尖峰岭热带山地雨林根部真菌?植物互作网络结构特征
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摘要
不同功能群的根部真菌可能会与植物差异性地互作,并进一步影响地下真菌与植物群落构建。本研究采用Illumina Miseq测序方法检测了海南尖峰岭热带山地雨林中常见植物的根部真菌;采用网络分析法比较了丛枝菌根(AM)真菌、外生菌根(ECM)真菌,以及所有根部真菌与植物互作的二分网络(bipartite networks)结构特性。从槭树科、番荔枝科、夹竹桃科、冬青科、棕榈科、壳斗科、樟科和木犀科等8科植物的根系中,检测到297,831条真菌ITS1序列,这些序列被划为1,279个真菌分类单元(OTUs),其中子囊菌门748个、担子菌门354个、球囊菌亚门80个,以及未知真菌97个。核心根部真菌群落(420个OTUs)中,至少有三类不同生态功能的真菌常见,即丛枝菌根真菌(40个OTUs,占总序列数23.4%)、外生菌根真菌(48个OTUs, 13.9%)和腐生型真菌(83个OTUs, 19.8%)。尖峰岭山地雨林根部真菌–植物互作网络结构特性的指标普遍显著高于/低于假定物种随机互作的零模型期待值。在群落水平,不同功能型的根部真菌–植物互作网络表现出不同或相反的结构特性,如丛枝菌根互作网络表现为比零模型预测值高的嵌套性和连接性,以及比零模型低的专一性,而外生菌根互作网络呈现出比零模型预测值低的嵌套性和连接性,以及比零模型高的专一性。在功能群水平,植物的生态位重叠度在AM互作网络高,而ECM互作网络低;真菌的生态位宽度在ECM互作网络窄,而在AM互作网络较宽。共现(co-occurrence)网络分析进一步揭示,ECM群落的物种对资源的高度种间竞争(植物、真菌高C-score),以及AM群落的物种无明显种间竞争(低C-score),可能分别是形成反嵌套ECM互作网络及高嵌套AM互作网络结构的原因。上述结果说明,尖峰岭山地雨林中至少有两种及以上的种间互作机制调节群落构建:驱动AM互作网络冗余(nestedness)及ECM互作网络的高生态位分化(专一性)。本研究在同一个森林内探讨了不同功能型的真菌-植物互作特性,对深入理解热带森林的物种共存机制和生态恢复具有重要意义。
Functionally diverse root-associated fungi may differentially interact with host plants, potentially affecting the assembly processes of belowground plant and fungi communities. Here, we applied the Illumina Miseq sequencing technique to identify root-associated fungi of plants which were co-dominant in a tropical montane rain forest on Hainan Island, China. Structural features of bipartite networks were compared among the whole root-associated, arbuscular mycorrhizal(AM) and ectomycorrhizal(ECM) fungus–plant interactions. A total of 297,831 fungal ITS1 sequences were obtained from eight families including Aceraceae,Annonaceae, Apocynaceae, Aquifoliaceae, Arecaceae, Fagaceae, Lauraceae, and Oleaceae. Fungal sequences were assigned to 1,279 OTUs comprised of Ascomycota(748 OTUs), Basidiomycota(354), Glomeromycota(80), and unidentified fungi(97). At least three functional groups of fungi i.e. putatively ECM(40 OTUs,represented 23.4% of the total fungal reads), AM(40, 13.9%) and saprophyte(83, 19.8%) were prevalent in the core root-associated fungal community(420 OTUs) of the tropical montane rain forest. Network analysis indicated that AM, ECM and root-associated fungus–plant interaction network showed structural features which cannot be predicate by null models assuming species interact randomly. Community level indices behaved differently among different ecotypes of fungus–plant interactions. Specifically, the degree of nestedness(NODF) and connectance were higher, while specialization was lower in the AM interaction network than the expected values from null models. In contrast, the ECM interaction network had a significantly higher degree of specialization and lower nestedness and connectance than the null models. At guild levels, plant niche overlap of AM and ECM interactions are higher and lower than the null model,respectively. Niche breadth of ECM fungi was narrower than that of AM fungi. Co-occurrence patterns of plant and fungus further confirmed competition for resources was intense in ECM interaction network(high C-score of both plants and fungi) and weak in the AM interaction network(low C-score). These findings suggest that at least two modes of interspecific interactions are critical for the assembly and coexistence of root-associated fungal communities, i.e. redundancy(nestedness) of AM interactions, and niche differentiation(specialization) of ECM interactions. Here we provide a comprehensive exploration of the interactions among functionally diverse root-associated fungal guild within a forest, which is key to understand the mechanisms maintaining species coexistence in tropical forests.
Functionally diverse root-associated fungi may differentially interact with host plants, potentially affecting the assembly processes of belowground plant and fungi communities. Here, we applied the Illumina Miseq sequencing technique to identify root-associated fungi of plants which were co-dominant in a tropical montane rain forest on Hainan Island, China. Structural features of bipartite networks were compared among the whole root-associated, arbuscular mycorrhizal(AM) and ectomycorrhizal(ECM) fungus–plant interactions. A total of 297,831 fungal ITS1 sequences were obtained from eight families including Aceraceae,Annonaceae, Apocynaceae, Aquifoliaceae, Arecaceae, Fagaceae, Lauraceae, and Oleaceae. Fungal sequences were assigned to 1,279 OTUs comprised of Ascomycota(748 OTUs), Basidiomycota(354), Glomeromycota(80), and unidentified fungi(97). At least three functional groups of fungi i.e. putatively ECM(40 OTUs,represented 23.4% of the total fungal reads), AM(40, 13.9%) and saprophyte(83, 19.8%) were prevalent in the core root-associated fungal community(420 OTUs) of the tropical montane rain forest. Network analysis indicated that AM, ECM and root-associated fungus–plant interaction network showed structural features which cannot be predicate by null models assuming species interact randomly. Community level indices behaved differently among different ecotypes of fungus–plant interactions. Specifically, the degree of nestedness(NODF) and connectance were higher, while specialization was lower in the AM interaction network than the expected values from null models. In contrast, the ECM interaction network had a significantly higher degree of specialization and lower nestedness and connectance than the null models. At guild levels, plant niche overlap of AM and ECM interactions are higher and lower than the null model,respectively. Niche breadth of ECM fungi was narrower than that of AM fungi. Co-occurrence patterns of plant and fungus further confirmed competition for resources was intense in ECM interaction network(high C-score of both plants and fungi) and weak in the AM interaction network(low C-score). These findings suggest that at least two modes of interspecific interactions are critical for the assembly and coexistence of root-associated fungal communities, i.e. redundancy(nestedness) of AM interactions, and niche differentiation(specialization) of ECM interactions. Here we provide a comprehensive exploration of the interactions among functionally diverse root-associated fungal guild within a forest, which is key to understand the mechanisms maintaining species coexistence in tropical forests.
引文
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Nguyen NH,Song Z,Bates ST,Branco S,Tedersoo L,Menke J,Schilling JS,Kennedy PG(2016)FUNGuild:An open annotation tool for parsing fungal community datasets by ecological guild.Fungal Ecology,20,241-248.
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Bascompte J(2007)Networks in ecology.Basic and Applied Ecology,8,485-490.
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Blaalid R,Davey ML,Kauserud H,Carlsen T,Halvorsen R,Hoiland K,Eidesen PB(2014)Arctic root-associated fungal community composition reflects environmental filtering.Molecular Ecology,23,649-659.
Blüthgen N,Fründ J,Vázquez DP,Menzel F(2008)What do interaction network metrics tell us about specialization and biological traits.Ecology,89,3387-3399.
Burkle LA,Marlin JC,Knight TM(2013)Plant-pollinator interactions over 120 years:Loss of species,co-occurrence,and function.Science,339,1611-1615.
Cannon PF,Kirk PM(2007)Fungal Families of the World.CABI Bioscience,Wallingford.
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Chagnon PL,Bradley RL,Klironomos JN(2012)Using ecological network theory to evaluate the causes and consequences of arbuscular mycorrhizal community structure.New Phytologist,194,307-312.
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Dickie KH,Cann C,Norman EC,Bamforth CW,Muller RE(2001)Foam-negative materials.Journal of the American Society of Brewing Chemists,59,17-23.
Edgar RC(2010)Search and clustering orders of magnitude faster than BLAST.Bioinformatics,26,2460-2461.
Edgar RC(2013)UPARSE:Highly accurate OTU sequences from microbial amplicon reads.Nature Methods,10,996.
Edgar RC(2018)Accuracy of taxonomy prediction for 16Sr RNA and fungal ITS sequences,PeerJ,6,e4652.
Fang JY,Li YD,Zhu B,Liu GH,Zhou GY(2004)Community structures and species richness in the montane rain forest of Jianfengling,Hainan Island,China.Biodiversity Science,12,29-43.(in Chinese with English abstract)[方精云,李意德,朱彪,刘国华,周光益(2004)海南岛尖峰岭山地雨林的群落结构、物种多样性以及在世界雨林中的地位.生物多样性,12,29-43.]
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Gao C,Montoya L,Xu L,Madera M,Hollingsworth J,Purdom E,Hutmacher RB,Dahlberg JA,Coleman-Derr D,Lemaux PG,Taylor JW(2019)Strong succession in arbuscular mycorrhizal fungal communities.The ISME Journal,13,214-226.
Gotelli NJ,Mc Cabe DJ(2002)Species co-occurrence:Ameta-analysis of J.M.Diamond’s assembly rules model.Ecology,83,2091-2096.
Huang CW,Liao YH,Ding Q(2017)Two sample pooling strategies revealed different root-associated fungal diversity of Rhododendron species.Acta Microbiologica Sinica,57,571-581.(in Chinese with English abstract)[黄彩微,廖映辉,丁琼(2017)两种混合样品策略对揭示杜鹃花根部真菌多样性的影响.微生物学报,57,571-581.]
James A,Pitchford JW,Plank MJ(2012)Disentangling nestedness from models of ecological complexity.Nature,487,227-230.
Jiang YX,Lu JP(1991)Tropical Forest Ecosystem of Jianfengling,Hainan Island,China.Science Press,Beijing.(in Chinese)[蒋有绪,卢俊培(1991)中国海南岛尖峰岭热带林生态系统.科学出版社,北京.]
Kivlin SN,Winston GC,Goulden ML,Treseder KK(2014)Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales.Fungal Ecology,12,14-25.
K?ljalg U,Nilsson RH,Abarenkov K,Tedersoo L,Taylor AFS,Bahram M,Bates ST,Bruns TD,Bengtsson-Palme J,Callaghan TM,Douglas B,Drenkhan T,Eberhardt U,Due?as M,Grebenc T,Griffith GW,Hartmann M,Kirk PM,Kohout P,Larsson E,Lindahl BD,Lücking R,Martín MP,Matheny PB,Nguyen NH,Niskanen T,Oja J,Peay KG,Peintner U,Peterson M,P?ldmaa K,Saag L,Saar I,Schü?ler A,Scott JA,Senés C,Smith ME,Suija A,Taylor DL,Telleria MT,Weiss M,Larsson K-H(2013)Towards a unified paradigm for sequence-based identification of fungi.Molecular Ecology,22,5271-5277.
Kress WJ,Erickson DL,Jones FA,Swenson NG,Perez R,Sanjur O,Bermingham E(2009)Plant DNA barcodes and a community phylogeny of a tropical forest dynamics plot in Panama.Proceedings of the National Academy of Sciences,USA,106,18621-18626.
Merges D,Bálint M,Schmitt I,B?hning-Gaese K,Neuschulz EL(2018)Spatial patterns of pathogenic and mutualistic fungi across the elevational range of a host plant.Journal of Ecology,106,1545-1557.
Newsham KK(2011)A meta-analysis of plant responses to dark septate root endophytes.New Phytologist,190,783-793.
Nguyen NH,Song Z,Bates ST,Branco S,Tedersoo L,Menke J,Schilling JS,Kennedy PG(2016)FUNGuild:An open annotation tool for parsing fungal community datasets by ecological guild.Fungal Ecology,20,241-248.
Patefield WM(1981)Algorithm AS 159:An efficient method of generating random R×C tables with given row and column totals.Journal of the Royal Statistical Society,Series C(Applied Statistics),30,91-97.
Pianka ER(1974)Niche overlap and diffuse competition.Proceedings of the National Academy of Sciences,USA,71,2141-2145.
Smith DP,Peay KG(2014)Sequence depth,not PCR replication,improves ecological inference from next generation DNA sequencing.PLoS ONE,9,e90234.
Smith SE,Read DJ(2008)Mycorrhizal Symbiosis,3rd edn.Academic Press,London.
Taudiere A,Munoz F,Lesne A,Monnet AC,Bellanger JM,Selosse MA,Moreau PA,Richard F(2015)Beyond ectomycorrhizal bipartite networks:Projected networks demonstrate contrasted patterns between early-and late-successional plants in Corsica.Frontiers in Plant Science,6,881.
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