长期不同磷肥施用量对砂姜黑土真菌多样性、群落组成和种间关系的影响
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摘要
以安徽蒙城砂姜黑土氮磷钾肥肥效长期定位试验为平台,选取P0(不施磷肥)、P1(P_2O_5 45 kg/hm~2)和P2(P_2O_5 90 kg/hm~2)3个磷肥施用梯度,采用现代高通量测序技术,探索长期施用磷肥对真菌多样性、群落组成和种间关系的影响。结果发现真菌多样性随磷肥施入量增加而降低,且与全磷和有效磷均成显著负相关。磷肥施用导致真菌群落组成发生明显改变,冗余分析结果表明这与全磷和可溶性有机碳密切相关。P1和P2中子囊菌门和子囊菌纲显著升高,而被孢霉菌门和被孢霉菌纲则显著降低。在属水平上,施磷处理中腐生营养型真菌显著升高,而病原型和共生型真菌显著降低:其中P0中Sagenomella、Simplicillium、Magnaporthiopsis、Schizothecium和Nigrospora等5个属相对丰度最高;P1中Plenodomus、Penicillium和Arthrobotrys相对丰度最高;P2中Cyphellophora、Zopfiella、Guehomyces、Mortierella和Mucor等5个属相对丰度最高。网络分析发现施磷后真菌网络复杂度和稳定性升高,物种间正相关关系增加,负相关关系减少。因此在砂姜黑土区长期施用磷肥可降低真菌多样性,增加土壤中腐生营养型真菌、减少共生或病原菌数量,同时提高物种间网络复杂度和稳定性。以上结果表明磷肥施用对促进土壤养分循环,控制植物病害、维持地下生态系统稳定性具有重要作用。
Phosphorus(P) deficiency is a limiting factor for agricultural production in the region covered with lime concretion black soil. Application of chemical P fertilizer is a common strategy to improve P availability. Numerous studies have demonstrated the essential role of P fertilization on soil fertility and crop yield, whereas relatively little is known about the effects of long-term P application on the belowground fungal community. The overall objective of this study was to investigate the effects of long-term P fertilization on fungal community diversity, composition, and intraspecific interactions in a lime concretion black soil, and to assess how the effects varied with application rate. Soils from a 21-year field experiment located in Mengcheng County, Anhui Province, were used, with treatments including three levels of P application rates, i.e.(1) P0: unamended control,(2) P1: chemical P fertilizer was applied at P_2O_5 45 kg/hm~2, and(3) P2: chemical P fertilizer was applied at P_2O_5 90 kg/hm~2. ITS1 gene pyrosequencing was employed to characterize the fungal community diversity and composition. The results showed that long-term P fertilization significantly improved soil fertility. Compared with the P0 treatment, the total P(TP) from the P2 and P1 treatments was 40.00% and 24.00% higher, and the available P(AP) was 384% and 144% higher, respectively. The Shannon index decreased with the P application rates, and was significantly negatively correlated with TP(r=-0.678, P=0.045) and AP(r=-0.677, P=0.045). Ascomycota was the dominant phylum in the studied soil, with its relative abundance being 65.71%—79.86%. Principal coordinate analysis(PCoA) revealed that the fungal community structure differed significantly among the different treatments. Redundancy analysis(RDA) further suggested that the fungal community structure was mainly determined by TP and dissolved organic carbon(DOC). Compared with the P0 treatment, the relative abundance of Ascomycota from P2 and P1 was 9.87% and 11.75% higher, and that of Sordariomycetes was 28.63% and 15.97% higher, respectively. Conversely, the relative abundance of Mortierellomycota from P2 and P1 was 42.63% and 43.81% lower, and that of Mortierellomycetes was 43.82% and 42.63% lower, respectively. Long-term P fertilization resulted in a significant enrichment of saprophytic fungi, namely, the genera of Plenodomus, Penicillium, and Arthrobotrys were enriched in the P1 treatment, and the genera of Cyphellophora, Zopfiella, Guehomyces, Mortierella, and Mucor were enriched in the P2 treatment. However, pathogenic(i.e., Simplicillium and Magnaporthiopsis) and symbiotic(i.e., Sagenomella and Nigrospora) fungi were depleted in the P1 and P2 treatments, relative to that of the P0 treatment. Co-occurrence network analysis revealed that long-term P fertilization increased network complexity, as reflected by the larger edge number and higher average degree in the P1 and P2 treatments than in the P0 treatment, which may enhance the network stability by reducing the spread of indirect effects in the treatments with P application. Moreover, the P1 and P2 treatments had a higher ratio of positive edges, indicating more cooperators in the P1 and P2 treatments, whereas more defectors occurred in the P0 treatment. Our results demonstrated that long-term P application can improve P availability, reduce fungal community diversity, alter fungal community structure, increase saprophytic taxa, eliminate pathogenic and symbiotic taxa, and enhance network complexity and stability in lime concretion black soil.
Phosphorus(P) deficiency is a limiting factor for agricultural production in the region covered with lime concretion black soil. Application of chemical P fertilizer is a common strategy to improve P availability. Numerous studies have demonstrated the essential role of P fertilization on soil fertility and crop yield, whereas relatively little is known about the effects of long-term P application on the belowground fungal community. The overall objective of this study was to investigate the effects of long-term P fertilization on fungal community diversity, composition, and intraspecific interactions in a lime concretion black soil, and to assess how the effects varied with application rate. Soils from a 21-year field experiment located in Mengcheng County, Anhui Province, were used, with treatments including three levels of P application rates, i.e.(1) P0: unamended control,(2) P1: chemical P fertilizer was applied at P_2O_5 45 kg/hm~2, and(3) P2: chemical P fertilizer was applied at P_2O_5 90 kg/hm~2. ITS1 gene pyrosequencing was employed to characterize the fungal community diversity and composition. The results showed that long-term P fertilization significantly improved soil fertility. Compared with the P0 treatment, the total P(TP) from the P2 and P1 treatments was 40.00% and 24.00% higher, and the available P(AP) was 384% and 144% higher, respectively. The Shannon index decreased with the P application rates, and was significantly negatively correlated with TP(r=-0.678, P=0.045) and AP(r=-0.677, P=0.045). Ascomycota was the dominant phylum in the studied soil, with its relative abundance being 65.71%—79.86%. Principal coordinate analysis(PCoA) revealed that the fungal community structure differed significantly among the different treatments. Redundancy analysis(RDA) further suggested that the fungal community structure was mainly determined by TP and dissolved organic carbon(DOC). Compared with the P0 treatment, the relative abundance of Ascomycota from P2 and P1 was 9.87% and 11.75% higher, and that of Sordariomycetes was 28.63% and 15.97% higher, respectively. Conversely, the relative abundance of Mortierellomycota from P2 and P1 was 42.63% and 43.81% lower, and that of Mortierellomycetes was 43.82% and 42.63% lower, respectively. Long-term P fertilization resulted in a significant enrichment of saprophytic fungi, namely, the genera of Plenodomus, Penicillium, and Arthrobotrys were enriched in the P1 treatment, and the genera of Cyphellophora, Zopfiella, Guehomyces, Mortierella, and Mucor were enriched in the P2 treatment. However, pathogenic(i.e., Simplicillium and Magnaporthiopsis) and symbiotic(i.e., Sagenomella and Nigrospora) fungi were depleted in the P1 and P2 treatments, relative to that of the P0 treatment. Co-occurrence network analysis revealed that long-term P fertilization increased network complexity, as reflected by the larger edge number and higher average degree in the P1 and P2 treatments than in the P0 treatment, which may enhance the network stability by reducing the spread of indirect effects in the treatments with P application. Moreover, the P1 and P2 treatments had a higher ratio of positive edges, indicating more cooperators in the P1 and P2 treatments, whereas more defectors occurred in the P0 treatment. Our results demonstrated that long-term P application can improve P availability, reduce fungal community diversity, alter fungal community structure, increase saprophytic taxa, eliminate pathogenic and symbiotic taxa, and enhance network complexity and stability in lime concretion black soil.
引文
[1] 王道中,郭熙盛,何传龙,刘枫.砂姜黑土长期定位施肥对小麦生长及土壤养分含量的影响.土壤通报,2007,38(1):55- 57.
[2] 李玮,乔玉强,陈欢,曹承富,杜世州,赵竹.秸秆还田和施肥对砂姜黑土理化性质及小麦-玉米产量的影响.生态学报,2014,34(17):5052- 5061.
[3] 王道中,郭熙盛,刘枫,何传龙.长期施肥对砂姜黑土无机磷形态的影响.植物营养与肥料学报,2009,15(3):601- 606.
[4] Beauregard M S,Hamel C,Atul-Nayyar,St-Arnaud M.Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa.Microbial Ecology,2010,59(2):379- 389.
[5] 马垒,郭志彬,王道中,赵炳梓.长期三水平磷肥施用梯度对砂姜黑土细菌群落结构和酶活性的影响.土壤学报,Doi:10.11766/trxb201805080149.
[6] Deacon J.Introduction:the fungi and fungal activities//Deacon J,ed.Fungal Biology.Malden,MA:Blackwell Publishing Ltd,2013:1- 15.
[7] Bao Z H,Matsushita Y,Morimoto S,Hoshino Y T,Suzuki C,Nagaoka K,Takenaka M,Murakami H,Kuroyanagi Y,Urashima Y,Sekiguchi H,Kushida A,Toyota K,Saito M,Tsushima S.Decrease in fungal biodiversity along an available phosphorous gradient in arable andosol soils in Japan.Canadian Journal of Microbiology,2013,59(6):368- 373.
[8] Liu M,Liu J,Chen X F,Jiang C Y,Wu M,Li Z P.Shifts in bacterial and fungal diversity in a paddy soil faced with phosphorus surplus.Biology and Fertility of Soils,2018,54(2):259- 267.
[9] Cheng Y,Ishimoto K,Kuriyama Y,Osaki M,Ezawa T.Ninety-year-,but not single,application of phosphorus fertilizer has a major impact on arbuscular mycorrhizal fungal communities.Plant and Soil,2013,365(1/2):397- 407.
[10] Song G,Chen R,Xiang W,Yang F,Zheng S,Zhang J,Zhang J,Lin X.Contrasting effects of long-term fertilization on the community of saprotrophic fungi and arbuscular mycorrhizal fungi in a sandy loam soil.Plant Soil and Environment,2015,61(3):127- 136.
[11] He D,Xiang X J,He J S,Wang C,Cao G M,Adams J,Chu H Y.Composition of the soil fungal community is more sensitive to phosphorus than nitrogen addition in the alpine meadow on the Qinghai-Tibetan Plateau.Biology and Fertility of Soils,2016,52(8):1059- 1072.
[12] 鲁如坤.土壤农业化学分析方法.北京:中国农业科技出版社,2000.
[13] Güsewell S,Gessner M O.N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms.Functional Ecology,2009,23(1):211- 219.
[14] Tapia-Torres Y,Rodríguez-Torres M D,Elser J J,Islas A,Souza V,García-Oliva F,Olmedo-álvarez G.How to live with phosphorus scarcity in soil and sediment:lessons from bacteria.Applied and Environmental Microbiology,2016,82(15):4652- 4662.
[15] Mouginot C,Kawamura R,Matulich K L,Berlemont R,Allison S D,Amend A S,Martiny A C.Elemental stoichiometry of fungi and bacteria strains from grassland leaf litter.Soil Biology and Biochemistry,2014,76:278- 285.
[16] Dighton J,White J F.The Fungal Community:Its Organization and Role in the Ecosystem.4th ed.Boca Raton:CRC Press,2017:501- 508.
[17] Ma M C,Jiang X,Wang Q F,Ongena M,Wei D,Ding J L,Guan D W,Cao F M,Zhao B S,Li J.Responses of fungal community composition to long-term chemical and organic fertilization strategies in Chinese mollisols.MicrobiologyOpen,2018,7(5):e00597.
[18] Sun R B,Dsouza M,Gilbert J A,Guo X S,Wang D Z,Guo Z B,Ni Y Y,Chu H Y.Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter.Environmental Microbiology,2016,18(12):5137- 5150.
[19] Ma A Z,Zhuang X L,Wu J M,Cui M M,Lv D,Liu C Z,Zhuang G Q.Ascomycota members dominate fungal communities during straw residue decomposition in arable soil.PLoS One,2013,8(6):e66146.
[20] Zhou J,Jiang X,Zhou B K,Zhao B S,Ma M C,Guan D W,Li J,Chen S F,Cao F M,Shen D L,Qin J.Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China.Soil Biology and Biochemistry,2016,95:135- 143.
[21] Dean S L,Farrer E C,Taylor D L,Porras-Alfaro A,Suding K N,Sinsabaugh R L.Nitrogen deposition alters plant-fungal relationships:linking belowground dynamics to aboveground vegetation change.Molecular Ecology,2014,23(6):1364- 1378.
[22] Ward N A,Schneider R W,Aime M C.Colonization of soybean rust sori by Simplicillium lanosoniveum.Fungal Ecology,2011,4(5):303- 308.
[23] Bei S K,Zhang Y L,Li T T,Christie P,Li X L,Zhang J L.Response of the soil microbial community to different fertilizer inputs in a wheat-maize rotation on a calcareous soil.Agriculture,Ecosystems & Environment,2018,260:58- 69.
[24] Tian J J,Gao X X,Zhang W M,Wang L,Qu L H.Molecular identification of endophytic fungi from aquilaria sinensis and artificial agarwood induced by pinholes-infusion technique.African Journal of Biotechnology,2013,12(21):3115- 3131.
[25] Zhao R L,Li W J,Zhang Y,Lin F C,Wang Y,Yang J Z,Hyde K D.Endophytic fungi from the medicinal plant,Panax notoginseng,isolated from healthy and root-rot diseased individuals.Chiang Mai Journal of Science,2014,41(2):249- 261.
[26] Eichlerová I,Homolka L,?if■ková L,Lisá L,Dobiá?ová P,Baldrian P.Enzymatic systems involved in decomposition reflects the ecology and taxonomy of saprotrophic fungi.Fungal Ecology,2015,13:10- 22.
[27] Va?utová M,Edwards-Joná?ová M,Baldrian ■.Distinct environmental variables drive the community composition of mycorrhizal and saprotrophic fungi at the alpine treeline ecotone.Fungal Ecology,2017,27:116- 124.
[28] Huang X Q,Liu L L,Wen T,Zhu R,Zhang J B,Cai Z C.Illumina MiSeq investigations on the changes of microbial community in the Fusarium oxysporum f.sp.cubense infected soil during and after reductive soil disinfestation.Microbiological Research,2015,181:33- 42.
[29] Francioli D,Schulz E,Lentendu G,Wubet T,Buscot F,Reitz T.Mineral vs.Organic amendments:microbial community structure,activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies.Frontiers in Microbiology,2016,7:1446.
[30] Suweis S,Grilli J,Banavar J R,Allesina S,Maritan A.Effect of localization on the stability of mutualistic ecological networks.Nature Communications,2015,6:10179.
[31] Feng Y Z,Guo Z Y,Zhong L H,Zhao F,Zhang J B,Lin X G.Balanced fertilization decreases environmental filtering on soil bacterial community assemblage in north china.Frontiers in Microbiology,2017,8:2376.
[32] Xun W B,Huang T,Li W,Ren Y,Xiong W,Ran W,Li D C,Shen Q R,Zhang R F.Alteration of soil bacterial interaction networks driven by different long-term fertilization management practices in the red soil of South China.Applied Soil Ecology,2017,120:128- 134.
[2] 李玮,乔玉强,陈欢,曹承富,杜世州,赵竹.秸秆还田和施肥对砂姜黑土理化性质及小麦-玉米产量的影响.生态学报,2014,34(17):5052- 5061.
[3] 王道中,郭熙盛,刘枫,何传龙.长期施肥对砂姜黑土无机磷形态的影响.植物营养与肥料学报,2009,15(3):601- 606.
[4] Beauregard M S,Hamel C,Atul-Nayyar,St-Arnaud M.Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa.Microbial Ecology,2010,59(2):379- 389.
[5] 马垒,郭志彬,王道中,赵炳梓.长期三水平磷肥施用梯度对砂姜黑土细菌群落结构和酶活性的影响.土壤学报,Doi:10.11766/trxb201805080149.
[6] Deacon J.Introduction:the fungi and fungal activities//Deacon J,ed.Fungal Biology.Malden,MA:Blackwell Publishing Ltd,2013:1- 15.
[7] Bao Z H,Matsushita Y,Morimoto S,Hoshino Y T,Suzuki C,Nagaoka K,Takenaka M,Murakami H,Kuroyanagi Y,Urashima Y,Sekiguchi H,Kushida A,Toyota K,Saito M,Tsushima S.Decrease in fungal biodiversity along an available phosphorous gradient in arable andosol soils in Japan.Canadian Journal of Microbiology,2013,59(6):368- 373.
[8] Liu M,Liu J,Chen X F,Jiang C Y,Wu M,Li Z P.Shifts in bacterial and fungal diversity in a paddy soil faced with phosphorus surplus.Biology and Fertility of Soils,2018,54(2):259- 267.
[9] Cheng Y,Ishimoto K,Kuriyama Y,Osaki M,Ezawa T.Ninety-year-,but not single,application of phosphorus fertilizer has a major impact on arbuscular mycorrhizal fungal communities.Plant and Soil,2013,365(1/2):397- 407.
[10] Song G,Chen R,Xiang W,Yang F,Zheng S,Zhang J,Zhang J,Lin X.Contrasting effects of long-term fertilization on the community of saprotrophic fungi and arbuscular mycorrhizal fungi in a sandy loam soil.Plant Soil and Environment,2015,61(3):127- 136.
[11] He D,Xiang X J,He J S,Wang C,Cao G M,Adams J,Chu H Y.Composition of the soil fungal community is more sensitive to phosphorus than nitrogen addition in the alpine meadow on the Qinghai-Tibetan Plateau.Biology and Fertility of Soils,2016,52(8):1059- 1072.
[12] 鲁如坤.土壤农业化学分析方法.北京:中国农业科技出版社,2000.
[13] Güsewell S,Gessner M O.N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms.Functional Ecology,2009,23(1):211- 219.
[14] Tapia-Torres Y,Rodríguez-Torres M D,Elser J J,Islas A,Souza V,García-Oliva F,Olmedo-álvarez G.How to live with phosphorus scarcity in soil and sediment:lessons from bacteria.Applied and Environmental Microbiology,2016,82(15):4652- 4662.
[15] Mouginot C,Kawamura R,Matulich K L,Berlemont R,Allison S D,Amend A S,Martiny A C.Elemental stoichiometry of fungi and bacteria strains from grassland leaf litter.Soil Biology and Biochemistry,2014,76:278- 285.
[16] Dighton J,White J F.The Fungal Community:Its Organization and Role in the Ecosystem.4th ed.Boca Raton:CRC Press,2017:501- 508.
[17] Ma M C,Jiang X,Wang Q F,Ongena M,Wei D,Ding J L,Guan D W,Cao F M,Zhao B S,Li J.Responses of fungal community composition to long-term chemical and organic fertilization strategies in Chinese mollisols.MicrobiologyOpen,2018,7(5):e00597.
[18] Sun R B,Dsouza M,Gilbert J A,Guo X S,Wang D Z,Guo Z B,Ni Y Y,Chu H Y.Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter.Environmental Microbiology,2016,18(12):5137- 5150.
[19] Ma A Z,Zhuang X L,Wu J M,Cui M M,Lv D,Liu C Z,Zhuang G Q.Ascomycota members dominate fungal communities during straw residue decomposition in arable soil.PLoS One,2013,8(6):e66146.
[20] Zhou J,Jiang X,Zhou B K,Zhao B S,Ma M C,Guan D W,Li J,Chen S F,Cao F M,Shen D L,Qin J.Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China.Soil Biology and Biochemistry,2016,95:135- 143.
[21] Dean S L,Farrer E C,Taylor D L,Porras-Alfaro A,Suding K N,Sinsabaugh R L.Nitrogen deposition alters plant-fungal relationships:linking belowground dynamics to aboveground vegetation change.Molecular Ecology,2014,23(6):1364- 1378.
[22] Ward N A,Schneider R W,Aime M C.Colonization of soybean rust sori by Simplicillium lanosoniveum.Fungal Ecology,2011,4(5):303- 308.
[23] Bei S K,Zhang Y L,Li T T,Christie P,Li X L,Zhang J L.Response of the soil microbial community to different fertilizer inputs in a wheat-maize rotation on a calcareous soil.Agriculture,Ecosystems & Environment,2018,260:58- 69.
[24] Tian J J,Gao X X,Zhang W M,Wang L,Qu L H.Molecular identification of endophytic fungi from aquilaria sinensis and artificial agarwood induced by pinholes-infusion technique.African Journal of Biotechnology,2013,12(21):3115- 3131.
[25] Zhao R L,Li W J,Zhang Y,Lin F C,Wang Y,Yang J Z,Hyde K D.Endophytic fungi from the medicinal plant,Panax notoginseng,isolated from healthy and root-rot diseased individuals.Chiang Mai Journal of Science,2014,41(2):249- 261.
[26] Eichlerová I,Homolka L,?if■ková L,Lisá L,Dobiá?ová P,Baldrian P.Enzymatic systems involved in decomposition reflects the ecology and taxonomy of saprotrophic fungi.Fungal Ecology,2015,13:10- 22.
[27] Va?utová M,Edwards-Joná?ová M,Baldrian ■.Distinct environmental variables drive the community composition of mycorrhizal and saprotrophic fungi at the alpine treeline ecotone.Fungal Ecology,2017,27:116- 124.
[28] Huang X Q,Liu L L,Wen T,Zhu R,Zhang J B,Cai Z C.Illumina MiSeq investigations on the changes of microbial community in the Fusarium oxysporum f.sp.cubense infected soil during and after reductive soil disinfestation.Microbiological Research,2015,181:33- 42.
[29] Francioli D,Schulz E,Lentendu G,Wubet T,Buscot F,Reitz T.Mineral vs.Organic amendments:microbial community structure,activity and abundance of agriculturally relevant microbes are driven by long-term fertilization strategies.Frontiers in Microbiology,2016,7:1446.
[30] Suweis S,Grilli J,Banavar J R,Allesina S,Maritan A.Effect of localization on the stability of mutualistic ecological networks.Nature Communications,2015,6:10179.
[31] Feng Y Z,Guo Z Y,Zhong L H,Zhao F,Zhang J B,Lin X G.Balanced fertilization decreases environmental filtering on soil bacterial community assemblage in north china.Frontiers in Microbiology,2017,8:2376.
[32] Xun W B,Huang T,Li W,Ren Y,Xiong W,Ran W,Li D C,Shen Q R,Zhang R F.Alteration of soil bacterial interaction networks driven by different long-term fertilization management practices in the red soil of South China.Applied Soil Ecology,2017,120:128- 134.
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