從而降低植物間的競爭，促進植物種間共存，增加物種多樣性。

1.2增加植物群落穩(wěn)定性

研究發(fā)現，AM真菌多樣性對植物群落的穩(wěn)定性起著重要作用。van der Heijden等[5]研究了AM真菌多樣性對歐洲鈣質草地群落穩(wěn)定性的影響，發(fā)現，當AM真菌多樣性較低時，只要AM真菌菌種發(fā)生變化，植物群落的結構和組成就會發(fā)生劇烈變動。然而，隨著AM真菌物種多樣性增加，菌種變化導致的植物群落不穩(wěn)定性逐漸消失。我們認為，造成植物群落穩(wěn)定性變異的現象可能是由植物的菌根依賴性和AM真菌的功能冗余決定[6,11]。在AM真菌物種多樣性較低時，兩種真菌具有相似功能的可能性較低。當AM真菌組成發(fā)生變化時，如前所述，對特定AM真菌具有較強依賴性的植物群落從屬種種群必然發(fā)生變化。然而，在高AM真菌物種多樣性條件下，不同種AM真菌出現功能冗余的現象可能發(fā)生。當植物群落缺失某種或幾種AM真菌時，具有相似功能的其他種AM真菌可以進行功能替代。從整個植物群落來看，其物種組成并不受到影響。Wagg等[12]發(fā)現，AM真菌多樣性可以減輕豆科植物和草本植物之間的競爭，從而促進群落的穩(wěn)定。這一現象可以從菌根介導的資源生態(tài)位分化進行解釋。豆科與草本植物的根際環(huán)境差異很大，在AM真菌多樣性較高的接種條件下，這可能導致二者選擇不同的AM真菌群落與之共生。不同AM真菌群落將會利用不同的土壤資源，從而減少兩者之間的競爭而穩(wěn)定群落。此外，葉少萍等[13]發(fā)現，接種AM真菌的狗牙根在刈割之后，具有較快的生長速率。這表明，即使受到干擾，在AM真菌物種多樣性較高時，植物群落也能夠很快恢復穩(wěn)定。

1.3提高植物群落生產力

AM真菌多樣性最重要的生態(tài)功能之一就是其能夠提高植物系統(tǒng)的生產力。van der Heijden等[5]和Vogelsang等[14]分別發(fā)現，植物群落的生產力隨著AM真菌物種多樣性增加而升高。對這一現象的潛在機制，目前，學術界存在較大爭議，互補效應 (complementary effect) 和選擇效應 (select effect) 均可對此現象作出解釋?！盎パa效應”學派以Koide為代表，認為，不同的AM真菌具有不同功能，隨著AM真菌物種多樣性增加，與之相應的功能多樣性也增加，通過“功能互補”，使植物群落的生產力增加。van der Heijden等[5]認為，AM真菌多樣性越高，其根外菌絲網絡越廣闊，能更充分地利用土壤中的養(yǎng)分。Jansa等[15]通過定量PCR技術，發(fā)現，雙接種AM真菌 (Glomusintraradices和G.etunicatum)，韭菜的P含量顯著高于任何一種單接種AM真菌處理，從而精確證實了“功能互補”假說。然而，“選擇效應”學派，以Wardle 為代表，認為，隨著AM真菌物種多樣性增加，植物群落遇到高效AM真菌(super fungus)的可能性增加，從而總的系統(tǒng)生產力也隨之增加[16]。Vogelsang等[14]發(fā)現，相對于單種AM真菌效應，互補效應要小得多，因此認為，AM真菌多樣新促進植物生產力增加的現象可能是由某一“超級”AM真菌引起。為了整合兩大學派的爭議，Wagg等[17]通過詳盡的實驗證實，“互補效應”在較為貧瘠的土壤中占主導地位，而“選擇效應”在肥沃土壤中占主導地位。

2AM真菌物種多樣性的影響因素

2.1寄主植物對AM真菌多樣性的影響

由于AM真菌為植物根系共生微生物，近年來，寄主植物對AM真菌多樣性的影響越來越受關注。在一定程度上，寄主植物多樣性決定著AM真菌多樣性[4]。研究發(fā)現，寄主對AM真菌多樣性的影響可以發(fā)生在不同分類水平上。在基因型或生態(tài)型水平上，郭紹霞和劉潤進[18]研究了不同品種牡丹根際AM真菌孢子群落，發(fā)現，AM真菌種屬組成隨牡丹品種不同而不同。Schechter和Bruns[19]研究了蛇紋巖和非蛇紋巖生態(tài)型Collinsiasparsiflora根內AM真菌群落，發(fā)現，不同生態(tài)型寄主根內AM真菌群落完全不同。在物種水平上，不同種寄主植物生理代謝、根系內環(huán)境及分泌物不同，必然會影響AM真菌的侵染策略，從而改變其群落組成[20- 21]。大量研究表明，同一生境共存的植物，其根內具有明顯不同的AM真菌群落，包括熱帶森林[22]、溫帶草地[9]、溫帶橡樹林[23]、半干旱海岸沙丘[24]、高山草甸[25]、干熱河谷[26]和農田[27]。在屬水平上，Lemanceau等[28]研究了4種Medicago屬植物，發(fā)現，其根內AM真菌群落組成也是完全不同。目前，在植物群落水平上，AM真菌多樣性也受到了廣泛關注。Johnson等[29]發(fā)現，植物群落組成會顯著影響AM真菌的多樣性。B?rstler等[30]研究了高山草甸AM真菌群落，發(fā)現，其多樣性變化與地上植物多樣性顯著相關。Hausmann和Hawkes[31- 32]發(fā)現，鄰體植物及建植次序均會影響AM真菌群落組成及多樣性。Alguacil等[33]研究發(fā)現，灌叢群落復雜性調控著AM真菌的多樣性。van de Voorde等[34]報道，植物群落構建歷史也會影響AM真菌的群落組成和多樣性。

2.2環(huán)境條件對AM真菌多樣性的影響

土壤及氣候顯著影響AM真菌群落組成和多樣性[4]。在稀樹草原，Landis等[35]發(fā)現，AM真菌多樣性與土壤類型和養(yǎng)分含量顯著相關，N含量高的土壤，AM真菌物種豐富度較高；這一結果與Santos等[36]的研究結果相反。Landis認為，此現象是由較低P/N比導致。Hazard等[37]發(fā)現，在景觀尺度上，AM真菌的群落組成由局部非生物環(huán)境決定，如土壤pH、降雨和土壤類型。Wirsel[38]發(fā)現，土壤條件是濕地蘆葦根內AM真菌群落多樣性變異的決定因子。此外，氣候因子，如海拔和溫度都會顯著影響AM真菌的多樣性。Gai等[39]研究了青藏高原高寒草甸系統(tǒng)，發(fā)現，延海拔梯度升高，AM真菌的物種豐富度依次降低。Lugo等[40]研究了南美普納草原，發(fā)現，AM真菌多樣性延海拔升高而降低。Wu等[41]報道了富士山AM真菌多樣性海拔梯度性分布格局。Koske[42]發(fā)現，當寄主植物和土壤條件相似，AM真菌物種多樣性隨溫度增加而增加。Pringle和Bever[43]發(fā)現，不同種AM真菌具有不同的物候特性，Acaulosporacolossica主要在暖季產孢，而Gigasporagigantea的產孢季節(jié)主要在冷季。

2.3人為干擾對AM真菌多樣性的影響

基于AM真菌多樣性的重要生態(tài)功能，人為干擾是否會導致AM真菌多樣性喪失，已經引起了廣泛關注。Helgason等[44]報道，與森林系統(tǒng)相比，農業(yè)措施，如耕作、施肥和農藥等降低了AM真菌物種多樣性。Oehl等[45]發(fā)現，土地使用強度與AM真菌物種多樣性呈負相關。Alguacil等[46]發(fā)現，不同耕作措施會直接或間接影響亞熱帶農作物根內AM真菌的多樣性。然而，Hijri等[47]對此卻提出了質疑。他們通過詳實的大田取樣與分子實驗技術驗證，發(fā)現，農田土壤AM真菌多樣性未必低，低投入輪作體系可能會更好的保護AM真菌多樣性。Alguacil等[48]發(fā)現，在熱帶稀樹草原，施磷顯著降低AM真菌多樣性。Santos等[36]發(fā)現，在瑞士半干旱草地，施用無機氮肥降低了AM真菌多樣性。Su和Guo[49]發(fā)現，過度放牧顯著降低了內蒙古草原AM真菌多樣性。然而，采取適當的人為措施也可以增加土壤AM真菌的多樣性。例如，Alguacil等[50]發(fā)現，通過長期城市垃圾填埋可以增加土壤AM真菌的多樣性。Verbruggen等[51]發(fā)現，有機農業(yè)顯著增強了AM真菌的物種豐富度。

3AM真菌物種多樣性維持機制

物種多樣性維持機制是生態(tài)學研究的核心之一[52]?；谏鷳B(tài)位分化維持群落物種多樣性的理論已經發(fā)展了近1個世紀。但是，自然群落物種多樣性的維持機制至今仍有諸多方面難以解釋。Hubbell[53]提出了“中性理論”，假定“不同物種的生態(tài)功能等價”，對傳統(tǒng)的生態(tài)位理論提出了挑戰(zhàn)。從而引起了理論生態(tài)學和群落生態(tài)學的強烈爭議。近年來，生態(tài)學家趨于將這兩種理論進行整合[54]。在不同環(huán)境條件下，生態(tài)位過程和中性過程可能會相互轉化。然而，目前關于物種多樣性維持機制的探討主要集中在植物群落，而對微生物群落的關注較少。?？瞬萚54]認為，未來研究應該更多關注生態(tài)位理論和中性理論在土壤微生物群落構建上的應用，以檢驗其普適性。

盡管AM真菌物種多樣性具有非常重要的生態(tài)功能，然而，迄今為止，其多樣性維持機制的理論和實驗研究極度缺乏。如前所述，AM真菌幾乎在所有陸地生境均有分布，因此，我們有理由認為，AM真菌的群落構建過程由中性隨機過程決定。Lekberg等[55]分析了不同干擾程度下大葉車前根內AM真菌群落，發(fā)現，有一種AM真菌序列類群出現于所有干擾條件，并占有優(yōu)勢地位，因此，認為，局部AM真菌群落構建由中性過程決定。然而，大量研究表明，環(huán)境條件和寄主植物會顯著影響AM真菌群落，暗示生態(tài)位過程對AM真菌多樣性維持起著主要作用。例如，Fitzsimons等[56]發(fā)現，土壤pH和NO3+能夠很好的預測AM真菌群落的變化。寄主植物的鄰體及建植次序、多樣性及群落構建歷史等顯著影響AM真菌群落構建過程[29,31- 32,34]。Davison等[57]發(fā)現，AM真群群落構建并非隨機，具有一定的寄主選擇性。Pringle和Bever[43]發(fā)現，北卡草地AM真菌多樣性是由物候和空間生態(tài)位共同維持。Dumbrell等[58]研究表明，生態(tài)位過程和隨機過程同時對AM真菌多樣性的維持起著作用。Caruso等[59]通過文獻整合分析，發(fā)現，多重群落構建規(guī)則維持AM真菌群落多樣性。以上分析表明，中性過程和生態(tài)位過程可能同時參與維持AM真菌群落的多樣性，孰主孰次，可能由環(huán)境條件決定。例如，毒性植物Ligulariavirgaurea驅動鄰體植物根內AM真菌群落構建由中性過程向生態(tài)位過程轉變[59]。

目前，關于生態(tài)位過程和中性過程對AM真菌群落多樣性維持的貢獻可以從以下兩條途徑進行判定：第一，基于AM真菌系統(tǒng)發(fā)育關系的最近關聯(lián)指數 (Nearest Related Index, NRI)[60]。如果NRI顯著大于0，則AM真菌群落成聚集格局，由生態(tài)位過程驅動；如果NRI等于0，則AM真菌群落由隨機中性過程驅動。這一分析可以用R軟件“picante”程輯包進行。第二，基于AIC值的模型篩選[61]。目前，用于檢驗生態(tài)位過程的模型有Broken stick、Pre-emption、Log-normal、Zipf 和Zipf-Mandelbrot，用于檢驗中性過程的模型有 ZSM。通過比較各個模型的AIC值，AIC值最小的模型即為解釋AM真菌多樣性維持過程的最佳模型。AIC=-2×log-likehood+2×npar，log-likehood為基于AM真菌群落數據計算的模型對數似然值，npar為模型所用的參數個數。

4研究展望

從20世紀80年代基于孢子形態(tài)分類的AM真菌物種多樣性研究開始，到90年代分子生物學技術引入，導致AM真菌分子多樣性研究的大力推進，至今已有30余年。目前，關于AM真菌多樣性的影響因素研究地較為清楚。未來的菌根生態(tài)研究應主要從以下幾個方面進行開展：

(1)AM真菌多樣性的生態(tài)功能：需要集中精力挖掘AM真菌多樣性增加植物群落生產力的潛在機制。目前，國際上僅有的幾項研究，僅僅闡述了AM真菌多樣性與植物生產力正相關的現象。但是，其內在機制還需進一步深究確認。

(2)AM真菌多樣性維持機制：需要在不同生態(tài)系統(tǒng)中開展中性理論與生態(tài)位理論的驗證，以及隨環(huán)境脅迫變化，二者之間是否會相互轉化。

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Arbuscular mycorrhizal fungal species diversity: ecological functioning,determinants and assembling mechanisms

YANG Haishui*, XIONG Yanqin, WANG Qi, GUO Yi, DAI Yajun, XU Mingmin

CollegeofAgriculture,NanjingAgriculturalUniversity,Nanjing210095,China

Abstract：Arbuscular mycorrhizal fungi (AMF) are a group of ecologically important soil microbes and show wide geographic distribution across the globe. AMF form obligate symbiosis with roots of -80% land plants. In the symbiosis, host plants provide carbon for AMF in return for several benefits, i.e., promoting nutrient uptake, tolerating drought and salt stress, resisting pathogens and herbivores, etc. AMF also can redistribute resources (i.e., C, N and P) between plants and alter their competitive interactions, and thus drive plant population dynamics and community processes. AMF diversity is one of the most important components in soil diversity. In the past decades, AMF are found in almost all terrestrial habitats, including grassland, forest, desert, wetland, alpine meadow, polar region and mangrove, etc. This suggests that AMF have high species diversity. Although AMF diversity has a relatively long research history, most studies only tried to investigate species composition in AMF communities, little is known about the functioning of AMF diversity. In this mini-review, we summarized the new advances in the AMF diversity field, including ecological functioning, determinants and assembling rules. AMF diversity has important ecological functioning. Here, we discussed three aspects: the effects on plant system diversity, stability and productivity. First, several studies reported that AMF diversity is an important determinant for plant diversity. This might be caused by mycorrhizal dependence of subordinate plants. Some studies found that host plants have some preferentially selection towards AMF. Thus, with increasing AMF diversity, subordinate plants will have a higher probability to meet their best AMF partner. Another possibility is that negative plant-mycorrhiza feedbacks might generate positive AMF diversity-plant diversity patterns. This might be caused by host selection towards specific AMF communities. Distinctive AMF communities will make host plants occupy different niche for soil resources. Secondly, AMF diversity could stabilize plant community. Two possibilities can be used to explain this pattern. One is functioning redundancy for several AMF species. In AMF communities with high diversity, loss of certain fungal species will not affect plant community because of similar functioning shared by other AMF. The other possibility is that high AMF diversity will relax competition between different plants for soil nutrients. Third, AMF diversity promotes plant productivity. It seems a general pattern but the mechanisms underling it are still in debate. Complementary effect states that different AMF have different functioning. Higher AMF diversity will have greater functional diversity, which will generate higher plant productivity. Sampling effect states that higher AMF diversity increases the probability of plants encountering the super fungus. Many factors can affect AMF diversity, but here, we are only concentrated in host plants, environmental conditions and anthropogenic disturbance. Host plants affect AMF diversity through different taxonomic levels, including genetype or ecotype, species and community. Environmental conditions include soil nutrient, i.e., N and P, soil type, pH, precipitation and temperature. Anthropogenic disturbance includes agricultural practices, such as tillage, pesticides, fertilization, and land use conversion. Lastly, we discussed the theoretical hypothesis of AMF community assembling process, and provided the analytical methods for dissecting niche and neutral process. At present, it is debating for the assembling process of AMF community in mycorrhizal ecology. In fact, both processes might act simultaneously for AMF community. We deem that future studies should pay attention to the mechanisms underling the positive AMF species diversity-plant productivity relationships, as well as the AMF diversity maintaining mechanisms.

Key Words:arbuscular mycorrhizal fungi; diversity; ecological roles; niche; neutral theory

基金項目:國家自然科學基金資助項目(31400373); 江蘇省自然科學基金資助項目(SBK20140689); 中國博士后科學基金資助項目(2014M561659)

收稿日期:2014- 10- 11; 網絡出版日期:2015- 10- 10

*通訊作者

Corresponding author.E-mail: yanghaishui@njau.edu.cn

DOI:10.5846/stxb201410112001

楊海水, 熊艷琴, 王琪, 郭伊, 戴亞軍, 許明敏.AM真菌物種多樣性：生態(tài)功能、影響因素及維持機制.生態(tài)學報,2016,36(10):2826- 2832.

Yang H S, Xiong Y Q, Wang Q, Guo Y, Dai Y J, Xu M M.Arbuscular mycorrhizal fungal species diversity: ecological functioning, determinants and assembling mechanisms.Acta Ecologica Sinica,2016,36(10):2826- 2832.