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Slope aspect influences arbuscular mycorrhizal fungus communities in arid ecosystems of the Daqingshan Mountains, Inner Mongolia, North China

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Abstract

Arbuscular mycorrhizal (AM) symbiosis plays an important role in ecosystem functioning, particularly in fragile environments. Little is known, however, about how AM fungus community composition responds to slope aspect. Our objective was to compare the AM fungus communities between sunny and shady slopes and to detect factors that influenced the distributions of AM fungi in arid ecosystems of the Daqingshan Mountains, Inner Mongolia, North China. AM fungus communities were evaluated based on small subunit ribosomal RNA genes (SSUs) using Illumina MiSeq sequencing. AM fungus community composition differed significantly between slope aspects, and sunny slopes had significantly higher AM fungus diversity and richness as well as spore density, total root colonization, arbuscule abundance, vesicle abundance, and hyphal colonization than shady slopes. Structural equation modeling (SEM) illustrated that the effects of slope aspect on AM fungus richness likely were mediated by available phosphorus, soil organic carbon, plant cover, and plant diversity. Available phosphorus was the principal factor that influenced AM fungus species richness, and soil organic carbon was the principal factor influencing spore density and total root colonization, suggesting that these factors especially might be responsible for differences between the AM fungus communities of different slope aspects. These findings elucidate the influence of slope aspect on AM fungus communities and may inform use of AM fungi in protection and restoration of vegetation with different slope aspects in arid ecosystems.

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References

  • Alguacil M, Torres M, Torrecillas E, Díaz G, Roldán A (2011) Plant type differently promote the arbuscular mycorrhizal fungi biodiversity in the rhizosphere after revegetation of a degraded, semiarid land. Soil Biol Biochem 43:167–173

    Article  CAS  Google Scholar 

  • Antoninka A, Reich PB, Johnson NC (2011) Seven years of carbon dioxide enrichment, nitrogen fertilization and plant diversity influence arbuscular mycorrhizal fungi in a grassland ecosystem. New Phytol 192:200–214

    Article  PubMed  Google Scholar 

  • Bai SL, Li GL, Liu Y, Kasten Dumroese R, Lv RH (2009) Ostryopsis davidiana seedlings inoculated with ectomycorrhizal fungi facilitate formation of mycorrhizae on Pinus tabulaeformis seedlings. Mycorrhiza 19:425–434

    Article  PubMed  Google Scholar 

  • Bai SL, Liu Y, Zhou J (2006) Resources investigation and ecological study on ectomycorrhizal fungi in Daqingshan Mountains, Inner Mongolia. Acta Ecol Sin 26:837–841

    CAS  Google Scholar 

  • Bai SL, Yan W, Hu YJ (2011) Mycorrhizal studies and resources investigation on ectomycorrhizal fungi in Daqingshan Mountains, Inner Mongolia. Inner Mongolian People’s Publishing House, Huhhot

    Google Scholar 

  • Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro-Fernández C, Lopéz-García A, Estrada B, Azcón R, Ferrol N, Azcón-Aguilar C (2011) Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J Arid Environ 75:1292–1301

    Article  Google Scholar 

  • Becklin KM, Pallo ML, Galen C (2011) Willows indirectly reduce arbuscular mycorrhizal fungal colonization in understorey communities. J Ecol 100:343–351

    Article  Google Scholar 

  • Begum F, Bajracharya RM, Sitaula BK, Sharma S (2013) Seasonal dynamics, slope aspect and land use effects on soil mesofauna density in the mid-hills of Nepal. Int J Biodivers Sci Ecosyst Serv Manag 9:290–297

    Article  Google Scholar 

  • Bennett AE, Bever JD (2009) Trade-offs between arbuscular mycorrhizal fungal competitive ability and host growth promotion in Plantago lanceolata. Oecologia 160:807–816

    Article  PubMed  Google Scholar 

  • Bonfim JA, Vasconcellos RLF, Gumiere T, Mescolotti DDLC, Oehl F, Cardoso EJBN (2016) Diversity of arbuscular mycorrhizal fungi in a Brazilian Atlantic forest toposequence. Microb Ecol 71:164–177

    Article  PubMed  Google Scholar 

  • Brenda B, Linderman RG (1983) Use of vesicular arbuscular mycorrhizal roots, intraradical vesicles and extraradical vesicles as inoculum. New Phytol 95:97–105

    Article  Google Scholar 

  • Brundrett MC, Ashwath N (2013) Glomeromycotan mycorrhizal fungi from tropical Australia III. Measuring diversity in natural and disturbed habitats. Plant Soil 370:419–433

    Article  CAS  Google Scholar 

  • Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Change Biol 20:3646–3659

    Article  Google Scholar 

  • Caravaca F, Alguacil M, Barea J, Roldán A (2005) Survival of inocula and native AM fungi species associated with shrubs in a degraded Mediterranean ecosystem. Soil Biol Biochem 37:227–233

    Article  CAS  Google Scholar 

  • Caravaca F, Alguacil M, Figueroa D, Barea J, Roldán A (2003) Re-establishment of Retama sphaerocarpa as a target species for reclamation of soil physical and biological properties in a semi-arid Mediterranean area. For Ecol Manag 182:49–58

    Article  Google Scholar 

  • Caravaca F, Barea J, Figueroa D, Roldan A (2002) Assessing the effectiveness of mycorrhizal inoculation and soil compost addition for enhancing reafforestation with Olea europaea subsp. sylvestris through changes in soil biological and physical parameters. Appl Soil Ecol 20:107–118

    Article  Google Scholar 

  • Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491

    Article  CAS  PubMed  Google Scholar 

  • Chu HY, Xiang XJ, Yang J, Adams JM, Zhang KP, Li YT, Shi Y (2016) Effects of slope aspects on soil bacterial and arbuscular fungal communities in a boreal forest in China. Pedosphere 26:226–234

    Article  Google Scholar 

  • Cornfield A (1960) Ammonia released on treating soils with N sodium hydroxide as a possible means of predicting the nitrogen-supplying power of soils. Nature 187:260–261

    Article  CAS  Google Scholar 

  • Cui XC, Hu JL, Wang JH, Yang JS, Lin XG (2016) Reclamation negatively influences arbuscular mycorrhizal fungal community structure and diversity in coastal saline-alkaline land in eastern China as revealed by Illumina sequencing. Appl Soil Ecol 98:140–149

    Article  Google Scholar 

  • da Silva IR, de Mello CMA, Neto RAF, da Silva DKA, de Melo AL, Oehl F, Maia LC (2014) Diversity of arbuscular mycorrhizal fungi along an environmental gradient in the Brazilian semiarid. Appl Soil Ecol 84:166–175

    Article  Google Scholar 

  • Du Toit M, Du Toit SHC, Hawkins DM (2001) Interactive LISREL: user’s guide. Scientific Software International

  • Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345

    Article  PubMed  Google Scholar 

  • Eisenhauer N, Bowker MA, Grace JB, Powell JR (2015) From patterns to causal understanding: structural equation modeling (SEM) in soil ecology. Pedobiologia 58:65–72

    Article  Google Scholar 

  • Gai JP, Tian H, Yang FY, Christie P, Li XL, Klironomos JN (2012) Arbuscular mycorrhizal fungal diversity along a Tibetan elevation gradient. Pedobiologia 55:145–151

    Article  Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Article  Google Scholar 

  • Graf F, Frei M (2013) Soil aggregate stability related to soil density, root length, and mycorrhiza using site-specific Alnus incana and Melanogaster variegatus s.L. Ecol Eng 57:314–323

    Article  Google Scholar 

  • Hao XL, Jiang R, Chen T (2011) Clustering 16S rRNA for OTU prediction: a method of unsupervised Bayesian clustering. Bioinformatics 27:611–618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiiesalu I, Pärtel M, Davison J, Gerhold P, Metsis M, Moora M, Öpik M, Vasar M, Zobel M, Wilson SD (2014) Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytol 203:233–244

    Article  CAS  PubMed  Google Scholar 

  • Hooper D, Coughlan J, Mullen M (2008) Structural equation modelling: guidelines for determining model fit. Electron J Bus Res Methods 6:53–60

    Google Scholar 

  • Jünemann S, Sedlazeck FJ, Prior K, Albersmeier A, John U, Kalinowski J, Mellmann A, Goesmann A, von Haeseler A, Stoye J (2013) Updating benchtop sequencing performance comparison. Nat Biotechnol 31:294–296

    Article  PubMed  Google Scholar 

  • Kutiel P (1992) Slope aspect effect on soil and vegetation in a Mediterranean ecosystem. Isr J Bot 41:243–250

    Google Scholar 

  • Laliberté E, Grace JB, Huston MA, Lambers H, Teste FP, Turner BL, Wardle DA (2013) How does pedogenesis drive plant diversity? Trends Ecol Evol 28:331–340

    Article  PubMed  Google Scholar 

  • Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:1424–1433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XL, George E, Marschner H (1991) Phosphorus depletion and pH decrease at the root-soil and hyphae-soil interfaces of VA mycorrhizal white clover fertilized with ammonium. New Phytol 119:397–404

    Article  CAS  Google Scholar 

  • Lin XG, Feng YZ, Zhang HY, Chen RR, Wang JH, Zhang JB, Chu HY (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environ Sci Technol 46:5764–5771

    Article  CAS  PubMed  Google Scholar 

  • Liu YJ, He JX, Shi GX, An LZ, Öpik M, Feng HY (2011) Diverse communities of arbuscular mycorrhizal fungi inhabit sites with very high altitude in Tibet Plateau. FEMS Microbiol Ecol 78:355–365

    Article  CAS  PubMed  Google Scholar 

  • Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12:2165–2179

    CAS  PubMed  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahé F, Mayor J, Bunge J, Chi J, Siemensmeyer T, Stoeck T, Wahl B, Paprotka T, Filker S, Dunthorn M (2014) Comparing high-throughput platforms for sequencing the V4 region of SSU-rDNA in environmental microbial eukaryotic diversity surveys. J Eukaryot Microbiol 62:338–345

    Article  PubMed  Google Scholar 

  • Mao L, Liu YJ, Shi GX, Jiang SJ, Cheng G, Li XM, An LZ, Feng HY (2014) Wheat cultivars form distinctive communities of root-associated arbuscular mycorrhiza in a conventional agroecosystem. Plant Soil 374:949–961

    Article  CAS  Google Scholar 

  • Martínez-García LB, Armas C, Miranda JDD, Padilla FM, Pugnaire FI (2011) Shrubs influence arbuscular mycorrhizal fungi communities in a semi-arid environment. Soil Biol Biochem 43:682–689

    Article  Google Scholar 

  • McGonigle T, Miller M, Evans D, Fairchild G, Swan J (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Nadal-Romero E, Petrlic K, Verachtert E, Bochet E, Poesen J (2014) Effects of slope angle and aspect on plant cover and species richness in a humid Mediterranean badland. Earth Surf Process Landf 39:1705–1716

    Article  Google Scholar 

  • Nelson D, Sommers L (1982) Total carbon, organic carbon, and organic matter. In: Page A (ed) Methods of soil analysis. Part 2. Chemical and microbiological properties. pp 539–579

  • Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M, Sieverding E (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42:724–738

    Article  CAS  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community Ecology Package 10

  • Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department of Agriculture, Washington

    Google Scholar 

  • Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij J, Reier Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241

    Article  PubMed  Google Scholar 

  • Öpik M, Zobel M, Cantero JJ, Davison J, Facelli JM, Hiiesalu I, Jairus T, Kalwij JM, Koorem K, Leal ME (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430

    Article  PubMed  Google Scholar 

  • Sato K, Suyama Y, Saito M, Sugawara K (2005) A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassl Sci 51:179–181

    Article  CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt EL, Belser L, Page A, Miller R, Keeney D (1982) Methods of soil analysis, Part 2, chemical and microbiological properties. In: Methods of soil analysis: Part 2: Chemical and microbiological properties

  • Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Senés-Guerrero C, Torres-Cortés G, Pfeiffer S, Rojas M, Schüßler A (2014) Potato-associated arbuscular mycorrhizal fungal communities in the Peruvian Andes. Mycorrhiza 24:405–417

    Article  PubMed  Google Scholar 

  • Sidari M, Ronzello G, Vecchio G, Muscolo A (2008) Influence of slope aspects on soil chemical and biochemical properties in a Pinus laricio forest ecosystem of Aspromonte (southern Italy). Eur J Soil Biol 44:364–372

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic press, New York

    Google Scholar 

  • Torrecillas E, del Mar AM, Roldán A (2012) Differences in the AMF diversity in soil and roots between two annual and perennial gramineous plants co-occurring in a Mediterranean, semiarid degraded area. Plant Soil 354:97–106

    Article  CAS  Google Scholar 

  • Tyndall RW (2005) Twelve years of herbaceous vegetation change in oak savanna habitat on a Maryland serpentine barren after Virginia Pine removal. Castanea 70:287–297

    Article  Google Scholar 

  • Van Der Heijden MG, Streitwolf-Engel R, Riedl R, Siegrist S, Neudecker A, Ineichen K, Boller T, Wiemken A, Sanders IR (2006) The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol 172:739–752

    Article  PubMed  Google Scholar 

  • Van Geel M, Busschaert P, Honnay O, Lievens B (2014) Evaluation of six primer pairs targeting the nuclear rRNA operon for characterization of arbuscular mycorrhizal fungal (AMF) communities using 454 pyrosequencing. J Microbiol Methods 106:93–100

    Article  CAS  PubMed  Google Scholar 

  • Veresoglou SD, Rillig MC (2014) Do closely related plants host similar arbuscular mycorrhizal fungal communities? A meta-analysis. Plant Soil 377:395–406

    Article  CAS  Google Scholar 

  • Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562

    Article  PubMed  Google Scholar 

  • Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils-effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–264

    Article  CAS  Google Scholar 

  • Wilson H, Johnson BR, Bohannan B, Pfeifer-Meister L, Mueller R, Bridgham SD (2016) Experimental warming decreases arbuscular mycorrhizal fungal colonization in prairie plants along a Mediterranean climate gradient. Peer J 4:e2083

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu QS, He XH, Zou YN, He KP, Sun YH, Cao MQ (2012) Spatial distribution of glomalin-related soil protein and its relationships with root mycorrhization, soil aggregates, carbohydrates, activity of protease and β-glucosidase in the rhizosphere of Citrus unshiu. Soil Biol Biochem 45:181–183

    Article  CAS  Google Scholar 

  • Xiang D, Verbruggen E, Hu YJ, Veresoglou SD, Rillig MC, Zhou WP, Xu TL, Li H, Hao ZP, Chen YL (2014) Land use influences arbuscular mycorrhizal fungal communities in the farming-pastoral ecotone of northern China. New Phytol 204:968–978

    Article  CAS  PubMed  Google Scholar 

  • Yang GW, Liu N, Lu WJ, Wang S, Kan HM, Zhang YJ, Xu L, Chen YL (2014) The interaction between arbuscular mycorrhizal fungi and soil phosphorus availability influences plant community productivity and ecosystem stability. J Ecol 102:1072–1082

    Article  CAS  Google Scholar 

  • Yang HS, Zang YY, Yuan YG, Tang JJ, Chen X (2012) Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evol Biol 12:1–13

    Article  Google Scholar 

  • Zangaro W, Rostirola LV, Souza PBD, Alves RDA, Rondina ABL, Nogueira MA, Carrenho R (2012) Root colonization and spore abundance of arbuscular mycorrhizal fungi in distinct successional stages from an Atlantic rainforest biome in southern Brazil. Mycorrhiza 23:221–233

    Article  PubMed  Google Scholar 

  • Zheng Y, Kim YC, Tian XF, Chen L, Yang W, Gao C, Song MH, Xu XL, Guo LD (2014) Differential responses of arbuscular mycorrhizal fungi to nitrogen addition in a near pristine Tibetan alpine meadow. FEMS Microbiol Ecol 89:594–605

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31360125), the Scientific Innovation Team of Inner Mongolia Agricultural University (No. NDDYTD 2013-7), and the Natural Science Foundation of Inner Mongolia (No. 2016MS0343).

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Correspondence to Shulan Bai.

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Min Liu and Rong Zheng contributed equally to this work.

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Liu, M., Zheng, R., Bai, S. et al. Slope aspect influences arbuscular mycorrhizal fungus communities in arid ecosystems of the Daqingshan Mountains, Inner Mongolia, North China. Mycorrhiza 27, 189–200 (2017). https://doi.org/10.1007/s00572-016-0739-7

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