生态学报  2016, Vol. 36 Issue (14): 4233-4243


韦莉莉, 卢昌熠, 丁晶, 俞慎
WEI Lili, LU Changyi, DING Jing, YU Shen.
Functional relationships between arbuscular mycorrhizal symbionts and nutrient dynamics in plant-soil-microbe system
生态学报[J]. 2016, 36(14): 4233-4243
Acta Ecologica Sinica[J]. 2016, 36(14): 4233-4243


收稿日期: 2014-12-04
网络出版日期: 2015-11-02
韦莉莉1, 卢昌熠1,2, 丁晶1,2, 俞慎1     
1. 中国科学院城市环境研究所, 厦门 361021;
2. 中国科学院大学, 北京 100049
摘要: 近几年随着有机农业的发展,丛枝菌根的作用受到特别关注。丛枝菌根是由植物根系与丛枝菌根真菌(AMF)形成的一种共生体。在植物-AMF-土壤系统中,AMF为植物提供N、P等营养的同时从根系得到所需的C。概述了植物-AMF-土壤系统中C、N、P等营养物质的交流以及AMF与土壤微生物的互作关系。丛枝菌根的形成可显著提高植物对P的吸收,且在高P条件下多余的P可储存于AMF中。AMF对土壤N循环的影响相当复杂,可能参与调控N循环的多个过程,如硝化作用、反硝化作用和氨氧化作用等。在有机质丰富的土壤中AMF菌丝可快速扩增并吸收其中的N,主要供菌丝自身所需,只有一小部分传递给植物。AMF对土壤C库的影响尚存争议,可能存在时间尺度的差异。短期内可活化土壤C,而在长期尺度上可能有利于土壤C的储存。AMF能够通过改变土壤微生物群落结构而影响植物-土壤体系的物质交流。AMF与解磷菌、根瘤菌和放线菌的协同增效作用可促进土壤有机质的降解或增强其固氮能力;AMF对氨氧化菌的抑制作用可降低氨的氧化减少N2O的释放。AMF与外生共生真菌EMF共存时,表现出协同增效作用,但EMF的优先定殖会限制AMF的侵染。AMF不同类群之间则主要表现为竞争和拮抗关系。AMF与土壤微生物之间的互作关系受土壤无机环境的影响,在养分亏缺条件下微生物之间往往表现为竞争关系。因植物、AMF与土壤微生物之间存在复杂的互作关系,为此AMF并不总是表现出其对植物营养的促进作用。目前关于AMF的作用机理仍以假说为主,需要进一步的实验验证。在植物-AMF-土壤系统中N与C的交流和P与C的交流并未表现出一致性,对N、P循环相互关系的进一步探讨有助于深入理解植物-土壤体系中的养分循环。植物、AMF和土壤微生物的养分来源及其对养分的相对需求强度和吸收效率尚未可知,因此无法深入理解AMF在植物-土壤体系中养分交流和转化的作用。在方法上,传统的土壤学方法在养分动态研究中存在局限性,现代分子生物学手段和化学计量学的结合值得尝试。
关键词: 丛枝菌根     根际     土壤微生物     养分循环     植物-AMF-土壤系统    
Functional relationships between arbuscular mycorrhizal symbionts and nutrient dynamics in plant-soil-microbe system
WEI Lili1, LU Changyi1,2, DING Jing1,2, YU Shen1     
1. Institute of Urban Environment, Chinese Academy of Science, Xiamen 361021, China;
2. University of Chinese Academy of Sciences, Beijing 100049, China
Abstract: Arbuscular mycorrhizal symbioses (AM symbioses), formed between Arbuscular mycorrhizal fungi (AMFs) and the majority (ca. 80%) of terrestrial plants, play an important part in the regulation of nutrient cycling in plant-soil systems. Owing to their potentially promising role in sustainable agriculture, AM symbioses have attracted increasing interest in the last decade. This review emphasized the functional interrelations among AM symbioses, soil free-living microbes, and the dynamics of carbon (C), nitrogen (N), and phosphorus (P) in plant-soil systems. The contribution of AM symbioses to plant P has become central to our understanding of AM symbiotic function over the past few decades. There is accumulating evidence that plant P uptake is bidirectionally regulated by AM symbioses. More specifically, plant P uptake is enhanced by AMF infection when the soil is P deficient, but when there is excessive soil P, its transfer to the plant is restricted and excessive P accumulates in hyphae, spores, or vessels. The ability of plants to take in P has been correlated with the volume of soil that their roots can explore. However, in the presence of AMF, mycorrhizal P uptake becomes the dominant pathway, even though plant growth or total P uptake may not be enhanced by the interaction. A benefit of AMF infection to plant P uptake is associated with carboxylate exudation produced by hyphae, which promote the mineralization and disaggregation of organic matter through enhancing the activities of phosphate-solubilizing bacteria. Comparatively, the effects of AMFs on N cycling are particularly complex since fungi are likely involved in all N processes. Arbuscular mycorrhizal fungi can take up both inorganic N and low-molecular-weight organic N from soil organic matter, which is primarily used by the fungus, with only a small amount being transferred to the roots. Arbuscular mycorrhizal fungi can also reduce N loss by regulating the trade-off between nitrification and denitrification, through reducing the concentrations of soil mineral N due to AMF uptake, improving rhizosphere aggregate stability, and decreasing the pH of soil subjected to AMF inoculation. Nitrogen loss as N2O is reduced as well from the soil inoculation with exogenous AMF. The reduction of N2O emissions is related to the shift of microbial community composition with the decrease of the microbial community responsible for N2O production and the increase of those microbial groups responsible for N2O consumption. Other soil microorganisms, including ammonia-oxidizing bacteria, can be suppressed by AMF infection, which also contributes to reduced N2O production. Arbuscular mycorrhizal fungi can also be associated with other root symbionts such as root nodules. While the exact mechanisms remain unclear, it is generally believed that AMFs deliver nutrients (such as P) for N fixation in nodules or by enhancing the activity of rhizobia. Because of increasing concerns regarding global climate change, AMF contribution to soil C storage has attracted considerable attention in recent years. Whether AMFs facilitate soil C sequestration or induce soil C loss remains under debate. One proposed explanation is that if AMFs promote soil C storage, then this becomes a short-term liability through the stimulation of organic matter decomposition and acceleration of litter degradation, while the long-term benefits include the incorporation of organic matter into soil aggregates and increased litter production due to enhanced plant growth. The flux of nutrient elements in plant-AMF-soil systems are associated with the interactions between AMF and pertinent soil microbes. Arbuscular mycorrhizal fungi generally facilitate the growth of phosphate-solubilizing bacteria, rhizobia, actinomycetes, and ectomycorrhizal fungi (EMF), and the inoculation of actinomycetes also promotes the growth of AMF. However, rhizobia and EMF appear to suppress the colonization and growth of AMF when they arrive before AMF. The interactions between AMF and soil microbes can also be regulated by soil nutrient level, such as the case of low soil nutrient conditions, in which AMFs compete for soil nutrients with free-living soil microbes. Competition can also occur among different AMF taxa. Indeed, the biogeochemical cycles of C, N, and P are interlinked in plant-soil systems, where there is an interaction between free-living soil microorganisms and AMFs, but it is unknown to date how the interactions among soil organisms regulate biogeochemical cycles of soil macro elements. A combined technique that uses both microbiological and stoichiometry methods may be needed to explore this "mystical territory".
Key words: arbuscular mycorrhiza symbosis     rhizosphere     soil microorganism     nutrient dynamic     plant-soil system    

菌根是植物根系与菌根真菌形成的共生体,广泛存在于自然界中,约80%的陆地植物能够形成菌根[1]。其中,丛枝菌根(Arbuscular mycorrhiza)是最古老且分布最为广泛的一类菌根[2],是由丛枝菌根真菌(Arbuscular mycorrhizal fungi,AMFs)在植物根细胞内形成的一种分枝共生结构。丛枝菌根真菌不仅存在于自然生态系统中,还可与大部分农作物的根系形成菌根[1]。AMF为宿主植物提供N、P等无机养分,同时从宿主植物获得C源。植物固定的含碳化合物近20%为AMF所利用[3-4]。AMF作为养分交换的通道,能够促进生态系统地上和地下部分进行养分交流,因而在生态系统养分循环中起重要的调节作用[5-7]。但过去关注的焦点在于AMF对植物营养方面的贡献,很少从植物-AMF-土壤系统,整体考察物质循环及其之间的平衡关系。本文重点阐述植物-AMF-土壤体系的碳氮磷物质流及AMF与土壤微生物的互作关系,旨在为今后开展植物养分利用率的协同调控研究和生产实践提供参考。

1 丛枝菌根促进植物-土壤系统的物质交流 1.1 对植物-土壤系统磷的调控




在高P条件下,AMF的生物量显著减少[17]。Balzergue等观察到在P含量高达750 mM条件下,豌豆(Pisum sativum)根系与AMF的物质交流几乎完全停止[17]。最新的研究表明,在高P条件下AMF限制P向地上部传递。随P施入量的增加,未接种的豆科植物地上部的P含量增加了143%,而接种植物地上部分的P含量仅增加了53%,地下部分P的增加幅度没有显著差异[18]。可见,在高P条件下多余的P可能储存在菌丝里。AMF在植物P吸收方面的研究相对较多,但仍然未能解答土壤高P对AMF抑制作用的机理。虽然有学者认为独脚金内酯可能参与了调节过程,但在高P条件下植物产生的独脚金内酯也随之减少,因而很可能存在其他信号物质参与调节AMF的定殖[18]

1.2 对植物-土壤系统氮循环的调节

过去普遍认为丛枝菌根主要的贡献在于促进植物对P的吸收。但近年来的研究表明,丛枝菌根在N素的生物地球化学循环中也发挥着重要的作用[19]。一方面,AMF能够直接吸收土壤中的NH4+[20]和NO3-[21]以及小分子有机氮,如甘氨酸及难降解的有机质壳聚糖等[22],并迅速传递给植物。其中,NH4+是AMF的主要N源[23-24]。另一方面,丛枝菌根的形成显著影响N素的生物吸收与同化、有机N矿化、生物固N、硝化和反硝化,以及淋溶等诸多土壤N循环过程(图 1)。丛枝菌根对N循环的影响非常复杂。AMF对NH4+的吸收利用限制了硝化作用[25],同时AMF对土壤NO3-的吸收限制了反硝化作用并降低了淋溶的损失[24]。另外,丛枝菌根还能够通过调节土壤团聚体,促进土壤聚合[26],调节土壤的通气状况,进而影响硝化和反硝化作用之间的平衡。丛枝菌根对硝化作用的影响还可能与AMF的分泌物有关。AMF的分泌物可降低土壤pH,使硝化作用减弱,导致土壤中NO3-含量减少[25]

图 1 丛枝菌根参与调控的土壤氮循环过程示意图 Fig. 1 Nitrogen processes regulated by AMF



1.3 影响土壤碳库

虽然已有研究观察到丛枝菌根的形成能够加速有机质的降解,但其生态意义并未得到关注。2012年Cheng等在Science上发文指出,由于菌根促进表层土新鲜凋落物和土壤有机质的降解,可能影响到土壤碳库的储量[11]。该文引发了激烈的讨论。Kowalchuk[31]在同期Science上以“Bad news for carbon sequestration?”为题,强调了这一研究结果的生态意义,即丛枝菌根通过促进有机质的降解可能使土壤CO2排放量增加,同时减少土壤C库的存量。2013年,德国和澳大利亚学者联合发表了一篇论述,分析了由丛枝菌根引起的表层有机质降解对生态系统土壤C库的短期和长期效应,指出短期内丛枝菌根的存在会引起土壤C库的暂时性减少,但从长期来看,多种因素的综合作用反而可能增加土壤C的储存[32]。比如,有机质降解后产生的难降解物质的输入、菌丝的输入、菌丝对土壤团聚体的稳定作用(保护有机质不被降解)、以及植物凋落物输入的增加等,都可能引起土壤有机碳的增加(图 2)[33-36]

图 2 土壤有机质的长期和短期动态概念图 Fig. 2 Conceptual short-term vs long-term dynamics of organic matter
1.4 丛枝菌根调节下植物-土壤系统中C、N、P的交互作用

AMF与宿主植物之间的物质交流处于动态平衡中,随植物-AMF-土壤系统中能量和养分状态而进行调整。AMF与根系的相互识别和物质交流依赖于信号物质的调控。根系分泌的独脚金内酯能够促进AMF的代谢和分枝,AMF则分泌信号物质刺激根系做出响应[3]。在缺P条件下,根系选择性地为传递较多养分的菌丝提供较多的C。比如,向贫瘠土壤中添加少量或适量的P,菌根根际的水溶性C含量增加[16];但当植物体内P含量较高时,根向AMF提供的C则减少[18]。根系提供的C是AMF的唯一碳源,因此植物的生长状况直接影响AMF可获得的碳量。遮阴处理后植物供给AMF的C减少,但在根际添加蔗糖后,根系和AMF吸收利用的C量均随之增加[19]。Konvalinková等[37]观察到,即使是短期的遮荫处理对AMF的功能也会产生较大的影响,AMF传递给植物的P显著减少,虽然定殖率和菌丝的生长未出现显著变化。离体实验的结果显示,当外源C的供给减半,AMF(Glomus intraradices)的孢子和菌丝里能累积高达7倍的P,占真菌干重的4%[38]。在低C条件下,菌丝未减弱自身的生长但限制了养分向植物的传递。储存在AMF里的P主要以复合磷酸盐的形式存在,植物在缺P条件下,复合磷酸盐能够被碱性磷酸酶解聚成为植物可利用的形式。因而,植物中的C、P含量跟AMF中的C、P含量处于动态平衡中(图 3)。

图 3 植物-AMF-土壤系统中C-N-P的动态平衡示意图 Fig. 3 Trade-offs between C-N-P in the Plant-AMF-soil system

过去曾推测AMF与植物进行着类似的C-N交换,即AMF为能够供给较多C的根系传递较多的N。但最近的研究表明,AMF菌丝对N的吸收和向植物的传递不受植物供给C量的影响[19]。菌丝的定殖和扩增受土壤有机质C:N比的调控。AMF菌丝往往定殖于C:N比较低的有机质土壤中,随着C:N比的增加,N矿化速率和N2O通量随之降低(图 3)[39]。AMF的定殖还与土壤中有机氮和无机氮的比例有关。丛枝菌根常形成于有机氮含量较低(有机氮:无机氮比较低)的土壤中(图 3),但AMF菌丝在富含有机氮的土壤中可快速扩增[19, 23]。可见,AMF对土壤N和P的吸收以及向植物的传递及其与植物C源的交流并未表现出一致性。

2 丛枝菌根与土壤微生物的相互作用


Marschner等[46]证明了菌根植物和非菌根植物根际具有不同的细菌群落。Miransari M等证明,AMF的侵染可直接或间接地影响根际微生物群落的数量和结构,使其发生变化并达到新的平衡[45]。在大多数陆生植物中,菌根真菌与土壤微生物存在着互惠互利的关系[46]。AMF接种后,菌丝分泌的磷酸酶能够提高土壤可利用P含量,球囊霉素可改变土壤结构、抑制病原菌、促进有益微生物的生长等。土壤微生物可能通过产生植物激素、改善土壤养分状况和土壤结构、控制病原菌和影响植物生长等途径,促进AMF的生长。但土壤微生物也可能因竞争养分资源对AMF产生抑制作用[47]

通常,丛枝菌根的形成可显著增加根表面细菌、放线菌和固氮菌的数量,而对真菌的影响很小。但亦有少数实验并未观察到菌根对根际微生物产生促进作用。不同类群的微生物对AMF的响应不同,比如何氏球囊霉(Glomus hoi)表现为正响应效应,而放线菌和丛毛单胞菌则显示负响应效应。AMF还可能通过影响微生物酶活性而改变微生物群落结构。其他土壤微生物对AMF的影响表现为多元化,既可能促进,也可能不产生任何影响,甚至可能抑制AMF的生长。

2.1 AMF与非共生土壤微生物 2.1.1 AMF与非共生细菌

AMF与土壤细菌可协同促进植物对P的吸收。Zhang等[48]利用尼龙网隔实验证明了AMF (Rhizophagus irregularis)和解磷菌(Pseudomonas alcaligenes)具有协同增效作用。单独接种AMF或解磷菌均能刺激土壤中酸性磷酸酶的活性。相对而言,单独接种AMF的土壤中酸性磷酸酶活性较高,而同时接种AMF和解磷菌土壤中酸性磷酸酶活性更高。但如果土壤P很低,AMF与土壤微生物可能因竞争有限的养分而发生相互抑制作用[13, 39]


2.1.2 AMF与非共生真菌

关于AMF与非共生真菌相互作用的研究相对较少。AMF可能会抑制其他真菌或者与特定真菌表现为协同效应。例如,油松幼苗的丛枝菌根抑制了根际土壤中一部分真菌的生长,使油松幼苗根际土壤中真菌的数量和种类减少[53];AMF(Glomus mosseae)与黄海葵附生真菌(Penicilliunm thomii)能够协同促进英国薄荷(Mentha piperita)的生长,提高植株的营养水平[54]。AMF的侵染可显著改变腐生真菌的群落结构,尤其是降低对葡萄糖敏感的菌群生物量[55]

2.2 AMF与其他共生菌 2.2.1 AMF与根瘤菌

AMF和根瘤菌往往同时存在于豆科植物的根系。AMF定殖于根的皮质,固氮菌则一般定殖于根瘤。但在胞外菌丝上也可能着生固氮菌[56]。最近的实验还观察到AMF直接定殖于根瘤上[16, 57]。丛枝菌根能够促使根瘤菌的形成并增强固氮作用[58],但根瘤菌在根部的侵染抑制了AMF的定殖。丛枝菌根可能为根瘤提供P和其他营养元素如铜和锌,从而增强根瘤的固氮作用[59-60]。而Larimer等和Kaschuk等对大量实验结果的Meta分析表明,虽然单独接种AMF和根瘤菌对植物N营养都有促进作用,但同时接种两种菌类并未起到协同增效作用[61-62]


2.2.2 AMF与放线菌

AMF与放线菌的相互作用能够有效的提高宿主植物的固N能力,改善植物的营养状况从而促进宿主植物的生长发育。弗兰克氏放线菌(Frankia)与非豆科植物共生形成根瘤[66]。放线根瘤与丛枝菌根同时接种于黑桤木(Alnus glutinosa)幼苗6个月后,表现出显著地协同增效作用,接种放线菌还促进了AMF菌丝的伸长生长[67]。AMF对放线菌也有促进作用,如辣椒根系中的放线菌数量因接种AMF而增加。同时接种AMF和放线菌,对植物的生长具有更明显的促进作用,植物吸收更多的养分元素,形成的根瘤数量更多、更大;但相对而言,单独接种AMF对植物生长的促进作用更加显著[66-68]。放线菌的侵染可促进AMF的定殖和植物养分的吸收。混合接种AMF和弗兰克放线菌的西藏沙棘,植株的固N水平和生物量明显高于单独接种AMF或单独接种弗兰克放线菌的植株[69]。但AMF与放线菌并非始终保持协同增效作用。在一定条件下,AMF与根际放线菌之间会产生拮抗作用,并对宿主植物的生长有抑制作用[70]

2.2.3 AMF与EMF


2.3 AMF的种间竞争

长期以来,关于AMF与植物相互关系的研究通常在土壤灭菌条件下进行,忽略了AMF之间相互作用的影响。然而最新的研究表明,AMF存在种间竞争[75-76]。Janoušková等[75]观察到,增加AMF侵染密度并未促进植物的生长,甚至因AMF的种间竞争而抑制植物的生长。相对于根际,AMF之间的竞争在根内表现更加剧烈[76]。AMF之间的竞争强度还与宿主提供的C量有关[77]。荫蔽处理(向AMF传输的C减少)的菌根共生体中,竞争力相对较弱的真菌(如Rhizophagus irregularis)其生长将被完全抑制[78]。Werner和Kiers发现[79],AMF之间的相互作用还与定殖顺序有关。先定殖的AMF对后定殖的AMF产生抑制作用,且随定殖时间间隔的延长,抑制作用加强,但后定殖的AMF并未对先定殖的AMF产生显著影响。土壤养分含量可在一定程度上调控AMF的种间相关性。施肥可改变AMF的群落结构,施入少量的P肥使Glomus spp.类AMF成为优势种,且有新的AMF定殖。当施入大量P肥,只观察到其中的两种AMF存在于土壤中[57]

3 问题与展望


相对P而言,丛枝菌根对植物-土壤系统N循环的研究起步较晚,存在疑问较多。与P不同的是,AMF对N的吸收与植物提供的C似乎无关,而与有机质含量密切相关。AMF可在有机质斑块中快速扩增,使有机质降解加快,吸收其中的N供自身生长所需,并传递其中的一小部分N给植物,同时将来自有机质的C传递给其他土壤微生物[7]。有大量实验结果显示,接种AMF的植物其N含量并没有显著增加[4, 25, 80]。因此,丛枝菌根在N循环和植物N营养方面的生态意义尚存在较大争议。Reynolds等[24]提出,只有在缺N条件下菌根对植物N的吸收才有意义。Hodge和Fitter[19]以及Veresoglou[25]则认为即使在高N水平下,AMF仍然对植物的N营养发挥作用,并认为其意义可能与减少代谢消耗有关。因为相对于根系而言,菌丝的生长需要消耗的能量较少[81]



目前的研究集中于根际范围,而AMF菌丝远远超越了根系分布的范围,菌丝圈(即围绕菌丝的区域)也是土壤微生物活跃的区域[23, 69],需要寻找有效的方法开展菌丝圈的研究。另外,将丛枝菌根真菌与传统的有机肥和化学肥料相结合,大规模的推广运用到现实农业中,对农业生产和生态环境都具有重要意义。如何将丛枝菌根真菌运用到现实农业生产中应成为今后研究的重点。

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