AM真菌物种多样性：生态功能、影响因素及维持机制

杨海水, 熊艳琴, 王　琪, 郭　伊, 戴亚军, 许明敏

南京农业大学农学院, 南京　210095



AM真菌物种多样性：生态功能、影响因素及维持机制

杨海水*, 熊艳琴, 王琪, 郭伊, 戴亚军, 许明敏

南京农业大学农学院, 南京210095

摘要:AM真菌物种多样性是土壤生态系统生物多样性的重要组分之一。尽管对AM真菌多样性已有多年研究，但是，已有研究绝大多数仅停留在对AM真菌群落种属解析层面上，对AM真菌物种多样性生态功能及维持机制方面的认识较浅。从生态功能、影响因素及维持机制3个方面系统地综述了近年来AM真菌多样性领域的研究进展。认为AM真菌多样性对植物群落生产力的调控机制及结合理论与实践解析AM真菌多样性维持机制是该领域未来的重点研究方向。

关键词：丛枝菌根真菌；多样性；生态功能；生态位；中性过程

丛枝菌根 (arbuscular mycorrhiza, AM) 真菌是一类分布广泛、异常丰富的土壤微生物[1]。AM真菌隶属于球囊菌门 (Glomeromycota)，能与80%以上的陆生植物根系形成共生关系[2]。在这一共生关系中，寄主植物为AM真菌提供碳源，而AM真菌为其寄主提供矿质养分。与此同时，还能促进寄主抵御环境胁迫。几乎所有陆地生境均有AM真菌分布，除了森林、农田及草地等常见生境之外，甚至一些极端生境中依然有AM真菌存在，包括沙漠、湿地、极地、高寒草甸及红树林生态系统等[3]。这表明，AM真菌具有丰富的物种多样性。刘润进 等[4]已对2010年之前不同生态系统中AM真菌多样性的研究状况进行了详细的综述分析。近年来，AM真菌物种多样性研究领域取得了诸多开创性成果，尤其在AM真菌物种多样性的生态功能和维持机制方面。针对AM真菌的物种多样性，本文分别从生态功能、影响因素及形成机制三个方面进行分析，旨在为AM真菌多样性的未来研究方向提供参考依据。

1 AM真菌物种多样性的生态功能

1.1促进植物群落多样性

研究发现，AM真菌物种多样性能够促进植物群落的物种多样性。van der Heijden 等[5]发现，AM真菌多样性是维持植物群落多样性的重要决定因子之一。在北美弃荒地草地生态系统，植物群落多样性与AM真菌物种丰度显著正相关。然而，这一现象背后的潜在机制并清楚。Urcelay和Diaz[6]对此提出了理论假设，认为这一现象是由植物的菌根依赖性决定。如果优势种的菌根依赖性较高，AM真菌促进优势种群进一步增加而降低植物群落多样性；如果从属种的菌根依赖性较高，AM真菌则增加植物群落多样性。而在此之前，O′Connor等[7]已经通过实验证实，在草地群落中，施加苯菌灵抑制菌根活性后，菌根依赖性较高的Medicagominima数量降低，菌根依赖性较低的Salviaverbenaca数量增加，而对非菌根植物Carrichteraannua无影响。基于前人研究，在特定环境中，一种植物对某些AM真菌具有一定的偏好性[8- 9]。可以对Urcelay和Diaz 的理论假设进一步扩展。随着AM真菌物种多样性增加，植物群落的从属种遇到各自偏好的AM真菌的可能性增大，从而扩大各自的种群，进而增加整个植物群落的多样性。Bever[8]将AM真菌的多样性与寄主植物多样性的关系归因于正、负反馈。如果AM真菌与某种植物正反馈互作，则促进该种植物的生长而降低植物群落多样性；反之，如果为负反馈，则促进不同植物的共存而增加植物的多样性。针对Bever的“负反馈促进寄主植物共存”的理论，因此，这可能是由寄主植物选择特异的AM真菌群落引起[10]。Vandenkoornhuyse等[9]发现，共存植物根内AM真菌群落组成是完全不同的。两组不同的AM真菌群落，可能会利用完全不同的土壤空间资源，从而造成两种寄主植物的资源生态位分化。这种菌根介导的生态位分化减少了寄主植物间的资源竞争，从而促进了互惠共存。因此，随着AM真菌物种多样性增加，植物群落从属种构建与之共生的特异性AM真菌群落的可能性增加，从而降低植物间的竞争，促进植物种间共存，增加物种多样性。

1.2增加植物群落稳定性

研究发现，AM真菌多样性对植物群落的稳定性起着重要作用。van der Heijden等[5]研究了AM真菌多样性对欧洲钙质草地群落稳定性的影响，发现，当AM真菌多样性较低时，只要AM真菌菌种发生变化，植物群落的结构和组成就会发生剧烈变动。然而，随着AM真菌物种多样性增加，菌种变化导致的植物群落不稳定性逐渐消失。我们认为，造成植物群落稳定性变异的现象可能是由植物的菌根依赖性和AM真菌的功能冗余决定[6,11]。在AM真菌物种多样性较低时，两种真菌具有相似功能的可能性较低。当AM真菌组成发生变化时，如前所述，对特定AM真菌具有较强依赖性的植物群落从属种种群必然发生变化。然而，在高AM真菌物种多样性条件下，不同种AM真菌出现功能冗余的现象可能发生。当植物群落缺失某种或几种AM真菌时，具有相似功能的其他种AM真菌可以进行功能替代。从整个植物群落来看，其物种组成并不受到影响。Wagg等[12]发现，AM真菌多样性可以减轻豆科植物和草本植物之间的竞争，从而促进群落的稳定。这一现象可以从菌根介导的资源生态位分化进行解释。豆科与草本植物的根际环境差异很大，在AM真菌多样性较高的接种条件下，这可能导致二者选择不同的AM真菌群落与之共生。不同AM真菌群落将会利用不同的土壤资源，从而减少两者之间的竞争而稳定群落。此外，叶少萍等[13]发现，接种AM真菌的狗牙根在刈割之后，具有较快的生长速率。这表明，即使受到干扰，在AM真菌物种多样性较高时，植物群落也能够很快恢复稳定。

1.3提高植物群落生产力

AM真菌多样性最重要的生态功能之一就是其能够提高植物系统的生产力。van der Heijden等[5]和Vogelsang等[14]分别发现，植物群落的生产力随着AM真菌物种多样性增加而升高。对这一现象的潜在机制，目前，学术界存在较大争议，互补效应 (complementary effect) 和选择效应 (select effect) 均可对此现象作出解释。“互补效应”学派以Koide为代表，认为，不同的AM真菌具有不同功能，随着AM真菌物种多样性增加，与之相应的功能多样性也增加，通过“功能互补”，使植物群落的生产力增加。van der Heijden等[5]认为，AM真菌多样性越高，其根外菌丝网络越广阔，能更充分地利用土壤中的养分。Jansa等[15]通过定量PCR技术，发现，双接种AM真菌 (Glomusintraradices和G.etunicatum)，韭菜的P含量显著高于任何一种单接种AM真菌处理，从而精确证实了“功能互补”假说。然而，“选择效应”学派，以Wardle 为代表，认为，随着AM真菌物种多样性增加，植物群落遇到高效AM真菌(super fungus)的可能性增加，从而总的系统生产力也随之增加[16]。Vogelsang等[14]发现，相对于单种AM真菌效应，互补效应要小得多，因此认为，AM真菌多样新促进植物生产力增加的现象可能是由某一“超级”AM真菌引起。为了整合两大学派的争议，Wagg等[17]通过详尽的实验证实，“互补效应”在较为贫瘠的土壤中占主导地位，而“选择效应”在肥沃土壤中占主导地位。

2AM真菌物种多样性的影响因素

2.1寄主植物对AM真菌多样性的影响

由于AM真菌为植物根系共生微生物，近年来，寄主植物对AM真菌多样性的影响越来越受关注。在一定程度上，寄主植物多样性决定着AM真菌多样性[4]。研究发现，寄主对AM真菌多样性的影响可以发生在不同分类水平上。在基因型或生态型水平上，郭绍霞和刘润进[18]研究了不同品种牡丹根际AM真菌孢子群落，发现，AM真菌种属组成随牡丹品种不同而不同。Schechter和Bruns[19]研究了蛇纹岩和非蛇纹岩生态型Collinsiasparsiflora根内AM真菌群落，发现，不同生态型寄主根内AM真菌群落完全不同。在物种水平上，不同种寄主植物生理代谢、根系内环境及分泌物不同，必然会影响AM真菌的侵染策略，从而改变其群落组成[20- 21]。大量研究表明，同一生境共存的植物，其根内具有明显不同的AM真菌群落，包括热带森林[22]、温带草地[9]、温带橡树林[23]、半干旱海岸沙丘[24]、高山草甸[25]、干热河谷[26]和农田[27]。在属水平上，Lemanceau等[28]研究了4种Medicago属植物，发现，其根内AM真菌群落组成也是完全不同。目前，在植物群落水平上，AM真菌多样性也受到了广泛关注。Johnson等[29]发现，植物群落组成会显著影响AM真菌的多样性。Börstler等[30]研究了高山草甸AM真菌群落，发现，其多样性变化与地上植物多样性显著相关。Hausmann和Hawkes[31- 32]发现，邻体植物及建植次序均会影响AM真菌群落组成及多样性。Alguacil等[33]研究发现，灌丛群落复杂性调控着AM真菌的多样性。van de Voorde等[34]报道，植物群落构建历史也会影响AM真菌的群落组成和多样性。

2.2环境条件对AM真菌多样性的影响

土壤及气候显著影响AM真菌群落组成和多样性[4]。在稀树草原，Landis等[35]发现，AM真菌多样性与土壤类型和养分含量显著相关，N含量高的土壤，AM真菌物种丰富度较高；这一结果与Santos等[36]的研究结果相反。Landis认为，此现象是由较低P/N比导致。Hazard等[37]发现，在景观尺度上，AM真菌的群落组成由局部非生物环境决定，如土壤pH、降雨和土壤类型。Wirsel[38]发现，土壤条件是湿地芦苇根内AM真菌群落多样性变异的决定因子。此外，气候因子，如海拔和温度都会显著影响AM真菌的多样性。Gai等[39]研究了青藏高原高寒草甸系统，发现，延海拔梯度升高，AM真菌的物种丰富度依次降低。Lugo等[40]研究了南美普纳草原，发现，AM真菌多样性延海拔升高而降低。Wu等[41]报道了富士山AM真菌多样性海拔梯度性分布格局。Koske[42]发现，当寄主植物和土壤条件相似，AM真菌物种多样性随温度增加而增加。Pringle和Bever[43]发现，不同种AM真菌具有不同的物候特性，Acaulosporacolossica主要在暖季产孢，而Gigasporagigantea的产孢季节主要在冷季。

2.3人为干扰对AM真菌多样性的影响

基于AM真菌多样性的重要生态功能，人为干扰是否会导致AM真菌多样性丧失，已经引起了广泛关注。Helgason等[44]报道，与森林系统相比，农业措施，如耕作、施肥和农药等降低了AM真菌物种多样性。Oehl等[45]发现，土地使用强度与AM真菌物种多样性呈负相关。Alguacil等[46]发现，不同耕作措施会直接或间接影响亚热带农作物根内AM真菌的多样性。然而，Hijri等[47]对此却提出了质疑。他们通过详实的大田取样与分子实验技术验证，发现，农田土壤AM真菌多样性未必低，低投入轮作体系可能会更好的保护AM真菌多样性。Alguacil等[48]发现，在热带稀树草原，施磷显著降低AM真菌多样性。Santos等[36]发现，在瑞士半干旱草地，施用无机氮肥降低了AM真菌多样性。Su和Guo[49]发现，过度放牧显著降低了内蒙古草原AM真菌多样性。然而，采取适当的人为措施也可以增加土壤AM真菌的多样性。例如，Alguacil等[50]发现，通过长期城市垃圾填埋可以增加土壤AM真菌的多样性。Verbruggen等[51]发现，有机农业显著增强了AM真菌的物种丰富度。

3AM真菌物种多样性维持机制

物种多样性维持机制是生态学研究的核心之一[52]。基于生态位分化维持群落物种多样性的理论已经发展了近1个世纪。但是，自然群落物种多样性的维持机制至今仍有诸多方面难以解释。Hubbell[53]提出了“中性理论”，假定“不同物种的生态功能等价”，对传统的生态位理论提出了挑战。从而引起了理论生态学和群落生态学的强烈争议。近年来，生态学家趋于将这两种理论进行整合[54]。在不同环境条件下，生态位过程和中性过程可能会相互转化。然而，目前关于物种多样性维持机制的探讨主要集中在植物群落，而对微生物群落的关注较少。牛克昌等[54]认为，未来研究应该更多关注生态位理论和中性理论在土壤微生物群落构建上的应用，以检验其普适性。

尽管AM真菌物种多样性具有非常重要的生态功能，然而，迄今为止，其多样性维持机制的理论和实验研究极度缺乏。如前所述，AM真菌几乎在所有陆地生境均有分布，因此，我们有理由认为，AM真菌的群落构建过程由中性随机过程决定。Lekberg等[55]分析了不同干扰程度下大叶车前根内AM真菌群落，发现，有一种AM真菌序列类群出现于所有干扰条件，并占有优势地位，因此，认为，局部AM真菌群落构建由中性过程决定。然而，大量研究表明，环境条件和寄主植物会显著影响AM真菌群落，暗示生态位过程对AM真菌多样性维持起着主要作用。例如，Fitzsimons等[56]发现，土壤pH和NO3+能够很好的预测AM真菌群落的变化。寄主植物的邻体及建植次序、多样性及群落构建历史等显著影响AM真菌群落构建过程[29,31- 32,34]。Davison等[57]发现，AM真群群落构建并非随机，具有一定的寄主选择性。Pringle和Bever[43]发现，北卡草地AM真菌多样性是由物候和空间生态位共同维持。Dumbrell等[58]研究表明，生态位过程和随机过程同时对AM真菌多样性的维持起着作用。Caruso等[59]通过文献整合分析，发现，多重群落构建规则维持AM真菌群落多样性。以上分析表明，中性过程和生态位过程可能同时参与维持AM真菌群落的多样性，孰主孰次，可能由环境条件决定。例如，毒性植物Ligulariavirgaurea驱动邻体植物根内AM真菌群落构建由中性过程向生态位过程转变[59]。

目前，关于生态位过程和中性过程对AM真菌群落多样性维持的贡献可以从以下两条途径进行判定：第一，基于AM真菌系统发育关系的最近关联指数 (Nearest Related Index, NRI)[60]。如果NRI显著大于0，则AM真菌群落成聚集格局，由生态位过程驱动；如果NRI等于0，则AM真菌群落由随机中性过程驱动。这一分析可以用R软件“picante”程辑包进行。第二，基于AIC值的模型筛选[61]。目前，用于检验生态位过程的模型有Broken stick、Pre-emption、Log-normal、Zipf 和Zipf-Mandelbrot，用于检验中性过程的模型有 ZSM。通过比较各个模型的AIC值，AIC值最小的模型即为解释AM真菌多样性维持过程的最佳模型。AIC=-2×log-likehood+2×npar，log-likehood为基于AM真菌群落数据计算的模型对数似然值，npar为模型所用的参数个数。

4研究展望

从20世纪80年代基于孢子形态分类的AM真菌物种多样性研究开始，到90年代分子生物学技术引入，导致AM真菌分子多样性研究的大力推进，至今已有30余年。目前，关于AM真菌多样性的影响因素研究地较为清楚。未来的菌根生态研究应主要从以下几个方面进行开展：

(1)AM真菌多样性的生态功能：需要集中精力挖掘AM真菌多样性增加植物群落生产力的潜在机制。目前，国际上仅有的几项研究，仅仅阐述了AM真菌多样性与植物生产力正相关的现象。但是，其内在机制还需进一步深究确认。

(2)AM真菌多样性维持机制：需要在不同生态系统中开展中性理论与生态位理论的验证，以及随环境胁迫变化，二者之间是否会相互转化。

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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

基金项目:国家自然科学基金资助项目(31400373); 江苏省自然科学基金资助项目(SBK20140689); 中国博士后科学基金资助项目(2014M561659)

收稿日期:2014- 10- 11; 网络出版日期:2015- 10- 10

*通讯作者

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

DOI:10.5846/stxb201410112001

杨海水, 熊艳琴, 王琪, 郭伊, 戴亚军, 许明敏.AM真菌物种多样性：生态功能、影响因素及维持机制.生态学报,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.