热带珊瑚岛植物种植对土壤改良及其微生物群落形成的影响
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摘要
植被及关联的土壤微生物对于维持热带珊瑚岛的生态系统功能和稳定性具有重要作用。采集了植物种植前的种植土和种植早期珊瑚砂土,以及栽植幼苗基质中的根际土和非根际土,利用扩增子测序的手段,分析其中的真菌和细菌的多样性、群落组成及变化。分析结果显示,种植土、幼苗基质中的非根际土和根际土可能是珊瑚砂土壤中微生物的重要来源,其中最主要的类群包括以担子菌门和接合菌门为代表的真菌,以及以变形菌门、酸杆菌门为代表的细菌。珊瑚砂土的真菌丰度(864.2±41.4,为每0.25 g土的物种数)显著低于来自苗基质的根际土(1086.1±64.3,P=0.014)和苗非根际土(1251.4±48.1,P<0.001);珊瑚砂土的细菌丰度与苗基质根际土和非根际土之间并没有显著性差异。通过对比种植土和植物种植后的珊瑚砂土的微生物群落β-多样性,也发现植物种植对真菌和细菌类群组成产生了影响;主要类群接合菌门真菌相对丰度从0.2%增加到17.4%,而伞菌纲真菌的相对丰度从20.8%下降到0.9%,β-变形菌纲细菌的相对丰度从17.7%下降到0.1%。研究结果启示,珊瑚砂土壤微生物的组成并非是对不同来源微生物进行简单的集合,其中生活史与植物关系密切的微生物类群,目前还未在珊瑚砂土壤中表现出优势分布;相反,一些在植物根际和非根际土中较少出现的微生物,在珊瑚砂土壤中则广为存在,从而说明土壤微生物群落恢复过程的复杂性。
Vegetation and associated soil microbial community play important roles in the maintenance of the function and stability of tropical coral island ecosystems. In this study, we collected different soil samples from a tropical coral island at the preliminary stage of plant community establishment. These soil samples included bulk soils before and after plant establishment(coral sand), nutrition soils used during planting(nutrition soils), and the bulk and rhizosphere soils of the transplanted seedlings in the nursery(nursery bulk and rhizosphere soils). Using amplicon sequencing, we assessed and compared the diversity, composition, and variation of fungal and bacterial communities among the four types of soil samples. Our results showed that the nutrition soils, nursery bulk and rhizosphere soils were important sources for microbial community restoration in coral sands. The major fungal phylums in these soils included Ascomycota and Zygomycota, while the major bacterial phylums included Proteobacteria and Acidobacteria. Fungal richness was significantly lower in coral sands(864.2±41.4) than in nursery rhizosphere(1086.1±64.3, P=0.014) and nursery bulk soils(1251.4±48.1, P<0.001). However, no significant difference in the bacterial richness was detected among these soils. The establishment of plant community also significantly altered the composition of both fungal and bacterial communities in the coral sands; the relative abundance of Zygomycota increased from 0.2% to 17.4%, Agaricomycetes decreased from 20.8% to 0.9%, and β-Proteobacteria decreased from 17.7% to 0.1%. Our results demonstrate that the process of microbial community restoration in the coral sands is not simply fulfilled by adding up microbial groups from the different soil sources; several microbial groups with lifestyles being closely associated with plants were not predominant in the coral sands. Furthermore, some microbial groups with lower relative abundances in the seedling soil samples were dominant in coral sands, suggesting that the soil microbial community restoration was complex.
Vegetation and associated soil microbial community play important roles in the maintenance of the function and stability of tropical coral island ecosystems. In this study, we collected different soil samples from a tropical coral island at the preliminary stage of plant community establishment. These soil samples included bulk soils before and after plant establishment(coral sand), nutrition soils used during planting(nutrition soils), and the bulk and rhizosphere soils of the transplanted seedlings in the nursery(nursery bulk and rhizosphere soils). Using amplicon sequencing, we assessed and compared the diversity, composition, and variation of fungal and bacterial communities among the four types of soil samples. Our results showed that the nutrition soils, nursery bulk and rhizosphere soils were important sources for microbial community restoration in coral sands. The major fungal phylums in these soils included Ascomycota and Zygomycota, while the major bacterial phylums included Proteobacteria and Acidobacteria. Fungal richness was significantly lower in coral sands(864.2±41.4) than in nursery rhizosphere(1086.1±64.3, P=0.014) and nursery bulk soils(1251.4±48.1, P<0.001). However, no significant difference in the bacterial richness was detected among these soils. The establishment of plant community also significantly altered the composition of both fungal and bacterial communities in the coral sands; the relative abundance of Zygomycota increased from 0.2% to 17.4%, Agaricomycetes decreased from 20.8% to 0.9%, and β-Proteobacteria decreased from 17.7% to 0.1%. Our results demonstrate that the process of microbial community restoration in the coral sands is not simply fulfilled by adding up microbial groups from the different soil sources; several microbial groups with lifestyles being closely associated with plants were not predominant in the coral sands. Furthermore, some microbial groups with lower relative abundances in the seedling soil samples were dominant in coral sands, suggesting that the soil microbial community restoration was complex.
引文
[1] 刘东明,陈红锋,王发国,易绮斐,邢福武.我国南沙群岛岛礁引种植物调查.热带亚热带植物学报,2015,23(2):167- 175.
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[7] 李刚,修伟明,王杰,于雯超,吴元凤,赵建宁,宋晓龙,杨殿林.呼伦贝尔沙地不同植被恢复模式土壤氨氧化细菌群落结构及多样性.农业环境科学学报,2014,33(1):111- 120.
[8] 钟芳,柴晓虹,王国基,段争虎.植被恢复方式对黄土丘陵区土壤理化性质及微生物特性的影响.中国沙漠,2014,34(4):1064- 1072.
[9] Jung J,Yeom J,Han J,Kim J,Park W.Seasonal changes in nitrogen-cycle gene abundances and in bacterial communities in acidic forest soils.Journal of Microbiology,2012,50(3):365- 373.
[10] Desai M S,Assig K,Dattagupta S.Nitrogen fixation in distinct microbial niches within a chemoautotrophy-driven cave ecosystem.The ISME Journal,2013,7(12):2411- 2423.
[11] Inoue J I,Oshima K,Suda W,Sakamoto M,Iino T,Noda S,Hongoh Y,Hattori M,Ohkuma M.Distribution and evolution of nitrogen fixation genes in the phylum Bacteroidetes.Microbes and Environments,2015,30(1):44- 50.
[12] Stein L Y,Klotz M G.The nitrogen cycle.Current Biology,2016,26(3):R94-R98.
[13] Yadav V,Kumar M,Deep D K,Kumar H,Sharma R,Tripathi T,Tuteja N,Saxena A K,Johri A K.A phosphate transporter root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant.The Journal of Biological Chemistry,2010,285(34):26532- 26544.
[14] Rosconi F,Trovero M F,de Souza E M,Fabiano E.Serobactins-mediated iron acquisition systems optimize competitive fitness of Herbaspirillum seropedicae inside rice plants.Environmental Microbiology,2016,18(8):2523- 2533.
[15] van der Heijden M G A,Bardgett R D,van Straalen N M.The unseen majority:soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems.Ecology Letters,2008,11(3):296- 310.
[16] Chowdhury S P,Uhl J,Grosch R,Alquéres S,Pittroff S,Dietel K,Schmitt-Kopplin P,Borriss R,Hartmann A.Cyclic Lipopeptides of Bacillus amyloliquefaciens subsp.plantarum colonizing the lettuce rhizosphere enhance plant defense responses toward the bottom rot pathogen Rhizoctonia solani.Molecular Plant-Microbe Interactions,2015,28(9):984- 995.
[17] 张守仕,谢克英,乔宝营,张娜.果树根际土壤取样分析技术研究.落叶果树,2015,47(6):25- 27.
[18] Martin K J,Rygiewicz P T.Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts.BMC Microbiology,2005,5:28.
[19] Purahong W,Wubet T,Lentendu G,Schloter M,Pecyna M J,Kapturska D,Hofrichter M,Krüger D,Buscot F.Life in leaf litter:novel insights into community dynamics of bacteria and fungi during litter decomposition.Molecular Ecology,2016,25(16):4059- 4074.
[20] Caporaso J G,Kuczynski J,Stombaugh J,Bittinger K,Bushman F D,Costello E K,Fierer N,Peňa A G,Goodrich J K,Gordon J I,Huttley G A,Kelley S T,Knights D,Koenig J E,Ley R E,Lozupone C A,McDonald D,Muegge B D,Pirrung M,Reeder J,Sevinsky J R,Turnbaugh P J,Walters W A,Widmann J,Yatsunenko T,Zaneveld J,Knight R.QIIME allows analysis of high-throughput community sequencing data.Nature Methods,2010,7(5):335- 336.
[21] Edgar R C,Haas B J,Clemente J C,Quince C,Knight R.UCHIME improves sensitivity and speed of chimera detection.Bioinformatics,2011,27(16):2194- 2200.
[22] Edgar R C.UPARSE:highly accurate OTU sequences from microbial amplicon reads.Nature Methods,2013,10(10):996- 998.
[23] R Core Team.R:A language and environment for statistical computing.R Foundation for Statistical Computing,Vienna,Austria,2013,URL:http://www.R-project.org/.
[24] Lanzén A,Epelde L,Blanco F,Martín I,Artetxe U,Garbisu C.Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient.Scientific Reports,2016,6:28257.
[25] ?tursová M,Bárta J,?antr■ spatial heterogeneity of ecosystem properties,microbial community composition and microbial activities in a temperate mountain forest soil.FEMS Microbiology Ecology,2016,92(12),doi:10.1093/femsec/fiw185.
[26] ?if■ková L,Větrovsk■.Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter.Environmental Microbiology,2016,18(1):288- 301.
[27] Nguema-Ona E,Vicré-gibouin M,Cannesan M A,Driouich A.Arabinogalactan proteins in root-microbe interactions.Trends in Plant Science,2013,18(8):440- 449.
[28] Mao Y J,Li X Z,Smyth E M,Yannarell A C,Mackie R I.Enrichment of specific bacterial and eukaryotic microbes in the rhizosphere of switchgrass (Panicum virgatum L.) through root exudates.Environmental Microbiology Reports,2014,6(3):293- 306.
[29] Wu L K,Wang J Y,Huang W M,Wu H M,Chen J,Yang Y Q,Zhang Z Y,Lin W X.Plant-microbe rhizosphere interactions mediated by Rehmannia glutinosa root exudates under consecutive monoculture.Scientific Reports,2015,5:15871,doi:10.1038/srep15871.
[30] Perdomo H,García D,Gené J,Cano J,Sutton D A,Summerbell R,Guarro J.Phialemoniopsis,a new genus of Sordariomycetes,and new species of Phialemonium and Lecythophora.Mycologia,2013,105(2):398- 421.
[31] Chen H,Ma Y,Zhang W F,Ma T,Wu H X.Molecular phylogeny of Colletotrichum (Sordariomycetes:Glomerellaceae) inferred from multiple gene sequences.Genetics and Molecular Research,2015,14(4):13649- 13662.
[32] Réblová M,Réblová K,?těpánek V.Molecular systematics of Barbatosphaeria (Sordariomycetes):multigene phylogeny and secondary ITS structure.Persoonia-Molecular Phylogeny and Evolution of Fungi,2015,35:21- 38.
[33] Liers C,Pecyna M J,Kellner H,Worrich A,Zorn H,Steffen K T,Hofrichter M,Ullrich R.Substrate oxidation by dye-decolorizing peroxidases (DyPs) from wood- and litter-degrading agaricomycetes compared to other fungal and plant heme-peroxidases.Applied Microbiology and Biotechnology,2013,97(13):5839- 5849.
[34] Mali T,Kuuskeri J,Shah F,Lundell T K.Interactions affect hyphal growth and enzyme profiles in combinations of coniferous wood-decaying fungi of Agaricomycetes.PLoS One,2017,12(9):e0185171,doi:10.1371/journal.pone.0185171.
[35] Lys?e E,Harris L J,Walkowiak S,Subramaniam R,Divon H H,Riiser E S,Llorens C,Gabaldón T,Kistler H C,Jonkers W,Kolseth A K,Nielsen K F,Thrane U,Frandsen R J N.The genome of the generalist plant pathogen Fusarium avenaceum is enriched with genes involved in redox,signaling and secondary metabolism.PLoS One,2014,9(11):e112703,doi:10.1371/journal.pone.0112703.
[36] Dang H X,Pryor B,Peever T,Lawrence C B.The Alternaria genomes database:a comprehensive resource for a fungal genus comprised of saprophytes,plant pathogens,and allergenic species.BMC Genomics,2015,16:239,doi:10.1186/s12864-015- 1430- 7.
[2] 任海,简曙光,张倩媚,王发国,沈彤,王俊.中国南海诸岛的植物和植被现状.生态环境学报,2017,26(10):1639- 1648.
[3] 王玮韧,郝珖存,王俊,张炜,黄峰,陆宏芳,简曙光,何聃,申卫军.珊瑚岛礁表层土壤的主要化学性质分析.热带亚热带植物学报,2018,26(5):465- 472.
[4] 邢福武,吴德邻,李泽贤,赵焕庭,陈史坚.我国南沙群岛的植物与植被概况.广西植物,1994,14(2):151- 156.
[5] 童毅,简曙光,陈权,李玉玲,邢福武.中国西沙群岛植物多样性.生物多样性,2013,21(3):364- 374.
[6] 翁伯琦,郑祥洲,丁洪,王煌平.植被恢复对土壤碳氮循环的影响研究进展.应用生态学报,2013,24(12):3610- 3616.
[7] 李刚,修伟明,王杰,于雯超,吴元凤,赵建宁,宋晓龙,杨殿林.呼伦贝尔沙地不同植被恢复模式土壤氨氧化细菌群落结构及多样性.农业环境科学学报,2014,33(1):111- 120.
[8] 钟芳,柴晓虹,王国基,段争虎.植被恢复方式对黄土丘陵区土壤理化性质及微生物特性的影响.中国沙漠,2014,34(4):1064- 1072.
[9] Jung J,Yeom J,Han J,Kim J,Park W.Seasonal changes in nitrogen-cycle gene abundances and in bacterial communities in acidic forest soils.Journal of Microbiology,2012,50(3):365- 373.
[10] Desai M S,Assig K,Dattagupta S.Nitrogen fixation in distinct microbial niches within a chemoautotrophy-driven cave ecosystem.The ISME Journal,2013,7(12):2411- 2423.
[11] Inoue J I,Oshima K,Suda W,Sakamoto M,Iino T,Noda S,Hongoh Y,Hattori M,Ohkuma M.Distribution and evolution of nitrogen fixation genes in the phylum Bacteroidetes.Microbes and Environments,2015,30(1):44- 50.
[12] Stein L Y,Klotz M G.The nitrogen cycle.Current Biology,2016,26(3):R94-R98.
[13] Yadav V,Kumar M,Deep D K,Kumar H,Sharma R,Tripathi T,Tuteja N,Saxena A K,Johri A K.A phosphate transporter root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant.The Journal of Biological Chemistry,2010,285(34):26532- 26544.
[14] Rosconi F,Trovero M F,de Souza E M,Fabiano E.Serobactins-mediated iron acquisition systems optimize competitive fitness of Herbaspirillum seropedicae inside rice plants.Environmental Microbiology,2016,18(8):2523- 2533.
[15] van der Heijden M G A,Bardgett R D,van Straalen N M.The unseen majority:soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems.Ecology Letters,2008,11(3):296- 310.
[16] Chowdhury S P,Uhl J,Grosch R,Alquéres S,Pittroff S,Dietel K,Schmitt-Kopplin P,Borriss R,Hartmann A.Cyclic Lipopeptides of Bacillus amyloliquefaciens subsp.plantarum colonizing the lettuce rhizosphere enhance plant defense responses toward the bottom rot pathogen Rhizoctonia solani.Molecular Plant-Microbe Interactions,2015,28(9):984- 995.
[17] 张守仕,谢克英,乔宝营,张娜.果树根际土壤取样分析技术研究.落叶果树,2015,47(6):25- 27.
[18] Martin K J,Rygiewicz P T.Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts.BMC Microbiology,2005,5:28.
[19] Purahong W,Wubet T,Lentendu G,Schloter M,Pecyna M J,Kapturska D,Hofrichter M,Krüger D,Buscot F.Life in leaf litter:novel insights into community dynamics of bacteria and fungi during litter decomposition.Molecular Ecology,2016,25(16):4059- 4074.
[20] Caporaso J G,Kuczynski J,Stombaugh J,Bittinger K,Bushman F D,Costello E K,Fierer N,Peňa A G,Goodrich J K,Gordon J I,Huttley G A,Kelley S T,Knights D,Koenig J E,Ley R E,Lozupone C A,McDonald D,Muegge B D,Pirrung M,Reeder J,Sevinsky J R,Turnbaugh P J,Walters W A,Widmann J,Yatsunenko T,Zaneveld J,Knight R.QIIME allows analysis of high-throughput community sequencing data.Nature Methods,2010,7(5):335- 336.
[21] Edgar R C,Haas B J,Clemente J C,Quince C,Knight R.UCHIME improves sensitivity and speed of chimera detection.Bioinformatics,2011,27(16):2194- 2200.
[22] Edgar R C.UPARSE:highly accurate OTU sequences from microbial amplicon reads.Nature Methods,2013,10(10):996- 998.
[23] R Core Team.R:A language and environment for statistical computing.R Foundation for Statistical Computing,Vienna,Austria,2013,URL:http://www.R-project.org/.
[24] Lanzén A,Epelde L,Blanco F,Martín I,Artetxe U,Garbisu C.Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient.Scientific Reports,2016,6:28257.
[25] ?tursová M,Bárta J,?antr■ spatial heterogeneity of ecosystem properties,microbial community composition and microbial activities in a temperate mountain forest soil.FEMS Microbiology Ecology,2016,92(12),doi:10.1093/femsec/fiw185.
[26] ?if■ková L,Větrovsk■.Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter.Environmental Microbiology,2016,18(1):288- 301.
[27] Nguema-Ona E,Vicré-gibouin M,Cannesan M A,Driouich A.Arabinogalactan proteins in root-microbe interactions.Trends in Plant Science,2013,18(8):440- 449.
[28] Mao Y J,Li X Z,Smyth E M,Yannarell A C,Mackie R I.Enrichment of specific bacterial and eukaryotic microbes in the rhizosphere of switchgrass (Panicum virgatum L.) through root exudates.Environmental Microbiology Reports,2014,6(3):293- 306.
[29] Wu L K,Wang J Y,Huang W M,Wu H M,Chen J,Yang Y Q,Zhang Z Y,Lin W X.Plant-microbe rhizosphere interactions mediated by Rehmannia glutinosa root exudates under consecutive monoculture.Scientific Reports,2015,5:15871,doi:10.1038/srep15871.
[30] Perdomo H,García D,Gené J,Cano J,Sutton D A,Summerbell R,Guarro J.Phialemoniopsis,a new genus of Sordariomycetes,and new species of Phialemonium and Lecythophora.Mycologia,2013,105(2):398- 421.
[31] Chen H,Ma Y,Zhang W F,Ma T,Wu H X.Molecular phylogeny of Colletotrichum (Sordariomycetes:Glomerellaceae) inferred from multiple gene sequences.Genetics and Molecular Research,2015,14(4):13649- 13662.
[32] Réblová M,Réblová K,?těpánek V.Molecular systematics of Barbatosphaeria (Sordariomycetes):multigene phylogeny and secondary ITS structure.Persoonia-Molecular Phylogeny and Evolution of Fungi,2015,35:21- 38.
[33] Liers C,Pecyna M J,Kellner H,Worrich A,Zorn H,Steffen K T,Hofrichter M,Ullrich R.Substrate oxidation by dye-decolorizing peroxidases (DyPs) from wood- and litter-degrading agaricomycetes compared to other fungal and plant heme-peroxidases.Applied Microbiology and Biotechnology,2013,97(13):5839- 5849.
[34] Mali T,Kuuskeri J,Shah F,Lundell T K.Interactions affect hyphal growth and enzyme profiles in combinations of coniferous wood-decaying fungi of Agaricomycetes.PLoS One,2017,12(9):e0185171,doi:10.1371/journal.pone.0185171.
[35] Lys?e E,Harris L J,Walkowiak S,Subramaniam R,Divon H H,Riiser E S,Llorens C,Gabaldón T,Kistler H C,Jonkers W,Kolseth A K,Nielsen K F,Thrane U,Frandsen R J N.The genome of the generalist plant pathogen Fusarium avenaceum is enriched with genes involved in redox,signaling and secondary metabolism.PLoS One,2014,9(11):e112703,doi:10.1371/journal.pone.0112703.
[36] Dang H X,Pryor B,Peever T,Lawrence C B.The Alternaria genomes database:a comprehensive resource for a fungal genus comprised of saprophytes,plant pathogens,and allergenic species.BMC Genomics,2015,16:239,doi:10.1186/s12864-015- 1430- 7.
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