Skip to main content
SpringerLink
Log in

Microbial functions and soil nitrogen mineralisation processes in the soil of a cool temperate forest in northern Japan

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

There is little knowledge about microbial functional community structures and the relationships between microbial communities and nitrogen transformation processes. Here, we investigated the relationships between soil microbial communities and nitrogen mineralisation potentials in a cool temperate forest throughout the growing season. Microbial communities were assessed by quantification of the total bacterial, archaeal, and fungal gene abundances and the bacterial and archaeal amoA gene abundances, functional predictions of bacteria and fungi, and analysis of the bacterial-fungal co-occurrence network. In mid-summer, ectomycorrhizal fungal abundance was significantly higher, whereas the total bacterial abundance was significantly lower. Bacterial and archaeal amoA gene abundances were also significantly higher in mid-summer. However, regardless of the seasonal fluctuation of microbial gene abundances, the net nitrification and nitrogen mineralisation potential did not show clear seasonality. In the network analysis, the microbial community was divided into 13 modules, which were subgroups assumed to have similar niches. Furthermore, two modules that mainly consisted of microbial species of Proteobacteria and Bacteroidetes were significantly and positively correlated with the net nitrification and mineralisation potentials. Our results indicated that microbial subgroups sharing similar niches, instead of total microbial abundances and functional gene abundances, could be important factors affecting the net nitrogen mineralisation potential.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Availability of data and material

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Aber JD, Melillo JM, Nadelhoffer KJ, McClaugherty CA, Pastor J (1985) Fine root turnover in forest ecosystems in relation to quantity and form of nitrogen availability: a comparison of two methods. Oecologia 66:317–321

    Article  Google Scholar 

  • Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925

    Article  Google Scholar 

  • Assigbetse K, Gueye M, Thioulouse J, Duponnois R (2005) Soil bacterial diversity responses to root colonization by an ectomycorrhizal fungus are not root-growth-dependent. Microb Ecol 50:350–359

    Article  Google Scholar 

  • Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545

    Article  Google Scholar 

  • Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351

    Article  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. In: Proceedings of the Third International ICWSM Conference, pp 361–362

  • Bödeker ITM, Lindahl BD, Olson Å, Clemmensen KE (2016) Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct Ecol 30:1967–1978

    Article  Google Scholar 

  • Bottomley PJ, Taylor AE, Myrold DD (2012) A consideration of the relative contributions of different microbial subpopulations to the soil N cycle. Front Microbiol 3:373

    Article  Google Scholar 

  • Boyle SA, Yarwood RR, Bottomley PJ, Myrold DD (2008) Bacterial and fungal contributions to soil nitrogen cycling under Douglas fir and red alder at two sites in Oregon. Soil Biol Biochem 40:443–451

    Article  Google Scholar 

  • Brooks DD, Chan R, Starks ER, Grayston SJ, Jones MD (2011) Ectomycorrhizal hyphae structure components of the soil bacterial community for decreased phosphatase production. FEMS Microbiol Ecol 76:245–255

    Article  Google Scholar 

  • Caffrey JM, Bano N, Kalanetra K, Hollibaugh JT (2007) Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME J 1:660–662

    Article  Google Scholar 

  • Chao Y, Liu W, Chen Y, Chen W, Zhao L, Ding Q et al (2016) Structure, variation, and co-occurrence of soil microbial communities in abandoned sites of a rare earth elements mine. Environ Sci Technol 50:11481–11490

    Article  Google Scholar 

  • Clauset A, Newman MEJ, Moore C (2004) Finding community structure in very large networks. Phys Rev 70:066111

    Google Scholar 

  • Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O et al (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071

    Article  Google Scholar 

  • Costa E, Pérez J, Kreft JU (2006) Why is metabolic labour divided in nitrification? Trends Microbiol 14:213–219

    Article  Google Scholar 

  • de Menezes AB, Prendergast-Miller MT, Richardson AE, Toscas P, Farrell M, Macdonald LM et al (2015) Network analysis reveals that bacteria and fungi form modules that correlate independently with soil parameters. Environ Microbiol 17:2677–2689

    Article  Google Scholar 

  • Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinform 13:113

    Article  Google Scholar 

  • Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM et al (2020) PICRUSt2 for prediction of metagenome functions. Nat Biotechnol 38:685–688

    Article  Google Scholar 

  • Ekblad A, Wallander H, Godbold DL, Cruz C, Johnson D, Baldrian P et al (2013) The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant Soil 366:1–27

    Article  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  Google Scholar 

  • Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120

    Article  Google Scholar 

  • Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017

    Article  Google Scholar 

  • Fraterrigo JM, Balser TC, Turner MG (2006) Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 87:570–579

    Article  Google Scholar 

  • Frossard A, Gerull L, Mutz M, Gessner MO (2012) Disconnect of microbial structure and function: Enzyme activities and bacterial communities in nascent stream corridors. ISME J 6:680–691

    Article  Google Scholar 

  • Gessler A, Schneider S, Von Sengbusch D, Weber P, Hanemann U, Huber C et al (1998) Field and laboratory experiments on net uptake of nitrate and ammonium the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol 138:275–285

    Article  Google Scholar 

  • Großkopf R, Janssen PH, Liesack W (1998) Diversity and structure of the methanogenic community in anoxic rice paddy soil microcosms as examined by cultivation and direct 16S rRNA gene sequence retrieval. Appl Environ Microbiol 64:960–969

    Article  Google Scholar 

  • Gubry-Rangin C, Nicol GW, Prosser JI (2010) Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74:566–574

    Article  Google Scholar 

  • Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985

    Article  Google Scholar 

  • Högberg MN, Briones MJI, Keel SG, Metcalfe DB, Campbell C, Midwood AJ et al (2010) Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. New Phytol 187:485–493

    Article  Google Scholar 

  • Högberg MN, Högberg P, Myrold DD (2007) Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150:590–601

    Article  Google Scholar 

  • Huygens D, Díaz S, Urcelay C, Boeckx P (2016) Microbial recycling of dissolved organic matter confines plant nitrogen uptake to inorganic forms in a semi-arid ecosystem. Soil Biol Biochem 101:142–151

    Article  Google Scholar 

  • Isobe K, Ise Y, Kato H, Oda T, Vincenot CE, Koba K et al (2020) Consequences of microbial diversity in forest nitrogen cycling: diverse ammonifiers and specialized ammonia oxidizers. ISME J 14:12–25

    Article  Google Scholar 

  • Isobe K, Koba K, Otsuka S, Senoo K (2011) Nitrification and nitrifying microbial communities in forest soils. J for Res 16:351–362

    Article  Google Scholar 

  • Isobe K, Ohte N (2014) Ecological perspectives on microbes involved in N-cycling. Microbes Environ 29:4–16

    Article  Google Scholar 

  • Isobe K, Ohte N, Oda T, Murabayashi S, Wei W, Senoo K et al (2015) Microbial regulation of nitrogen dynamics along the hillslope of a natural forest. Front Environ Sci 2:63

    Article  Google Scholar 

  • Isobe K, Oka H, Watanabe T, Tateno R, Urakawa R, Liang C et al (2018) High soil microbial activity in the winter season enhances nitrogen cycling in a cool-temperate deciduous forest. Soil Biol Biochem 124:90–100

    Article  Google Scholar 

  • IUSS Working Group WRB (2015) International soil classification system for naming soils and creating legends for soil maps. World Reference Base for Soil Resources 2014, update 2015

  • Iwaoka C, Imada S, Taniguchi T, Du S, Yamanaka N, Tateno R (2018) The impacts of soil fertility and salinity on soil nitrogen dynamics mediated by the soil microbial community beneath the Halophytic Shrub Tamarisk. Microb Ecol 75:985–996

    Article  Google Scholar 

  • Jia Z, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671

    Article  Google Scholar 

  • Jones CM, Hallin S (2019) Geospatial variation in co-occurrence networks of nitrifying microbial guilds. Mol Ecol 28:293–306

    Article  Google Scholar 

  • Jung J, Yeom J, Kim J, Han J, Lim HS, Park H et al (2011) Change in gene abundance in the nitrogen biogeochemical cycle with temperature and nitrogen addition in Antarctic soils. Res Microbiol 162:1018–1026

    Article  Google Scholar 

  • Kaiser C, Fuchslueger L, Koranda M, Gorfer M, Stange CF, Kitzler B et al (2011) Plants control the seasonal dynamics of microbial N cycling in a beech forest soil by belowground C allocation. Ecology 92:1036–1051

    Article  Google Scholar 

  • Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J, Schweiger P et al (2010) Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol 187:843–858

    Article  Google Scholar 

  • Kang H, Gao H, Yu W, Yi Y, Wang Y, Ning M (2018) Changes in soil microbial community structure and function after afforestation depend on species and age: case study in a subtropical alluvial island. Sci Total Environ 625:1423–1432

    Article  Google Scholar 

  • Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–D462

    Article  Google Scholar 

  • Kersters K, DeVos P, Gills M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the proteobacteria. In: Dworkin M, Falkow S, Eosenberg E, Schleifer K-H, Stackbrandt E (eds) The prokaryotes. Springer, New York, pp 3–37

    Chapter  Google Scholar 

  • Kielak AM, Barreto CC, Kowalchuk GA, van Veen JA, Kuramae EE (2016) The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 7:744

    Article  Google Scholar 

  • Langfelder P, Horvath S (2007) Eigengene networks for studying the relationships between co-expression modules. BMC Syst Biol 1:54

    Article  Google Scholar 

  • Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559

    Article  Google Scholar 

  • Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA et al (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821

    Article  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  Google Scholar 

  • Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415

    Article  Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    Article  Google Scholar 

  • Lindahl BO, Taylor AFS, Finlay RD (2002) Defining nutritional constraints on carbon cycling in boreal forests-towards a less “phytocentric” perspective. Plant Soil 242:123–135

    Article  Google Scholar 

  • Lladó S, Žifčáková L, Větrovský T, Eichlerová I, Baldrian P (2016) Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision 1 for polysaccharide decomposition. Biol Fertil Soils 52:251–260

    Article  Google Scholar 

  • Matsuoka S, Sugiyama Y, Tateno R, Imamura S, Kawaguchi E, Osono T (2020) Evaluation of host effects on ectomycorrhizal fungal community compositions in a forested landscape in northern Japan. R Soc Open Sci 7:191952

    Article  Google Scholar 

  • Mendes LW, Kuramae EE, Navarrete AA, Van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–1587

    Article  Google Scholar 

  • Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55

    Article  Google Scholar 

  • Moore-Kucera J, Dick RP (2008) PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence. Microb Ecol 55:500–511

    Article  Google Scholar 

  • Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    Article  Google Scholar 

  • Nakayama M, Imamura S, Taniguchi T, Tateno R (2019) Does conversion from natural forest to plantation affect fungal and bacterial biodiversity, community structure, and co-occurrence networks in the organic horizon and mineral soil? For Ecol Manag 446:238–250

    Article  Google Scholar 

  • Nakayama M, Tateno R (2018) Solar radiation strongly influences the quantity of forest tree root exudates. Trees 32:871–879

    Article  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Newman MEJ (2006) Modularity and community structure in networks. Proc Natl Acad Sci USA 103:8577–8582

    Article  Google Scholar 

  • Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J et al (2016) FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248

    Article  Google Scholar 

  • Okano Y, Hristova KR, Leutenegger CM, Jackson LE, Denison RF, Gebreyesus B et al (2004) Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil. Appl Environ Microbiol 70:1008–1016

    Article  Google Scholar 

  • Osburn ED, Barrett JE (2020) Abundance and functional importance of complete ammonia-oxidizing bacteria (comammox) versus canonical nitrifiers in temperate forest soils. Soil Biol Biochem 145:107801

    Article  Google Scholar 

  • Osburn ED, Elliottt KJ, Knoepp JD, Miniat CF, Barrett JE (2018) Soil microbial response to Rhododendron understory removal in southern Appalachian forests: effects on extracellular enzymes. Soil Biol Biochem 127:50–59

    Article  Google Scholar 

  • Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974

    Article  Google Scholar 

  • Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL et al (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110:6548–6553

    Article  Google Scholar 

  • Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51

    Article  Google Scholar 

  • Pinnell LJ, Dunford E, Ronan P, Hausner M, Neufeld JD (2014) Recovering glycoside hydrolase genes from active tundra cellulolytic bacteria. Can J Microbiol 60:469–476

    Article  Google Scholar 

  • Prevost-Boure NC, Maron PA, Ranjard L, Nowak V, Dufrene E, Damesin C et al (2011) Seasonal dynamics of the bacterial community in forest soils under different quantities of leaf litter. Appl Soil Ecol 47:14–23

    Article  Google Scholar 

  • Purahong W, Krüger D, Buscot F, Wubet T (2016) Correlations between the composition of modular fungal communities and litter decomposition-associated ecosystem functions. Fungal Ecol 22:106–114

    Article  Google Scholar 

  • Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240

    Article  Google Scholar 

  • Reich PB, Grigal DF, Aber JD, Gower ST (1997) Nitrogen mineralization and productivity in 50 hardwood and conifer stands on diverse soils. Ecology 78:335–347

    Article  Google Scholar 

  • Ribbons RR, Levy-Booth DJ, Masse J, Grayston SJ, McDonald MA, Vesterdal L, Prescott CE (2016) Linking microbial communities, functional genes and nitrogen-cycling processes in forest floors under four tree species. Soil Biol Biochem 103:181–191

    Article  Google Scholar 

  • Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    Article  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  Google Scholar 

  • Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596

    Article  Google Scholar 

  • Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315

    Article  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Article  Google Scholar 

  • Shirakawa M, Uehara I, Tanaka M (2019) Mycorrhizosphere bacterial communities and their sensitivity to antibacterial activity of Ectomycorrhizal Fungi. Microbes Environ 34:191–198

    Article  Google Scholar 

  • Singh JS, Gupta SR (1977) Plant decomposition and soil respiration in terrestrial ecosystems. Bot Rev 43:449–528

    Article  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Article  Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451

    Article  Google Scholar 

  • Sun S, Li S, Avera BN, Strahm BD, Badgley BD (2017) Soil bacterial and fungal communities show distinct recovery patterns during forest ecosystem restoration. Appl Environ Microbiol 83:966–983

    Article  Google Scholar 

  • Tateno R, Hishi T, Takeda H (2004) Above- and belowground biomass and net primary production in a cool-temperate deciduous forest in relation to topographical changes in soil nitrogen. For Ecol Manag 193:297–306

    Article  Google Scholar 

  • Tatsumi C, Taniguchi T, Du S, Yamanaka N, Tateno R (2020) Soil nitrogen cycling is determined by the competition between mycorrhiza and ammonia-oxidizing prokaryotes. Ecology 101:e02963

    Article  Google Scholar 

  • Tatsumi C, Taniguchi T, Du S, Yamanaka N, Tateno R (2019) The steps in the soil nitrogen transformation process vary along an aridity gradient via changes in the microbial community. Biogeochemistry 144:15–29

    Article  Google Scholar 

  • Taylor AE, Giguere AT, Zoebelein CM, Myrold DD, Bottomley PJ (2017) Modeling of soil nitrification responses to temperature reveals thermodynamic differences between ammonia-oxidizing activity of archaea and bacteria. ISME J 11:896–908

    Article  Google Scholar 

  • Toju H, Kishida O, Katayama N, Takagi K (2016) Networks depicting the fine-scale co-occurrences of fungi in soil horizons. PLoS ONE 11:1–18

    Article  Google Scholar 

  • Toju H, Tanabe AS, Yamamoto S, Sato H (2012) High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS ONE 7:e40863

    Article  Google Scholar 

  • Torsvik V, Øvreås L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5:240–245

    Article  Google Scholar 

  • Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364

    Article  Google Scholar 

  • Trivedi P, Delgado-Baquerizo M, Trivedi C, Hu H, Anderson IC, Jeffries TC et al (2016) Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships. ISME J 10:2593–2604

    Article  Google Scholar 

  • Urakawa R, Ohte N, Shibata H, Isobe K, Tateno R, Oda T et al (2016) Factors contributing to soil nitrogen mineralization and nitrification rates of forest soils in the Japanese archipelago. For Ecol Manage 361:382–396

    Article  Google Scholar 

  • Urbanová M, Šnajdr J, Baldrian P (2015) Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees. Soil Biol Biochem 84:53–64

    Article  Google Scholar 

  • Uroz S, Oger P, Tisserand E, Cébron A, Turpault M-P, Buée M et al (2016) Specific impacts of beech and Norway spruce on the structure and diversity of the rhizosphere and soil microbial communities. Sci Rep 6:27756

    Article  Google Scholar 

  • Ushio M, Kitayama K, Balser TC (2010) Tree species-mediated spatial patchiness of the composition of microbial community and physicochemical properties in the topsoils of a tropical montane forest. Soil Biol Biochem 42:1588–1595

    Article  Google Scholar 

  • Vitousek P, Howarth R (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  • Wan X, Huang Z, He Z, Yu Z, Wang M, Davis MR, Yang Y (2015) Soil C: N ratio is the major determinant of soil microbial community structure in subtropical coniferous and broadleaf forest plantations. Plant Soil 387:103–116

    Article  Google Scholar 

  • Wertz S, Degrange V, Prosser JI, Poly F, Commeaux C, Freitag T et al (2006) Maintenance of soil functioning following erosion of microbial diversity. Environ Microbiol 8:2162–2169

    Article  Google Scholar 

  • Wilhelm RC, Singh R, Eltis LD, Mohn WW (2019) Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing. ISME J 13:413–429

    Article  Google Scholar 

  • Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L et al (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77:4618–4625

    Article  Google Scholar 

  • Zhang L-M, Hu H-W, Shen J-P, He J-Z (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045

    Article  Google Scholar 

  • Zhu T, Meng T, Zhang J, Zhong W, Müller C, Cai Z (2015) Fungi-dominant heterotrophic nitrification in a subtropical forest soil of China. J Soils Sediments 15:705–709

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Takahito Yoshioka, Dr. Kazuya Kobayashi and the member of Forest Information Laboratory for the helpful suggestion. We also thank Takayuki Yamauchi, Yasuyuki Shibata, Tomoyuki Nakagawa, Jun Yanagimoto, Ken-ichi Ohta, Yuhei Nishioka, Makoto Furuta, Yasunori Kishimoto, Yoichiro Kitagawa, Masaru Okuda, Akira Yamanaka, Yuta Miyagi, Syuichi Sato, Yukie Kawamura and Michiko Shimizu as the staffs of Hokkaido forest research station, Field Science Education and Research Center, Kyoto University for helping the experiments. This study was supported by JSPS-KAKENHI (No. 23780166, 26292085, 18H02241).

Funding

This study was supported by JSPS-KAKENHI: 18H02241, 26292085, 23780166.

Author information

Authors and Affiliations

  1. Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan

    Masataka Nakayama, Shihomi Imamura & Chikae Tatsumi

  2. Research Faculty of Agriculture, Hokkaido University, Hokkaido, 060-8589, Japan

    Chikae Tatsumi

  3. Arid Land Research Center, Tottori University, Tottori, 680-0001, Japan

    Takeshi Taniguchi

  4. Filed Science Education and Research Center, Kyoto University, Kyoto, 606-8502, Japan

    Ryunosuke Tateno

Authors
  1. Masataka Nakayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shihomi Imamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chikae Tatsumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takeshi Taniguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ryunosuke Tateno
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MN, SI and RT conceived and designed the experiment; MN, SI and RT performed the experiment; MN, SI, CT and TT performed data analysis; MN prepared figures and tables; MN and RT took the lead in writing the manuscript with input from all authors.

Corresponding author

Correspondence to Masataka Nakayama.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Steven Perakis.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakayama, M., Imamura, S., Tatsumi, C. et al. Microbial functions and soil nitrogen mineralisation processes in the soil of a cool temperate forest in northern Japan. Biogeochemistry 155, 359–379 (2021). https://doi.org/10.1007/s10533-021-00830-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-021-00830-7

Keywords

Search

Navigation