Impact of 36 years of nitrogen fertilization on microbial community composition and soil carbon cycling-related enzyme activities in rhizospheres and bulk soils in northeast China

Wang, Q.; Ma, Mingchao; Jiang, X.; Guan, D.; Wei, D.; Zhao, B.; Chen, S.; Cao, F.; Li, L.; Yang, X.; Li, J.

doi:10.1016/j.apsoil.2018.12.019

Article (Scientific journals)

Impact of 36 years of nitrogen fertilization on microbial community composition and soil carbon cycling-related enzyme activities in rhizospheres and bulk soils in northeast China

Wang, Q.; Ma, Mingchao; Jiang, X. et al.

2019 • In Applied Soil Ecology, 136, p. 148-157

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/266307

DOI
10.1016/j.apsoil.2018.12.019

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

1-s2.0-S0929139318303640-main.pdf

Publisher postprint (1.2 MB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Black soil; Decomposition; Enzyme activities; Nitrogen fertilization; Rhizosphere

Abstract :

[en] Nitrogen (N) deposition can change ecosystem functions but little is known of long-term N-deposition and rhizosphere effects on the microbial community composition and enzymes activities related to the carbon (C) cycle in the black soil common to northeastern China. Here, we studied two enzyme activities involved in C cycles and microbial community composition in both the rhizosphere and bulk soil from a long-term (36-year) fertilization field experiment. N-addition significantly decreased bacterial abundance and phenol oxidase activity, but enhanced fungal abundance and peroxidase activity, in both the rhizosphere and bulk soil. The fungal diversity exhibited more obvious shifts than the bacterial diversity after long-term N-addition, resulting in significantly decreased bacterial and fungal diversity levels, except for bacterial diversity in the rhizosphere, which was not significantly changed. Moreover, the enzyme activities and the bacterial and fungal abundance levels were higher in the rhizosphere than in the bulk soil, suggesting a rhizosphere effect on microbial activities involved in the C cycle. There was a significant difference in the microbial community compositions among different N-addition levels. A lesser β-diversity response to N-addition was observed in the rhizosphere than in the bulk soil, and the responses of fungal communities were greater than those of bacterial communities. Our findings suggested that rhizosphere effects and fertilization regimes both have significant influences on microbial communities and soil enzyme activities, and that fungi were more sensitive than bacteria in responding to N-deposition. © 2018

Disciplines :

Microbiology

Author, co-author :

Wang, Q.; Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China, College of Biological Sciences, China Agricultural University, Beijing, 100094, China

Ma, Mingchao ; Université de Liège - ULiège

Jiang, X.; Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China, Laboratory of Quality & Safety Risk Assessment for Microbial Products (Beijing), Ministry of Agriculture, Beijing, 100081, China

Guan, D.; Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

Wei, D.; The Institute of Soil Fertility and Environmental Sources, Heilongjiang Academy of Agricultural Sciences, Harbin, 150086, China

Zhao, B.; Laboratory of Quality & Safety Risk Assessment for Microbial Products (Beijing), Ministry of Agriculture, Beijing, 100081, China

Chen, S.; College of Biological Sciences, China Agricultural University, Beijing, 100094, China

Cao, F.; Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China, Laboratory of Quality & Safety Risk Assessment for Microbial Products (Beijing), Ministry of Agriculture, Beijing, 100081, China

Li, L.; Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

Yang, X.; Laboratory of Quality & Safety Risk Assessment for Microbial Products (Beijing), Ministry of Agriculture, Beijing, 100081, China

Li, J.; Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, 100081, China, Laboratory of Quality & Safety Risk Assessment for Microbial Products (Beijing), Ministry of Agriculture, Beijing, 100081, China

Language :

English

Title :

Impact of 36 years of nitrogen fertilization on microbial community composition and soil carbon cycling-related enzyme activities in rhizospheres and bulk soils in northeast China

Publication date :

2019

Journal title :

Applied Soil Ecology

ISSN :

0929-1393

Publisher :

Elsevier, Netherlands

Volume :

136

Pages :

148-157

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 21 December 2021

Statistics

Number of views

41 (2 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Abarenkov, K., Henrik Nilsson, R., Larsson, K.H., Alexander, I.J., Eberhardt, U., Erland, S., Høiland, K., Kjøller, R., Larsson, E., Pennanen, T., Sen, R., Taylor, A.F., Tedersoo, L., Ursing, B.M., Vrålstad, T., Liimatainen, K., Peintner, U., Koljalg, U., The UNITE database for molecular identification of fungierecent updates and future perspectives. New Phytol. 186 (2010), 281–285.
Ai, C., Liang, G., Sun, J., Wang, X., He, P., Zhou, W., Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvo-aquic soil. Soil Biol. Biochem. 57 (2013), 30–42.
Ai, C., Liang, G., Sun, J., Wang, X., He, P., Zhou, W., He, X., Reduced dependence of rhizosphere microbiome on plant-derived carbon in 32-year long-term inorganic and organic fertilized soils. Soil Biol. Biochem. 80 (2015), 70–78.
Allison, S.D., Czimczik, C.I., Treseder, K.K., Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Global Change Biol. 14 (2008), 1156–1168.
Bååth, E., Anderson, T.H., Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol. Biochem. 35 (2003), 955–963.
Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., Vivanco, J.M., The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57 (2006), 233–266.
Baldrian, P., Distribution of extracellular enzymes in soils: spatial heterogeneity and determining factors at various scales. Soil Sci. Soc. Am. J. 78 (2014), 11–18.
Bardgett, R.D., Freeman, C., Ostle, N.J., Microbial contributions to climate change through carbon cycle feedbacks. ISME J. 2 (2008), 805–814.
Beare, M.H., Parmelee, R.W., Hendrix, P.F., Cheng, W., Coleman, D.C., Crossley, D.A., Microbial and faunal interactions and effects on litter nitrogen and decomposition in agroecosystems. Ecol. Monogr. 62 (1992), 569–591.
Blaalid, R., Kumar, S., Nilsson, R.H., Abarenkov, K., Kirk, P.M., Kauserud, H., ITS1 versus ITS2 as DNA metabarcodes for fungi. Mol. Ecol. Resour. 13 (2013), 218–224.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7 (2010), 335–336.
Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., Fierer, N., Knight, R., Global patterns of 16S rRNA diversity at a depth of millions of sequences per samplem. PNAS 108 (2011), 4516–4522.
Carreiro, M.M., Sinsabaugh, R.L., Repert, D.A., Parkhurst, D.F., Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81 (2000), 2359–2365.
Cheng, W., Johnson, D.W., Fu, S., Rhizosphere effects on decomposition. Soil Sci. Soc. Am. J. 67 (2003), 1418–1427.
Cline, L.C., Zak, D.R., Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology 96 (2015), 3374–3385.
Craine, J.M., Morrow, C., Fierer, N., Microbial nitrogen limitation increases decomposition. Ecology 88 (2007), 2105–2113.
De Vries, F.T., Hoffland, E., van Eekeren, N., Brussard, L., Bloem, J., Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol. Biochem. 38 (2006), 2092–2103.
Dean, S.L., Farrer, E.C., Lee, T.D., Andrea, P.A., Suding, K.N., Sinsabaugh, R.L., Nitrogen deposition alters plant-fungal relationships: linking belowground dynamics to aboveground vegetation change. Mol. Ecol. 23 (2014), 1364–1378.
Denef, K., Roobroeck, D., Wadu, M.C.M., Lootens, P., Boeckx, P., Microbial community composition and rhizodeposit-carbon assimilation in differently managed temperate grassland soils. Soil Biol. Biochem. 41 (2009), 144–153.
Ding, J., Jiang, X., Ma, M., Zhou, B., Guan, D., Zhao, B., Zhou, J., Cao, F., Li, L., Li, J., Effect of 35 years inorganic fertilizer and manure amendment on structure of bacterial and archaeal communities in black soil of northeast China. Appl. Soil Ecol. 105 (2016), 187–195.
Edgar, R.C., UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10 (2013), 996–998.
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 (2011), 2194–2200.
Fierer, N., Strickland, M.S., Liptzin, D., Bradford, M.A., Cleveland, C.C., Global patterns in belowground communities. Ecol. Lett. 12 (2009), 1238–1249.
Fierer, N., Lauber, C.L., Ramirez, K.S., Zaneveld, J., Bradford, M.A., Knight, R., Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J. 6 (2012), 1007–1017.
Fowler, D., Sutton, M.A., The global nitrogen cycle in the twenty-first century: introduction. Philos. Trans. R. Soc. B Biol. Sci., 368, 2013, 20130165.
Frey, S.D., Elliott, E.T., Paustian, K., Bacterial and fungal abundance and biomass in conventional and no-tillage agroecosystems along two climatic gradients. Soil Biol. Biochem. 31 (1999), 573–585.
Galloway, J.N., Townsend, A.R., Erisman, J.W., Bekunda, M., Cai, Z., Freney, J.R., Martinelli, L.A., Seitzinger, S.P., Sutton, M.A., Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320 (2008), 889–892.
Garbeva, P., Silby, M.W., Raaijmakers, J.M., Levy, S.B., Wd, B., Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors. ISME J. 5 (2011), 973–985.
Geiser, D.M., Gueidan, C., Miadlikowska, J., Lutzoni, F., Kauff, F., Hofstetter, V., Fraker, E., Schoch, C.L., Tibell, L., Untereiner, W.A., Eurotiomycetes: eurotiomycetidae and chaetothyriomycetidae. Mycologia 98 (2006), 1053–1064.
Ghannoum, M.A., Jurevic, R.J., Mukherjee, P.K., Cui, F., Sikaroodi, M., Naqvi, A., Gillevet, P.M., Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog., 6, 2010, e1000713.
Giagnoni, L., Pastorelli, R., Mocali, S., Arenella, M., Nannipieri, P., Renella, G., Availability of different nitrogen forms changes the microbial communities and enzyme activities in the rhizosphere of maize lines with different nitrogen use efficiency. Appl. Soil Ecol. 98 (2015), 30–38.
Guo, J.H., Liu, X.J., Zhang, Y., Shen, J.L., Han, W.X., Zhang, W.F., Christie, P., Goulding, K.W., Vitousek, P.M., Zhang, F.S., Significant acidification in major Chinese croplands. Science 327 (2010), 1008–1010.
Helmke, P.A., Sparks, D.L., Sparks, D.L., Page, A.L., Helmke, P.A., Loeppert, R.H., Soltanpour, P.N., Tabatabai, M.A., Johnston, C.T., Sumner, M.E., Lithium, sodium, potassium, rubidium, and cesium. methods of soil analysis part 3—chemical. Methods, 1996, 551–574.
Houbraken, J., Samson, R.A., Phylogeny of Penicillium and the segregation of Trichocomaceae into three families. Stud. Mycol. 70 (2011), 1–51.
Jian, S., Li, J., Chen, J., Wang, G., Mayes, M.A., Dzantor, K.E., Hui, D., Luo, Y., Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: a meta-analysis. Soil Biol. Biochem. 101 (2016), 32–43.
Keiblinger, K.M., Schneider, T., Roschitzki, B., Schmid, E., Eberl, L., Hämmerle, I., Leitner, S., Richter, A., Wanek, W., Riedel, K., Zechmeister-Boltenstern, S., Effects of stoichiometry and temperature perturbations on beech leaf litter decomposition, enzyme activities and protein expression. Biogeosciences 9 (2012), 4537–4551.
Lauber, C.L., Strickland, M.S., Bradford, M.A., Fierer, N., The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol. Biochem. 40 (2008), 2407–2415.
Lebeis, S.L., Paredes, S.H., Lundberg, D.S., Breakfield, N., Gehring, J., Mcdonald, M., Malfatti, S., Glavina del Rio, T., Jones, C.D., Tringe, S.G., PLANT MICROBIOME. salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349 (2015), 860–864.
Li, X., Deng, Y., Li, Q., Lu, C., Wang, J., Zhang, H., Zhu, J., Zhou, J., He, Z., Shifts of functional gene representation in wheat rhizosphere microbial communities under elevated ozone. ISME J. 7 (2013), 660–671.
Li, J., Ziegler, S.E., Lane, C.S., Billings, S.A., Legacies of native climate regime govern responses of boreal soil microbes to litter stoichiometry and temperature. Soil Biol. Biochem. 66 (2013), 204–213.
Liljeroth, E., Bååth, E., Mathiasson, I., Lundborg, T., Root exudation and rhizoplane bacterial abundance of barley (Hordeum vulgare L.) in relation to nitrogen fertilization and root growth. Plant Soil 127 (1990), 81–89.
Luis, P., Walther, G., Kellner, H., Martin, F., Buscot, F., Diversity of laccase genes from basidiomycetes in a forest soil. Soil Biol. Biochem. 36 (2004), 1025–1036.
Ma, A., Zhuang, X., Wu, J., Cui, M., Lv, D., Liu, C., Zhuang, G., Ascomycota members dominate fungal communities during straw residue decomposition in arable soil. PLoS One, 8, 2013, e66146.
Mack, M.C., Schuur, E.A., Bretharte, M.S., Shaver, G.R., Chapin, F.S., Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431 (2004), 440–443.
Magoč T., Salzberg, S.L., FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27 (2011), 2957–2963.
Meier, I.C., Pritchard, S.G., Brzostek, E.R., Mccormack, M.L., Phillips, R.P., The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO 2 . New Phytol. 205 (2015), 1164–1174.
Melillo, J.M., Aber, J.D., Muratore, J.F., Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63 (1982), 621–626.
Miura, T., Niswati, A., Swibawa, I.G., Haryani, S., Gunito, H., Shimano, S., Fujie, K., Kaneko, N., Diversity of fungi on decomposing leaf litter in a sugarcane plantation and their response to tillage practice and bagasse mulching: implications for management effects on litter decomposition. Microb. Ecol. 70 (2015), 646–658.
Olsen, S.R., Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate, 1954, United States Department Of Agriculture, 1–19.
Patra, A.K., Abbadie, L., Clays-Josserand, A., Degrange, V., Grayston, S.J., Loiseau, P., Mahmood, S., Nazaret, S., Philippot, L., Poly, F., Prosser, J.I., Richaume, A., Le Roux, X., Effects of grazing on microbial functional groups involved in soil N dynamics. Ecol. Monogr. 75 (2005), 65–80.
Paungfoo-Lonhienne, C., Yeoh, Y.K., Kasinadhuni, N.R., Lonhienne, T.G., Robinson, N., Hugenholtz, P., Ragan, M.A., Schmidt, S., Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere. Sci. Rep., 5, 2015, 8678.
Peiffer, J.A., Spor, A., Koren, O., Jin, Z., Tringe, S.G., Dangl, J.L., Buckler, E.S., Ley, R.E., Diversity and heritability of the maize rhizosphere microbiome under field conditions. PNAS 110 (2013), 6548–6553.
Phillips, R.P., Fahey, T.J., Fertilization effects on fineroot biomass, rhizosphere microbes and respiratory fluxes in hardwood forest soils. New Phytol. 176 (2007), 655–664.
Phillips, R.P., Finzi, A.C., Bernhardt, E.S., Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO 2 fumigation. Ecol. Lett. 14 (2011), 187–194.
Phoenix, G.K., Emmett, B.A., Britton, A.J., Caporn, S.J.M., Dise, N.B., Helliwell, R., Jones, L., Leake, J.R., Leith, I.D., Sheppard, L.J., Impacts of atmospheric nitrogen deposition: responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments. Global Change Biol. 18 (2012), 1197–1215.
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. Mol. Ecol. 25 (2016), 4059–4074.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41 (2013), 590–596.
Rabinovich, M.L., Bolobova, A.V., Vasil'Chenko, L.G., Fungal decomposition of natural aromatic structures and xenobiotics: a review. Appl. Biochem. Microbiol. 40 (2004), 1–17.
Ramirez, K.S., Craine, J.M., Noah, F., Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Global Change Biol. 18 (2012), 1918–1927.
Rousk, J., Frey, S.D., Revisiting the hypothesis that fungal-to-bacterial dominance characterizes turnover of soil organic matter and nutrients. Ecol. Monogr. 85 (2015), 457–472.
Saito, T., Hong, P., Kato, K., Okazaki, M., Inagaki, H., Maeda, S., Yokogawa, Y., Purification and characterization of an extracellular laccase of a fungus (family Chaetomiaceae) isolated from soil. Enzyme Microb. Technol. 33 (2003), 520–526.
Saiya-Cork, K.R., Sinsabaugh, R.L., Zak, D.R., The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol. Biochem. 34 (2002), 1309–1315.
Schneider, T., Keiblinger, K.M., Schmid, E., Sterflinger-Gleixner, K., Ellersdorfer, G., Roschitzki, B., Richter, A., Eberl, L., Zechmeister-Boltenstern, S., Riedel, K., Who is who in litter decomposition? metaproteomics reveals major microbial players and their biogeochemical functions. ISME J. 6 (2012), 1749–1762.
Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., Chen, W., Consortium, F.B., Bolchacova, E., Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS 109 (2012), 6241–6246.
Shrestha, M., Shrestha, P.M., Frenzel, P., Conrad, R., Effect of nitrogen fertilization on methane oxidation, abundance, community structure, and gene expression of methanotrophs in the rice rhizosphere. ISME J. 4 (2010), 1545–1556.
Sinsabaugh, R.S., Enzymic analysis of microbial pattern and process. Biol. Fertil. Soils 17 (1994), 69–74.
Sinsabaugh, R.L., Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol. Biochem. 42 (2010), 391–404.
Sinsabaugh, R.L., Lauber, C.L., Weintraub, M.N., Ahmed, B., Allison, S.D., Crenshaw, C., Contosta, A.R., Cusack, D., Frey, S., Gallo, M.E., Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 11 (2008), 1252–1264.
Sinsabaugh, R.L., Moorhead, D.L., Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol. Biochem. 26 (1994), 1305–1311.
Sterner, R.W., Elser, J.J., Ecological Stoichiometry: The Biology of Elements From Molecules to The Biosphere. 2002, Princeton University Press.
Strickland, T.C., Sollins, P., Improved method for separating light- and heavy-fraction organic material from soil. Soil Sci. Soc. Am. J. 51 (1987), 1390–1393.
Sun, R., Dsouza, M., Gilbert, J.A., Guo, X., Wang, D., Guo, Z., Ni, Y., Chu, H., Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environ. Microbiol. 18 (2016), 5137–5150.
Treseder, K.K., Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol. Lett. 11 (2008), 1111–1120.
Turner, S.M., Newman, E.I., Growth of bacteria on roots of grasses: influence of mineral nutrient supply and interactions between species. J. Gen. Microbiol. 130 (1984), 505–512.
Tyc, O., Berg, M.V.D., Gerards, S., Veen, J.A.V., Raaijmakers, J.M., Boer, W.D., Garbeva, P., Impact of interspecific interactions on antimicrobial activity among soil bacteria. Front. Microbiol. 5 (2014), 262–265.
Vitousek, P.M., Aber, J.D., Howarth, R.W., Schlesinger, W.H., Vitousek, P.M., Aber, J.D., Likens, G.E., Matson, P.A., Schindler, D.W., Tilman, D.G., Human alteration of the global nitrogen cycle: sources and consequences. Ecol. Appl. 7 (1997), 737–750.
Waldrop, M.P., Zak, D.R., Sinsabaugh, R.L., Gallo, M., Lauber, C., Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol. Appl. 14 (2004), 1172–1177.
Wang, L., Feng, Y., Tian, J., Xiang, M., Sun, J., Ding, J., Yin, W., Stadler, M., Che, Y., Liu, X., Farming of a defensive fungal mutualist by an attelabid weevil. ISME J. 9 (2015), 1793–1801.
Wei, D., Yang, Q., Zhang, J.Z., Wang, S., Chen, X.L., Zhang, X.L., Wei-Qun, L.I., Bacterial community structure and diversity in a black soil as affected by long-term fertilization. Pedosphere 18 (2008), 582–592.
Wurzbacher, C., Rösel, S., Rychła, A., Grossart, H.P., Importance of saprotrophic freshwater fungi for pollen degradation. PLoS One, 9, 2014, e94643.
Xiong, X., Grunwald, S., Myers, D.B., et al. Interaction effects of climate and land use/land cover change on soil organic carbon sequestration [J]. Sci. Total Environ. 493 (2014), 974–982.
Zámocký M., Tafer, H., Chovanová K., Lopandic, K., Kamlárová A., Obinger, C., Genome sequence of the filamentous soil fungus Chaetomium cochliodes reveals abundance of genes for heme enzymes from all peroxidase and catalase superfamilies. BMC Genomics, 17, 2016, 763.
Zeng, J., Liu, X., Song, L., Lin, X., Zhang, H., Shen, C., Chu, H., Nitrogen fertilization directly affects soil bacterial diversity and indirectly affects bacterial community composition. Soil Biol. Biochem. 92 (2016), 41–49.
Zhou, J., Guan, D., Zhou, B., Zhao, B., Ma, M., Qin, J., Jiang, X., Chen, S., Cao, F., Shen, D., Influence of 34-years of fertilization on bacterial communities in an intensively cultivated black soil in northeast China. Soil Biol. Biochem. 90 (2015), 42–51.
Zhou, J., Jiang, X., Zhou, B., Zhao, B., Ma, M., Guan, D., Li, J., Chen, S., Cao, F., Shen, D., Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biol. Biochem. 95 (2016), 135–143.
Zhu, S., Vivanco, J.M., Manter, D.K., Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl. Soil Ecol. 107 (2016), 324–333.