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Dissimilatory nitrate reduction to ammonium dominates soil nitrate retention capacity in subtropical forests

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Abstract

The abundance, community composition and activity of key nitrogen (N)-cycling functional guilds were monitored at a site where coniferous Cunninghamia lanceolate and broadleaved Mytilaria laosensis were planted in 1993. Leaf cellulose, litter C/N ratio, leaf dry matter content, soil inorganic N content were significantly higher under C. lanceolata, while specific leaf area, litter production, litter magnesium, soil C and soil C/NO3 ratio were higher under M. laosensis. The 15N tracing experiment together with quantitative PCR revealed that autotrophic nitrification rates, as well as the abundances of ammonia-oxidizing archaea and comammox Nitrospira were significantly higher under C. lanceolate than M. laosensis. However, M. laosensis exhibited substantially higher nitrate retention capacity via dissimilatory nitrate reduction to ammonium (DNRA), accompanied by a significantly higher abundance of nrfA gene than C. lanceolate. The Illumina sequencing indicated that tree species markedly affected soil bacterial community composition regardless of the soil layers. Redundancy analysis suggested that litter C/N ratio was the most influential factor explaining functional gene abundances and bacterial communities. Taken together, our findings showed that M. laosensis improved soil N retention capacity mainly through inhibiting autotrophic nitrification while enhancing DNRA activity. This study highlights the importance of tree species identity in influencing the microbially-mediated N cycling and bacterial community composition.

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References

  • Andrianarisoa K, Zeller B, Poly F, Siegenfuhr H, Bienaimé S, Ranger J, Dambrine E (2010) Control of nitrification by tree species in a common-garden experiment. Ecosystems 13:1171–1187

    Article  CAS  Google Scholar 

  • Angst Š, Harantová L, Baldrian P, Angst G, Cajthaml T, Straková P, Blahut J, Veselá H, Frouz J (2019) Tree species identity alters decomposition of understory litter and associated microbial communities: a case study. Biol Fertil Soils 55:525–538

    Article  CAS  Google Scholar 

  • Bengtson P, Falkengren-Grerup U, Bengtsson G (2006) Spatial distributions of plants and gross N transformation rates in a forest soil. J Ecol 94:754–764

    Article  CAS  Google Scholar 

  • Bonito G, Reynolds H, Robeson MS, Nelson J, Hodkinson BP, Gerald T, Schadt CW, Vilgalys R (2014) Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol Ecol 23:3356–3370

    Article  PubMed  Google Scholar 

  • Bowman WD, Cleveland CC, Halada Ĺ, Hreško J, Baron J (2008) Negative impact of nitrogen deposition on soil buffering capacity. Nat Geosci 1:767–770

    Article  CAS  Google Scholar 

  • Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252

    Article  CAS  PubMed  Google Scholar 

  • Burton J, Chen CC, Xu ZH, Ghadiri H (2010) Soil microbial biomass, activity and community composition in adjacent native and plantation forests of subtropical Australia. J Soils Sediment 10:1267–1277

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cornelissen JHC, Lavore S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardized and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Article  Google Scholar 

  • Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92:621–632

    Article  PubMed  Google Scholar 

  • de Schrijver A, de Frenne P, Staelens J, Verstraeten G, Muys B, Vesterdal L, Wuyts K, van Nevel L, Schelfhout S, de Nevekris S, Verheyen K (2012) Tree species traits cause divergence in soil acidification during four decades of postagricultural forest development. Glob Chang Biol 18:1127–1140

    Article  Google Scholar 

  • Duan M, House J, Liu Y, Chang SX (2018) Contrasting responses of gross and net nitrogen transformations to salinity in a reclaimed boreal forest soil. Biol Fertil Soils 54:385–395

    Article  CAS  Google Scholar 

  • Dukunde A, Schneider D, Schmidt M, Veldkamp E, Daniel R (2019) Tree species shape soil bacterial community structure and function in temperate deciduous forests. Front Microbiol 10:1519

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2016) UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv:081257

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci 103:626–631

    Article  CAS  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  CAS  PubMed  Google Scholar 

  • Freschet GT, Cornwell WK, Wardle DA, Elumeeva TG, Liu WD, Jackson BG, Onipchenko VG, Soudzilovskaia NA, Tao JP, Cornelissen JHC (2013) Linking litter decomposition of above- and below-ground organs to plant–soil feedbacks worldwide. J Ecol 101:943–952

    Article  CAS  Google Scholar 

  • Harrison KA, Bardgett RD (2010) Influence of plant species and soil conditions on plant–soil feedback in mixed grassland communities. J Ecol 98:384–395

    Article  Google Scholar 

  • Hayden HL, Drake J, Imhof M, Oxley APA, Norng S, Mele PM (2010) The abundance of nitrogen cycle genes amoA and nifH depends on land-uses and soil types in south-eastern Australia. Soil Biol Biochem 42:1774–1783

    Article  CAS  Google Scholar 

  • Hobbie SE (2015) Plant species effects on nutrient cycling: revisiting litter feedbacks. Trends Ecol Evol 30:357–363

    Article  PubMed  Google Scholar 

  • Hu HW, Chen D, He JZ (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev 39:729–749

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Wan X, He Z, Yu Z, Wang M, Hu Z, Yang Y (2013) Soil microbial biomass, community composition and soil nitrogen cycling in relation to tree species in subtropical China. Soil Biol Biochem 62:68–75

    Article  CAS  Google Scholar 

  • Huygens D, Boeckx P, Templer P, Paulino L, Van CO, Oyarzún C, Müller C, Godoy R (2008) Mechanisms for retention of bioavailable nitrogen in volcanic rainforest soils. Nat Geosci 1:543–548

    Article  CAS  Google Scholar 

  • Kaiser K, Wemheuer B, Korolkow V, Wemheuer F, Nacke H, Schöning I, Schrumpf M, Daniel R (2016) Driving forces of soil bacterial community structure, diversity, and function in temperate grasslands and forests. Sci Rep 6:33696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H, Bae HS, Reddy KR, Ogram A (2016) Distributions, abundances and activities of microbes associated with the nitrogen cycle in riparian and stream sediments of a river tributary. Water Res 106:51–61

    Article  CAS  PubMed  Google Scholar 

  • Knops JMH, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466

    Article  Google Scholar 

  • Langenbruch C, Helfrich M, Flessa H (2012) Effects of beech (Fagus sylvatica), ash (Fraxinus excelsior) and lime (Tilia spec.) on soil chemical properties in a mixed deciduous forest. Plant Soil 352:389–403

    Article  CAS  Google Scholar 

  • Laughlin DC (2011) Nitrification is linked to dominant leaf traits rather than functional diversity. J Ecol 99:1091–1099

    Article  Google Scholar 

  • Leloup J, Baude M, Nunan N, Meriguet J, Dajoz I, Roux XL, Raynaud X (2018) Unravelling the effects of plant species diversity and aboveground litter input on soil bacterial communities. Geoderma 317:1–7

    Article  Google Scholar 

  • Li P, Shen CC, Jiang L, Feng ZZ, Fang JY (2019) Difference in soil bacterial community composition depends on forest type rather than nitrogen and phosphorus additions in tropical montane rainforests. Bio Fertil Soils 55:313–323

    Article  CAS  Google Scholar 

  • Liu HY, Ding Y, Zhang QC, Liu XM, Xu JM, Li Y, Di HJ (2018) Heterotrophic nitrification and denitrification are the main sources of nitrous oxide in two paddy soils. Plant Soil 445:39–53

    Article  CAS  Google Scholar 

  • Lovett GM, Weathers KC, Arthur MA, Schultz JC (2004) Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochem 67:289–308

    Article  CAS  Google Scholar 

  • Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704

    Article  CAS  PubMed  Google Scholar 

  • Minick KJ, Pandey CB, Fox TR, Subedi S (2016) Dissimilatory nitrate reduction to ammonium and N2O flux: effect of soil redox potential and N fertilization in loblolly pine forests. Biol Fertil Soils 52:601–614

    Article  CAS  Google Scholar 

  • Müller C, Rütting T, Kattge J, Laughlin RJ, Stevens RJ (2007) Estimation of parameters in complex 15N tracing models by Monte Carlo sampling. Soil Biol Biochem 39:715–726

    Article  CAS  Google Scholar 

  • Nacke H, Thürmer A, Wollherr A, Will C, Hodac L, Herold N, Schöning I, Schrumpf M, Daniel R (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6:e17000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nannipieri P, Penton CR, Purahong W, Schloter M, van Elsas JD (2019) Recommendations for soil microbiome analyses. Biol Fertil Soils 55:765–766

    Article  Google Scholar 

  • Pajares S, Bohannan BJ (2016) Ecology of nitrogen fixing, nitrifying, and denitrifying microorganisms in tropical forest soils. Front Microbiol 7:1045

    PubMed  PubMed Central  Google Scholar 

  • Pan H, Xie K, Zhang QC, Jia ZJ, Xu JM, Di HJ, Li Y (2018) Archaea and bacteria respectively dominate nitrification in lightly and heavily grazed soil in a grassland system. Bio Fertil Soils 54:41–54

    Article  CAS  Google Scholar 

  • Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14:993–1008

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer B, Fender AC, Lasota S, Hertel D, Jungkunst HF, Daniel R (2013) Leaf litter is the main driver for changes in bacterial community structures in the rhizosphere of ash and beech. Appl Soil Ecol 72:150–160

    Article  Google Scholar 

  • Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. For Ecol Manag 309:19–27

    Article  Google Scholar 

  • Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin HL, Xing XY, Tang YF, Hou HJ, Yang J, Shen R, Zhang WZ, Liu Y, Wei WX (2019) Linking soil N2O emissions with soil microbial community abundance and structure related to nitrogen cycle in two acid forest soils. Plant Soil 435:95–109

    Article  CAS  Google Scholar 

  • Reverchon F, Bai SH, Liu X, Blumfield TJ (2015) Tree plantation systems influence nitrogen retention and the abundance of nitrogen functional genes in the Solomon Islands. Front Microbiol 6:1439

    Article  PubMed  PubMed Central  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  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Saghir NS, Mungwari FP, Mulvaney RL, Azam F (1993) Determination of nitrogen by microdiffusion in Mason jars. II. Inorganic nitrogen-15 in soil extracts. Commun Soil Sci Plan 24:2747–2763

    Article  CAS  Google Scholar 

  • Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489

    Article  Google Scholar 

  • Shi XZ, Hu HW, Müller C, He JZ, Chen DL, Suter HC (2016) Effects of the nitrification inhibitor 3,4-dimethylpyrazole phosphate on nitrification and nitrifiers in two contrasting agricultural soils. Appl Environ Microbiol 82:5236–5248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi XZ, Hu HW, Zhu-Barker X, Hayden H, Wang JT, Suter H, Chen DL, He JZ (2017) Nitrifier-induced denitrification is an important source of soil nitrous oxide and can be inhibited by a nitrification inhibitor 3,4-dimethylpyrazole phosphate. Environm Microbiol 19:4851–4865

    Article  CAS  Google Scholar 

  • Shi XZ, Hu HW, Wang JQ, He JZ, Zheng CY, Wan XH, Huang ZQ (2018) Niche separation of comammox Nitrospira and canonical ammonia oxidizers in an acidic subtropical forest soil under long-term nitrogen deposition. Soil Biol Biochem 126:114–122

    Article  CAS  Google Scholar 

  • Song B, Lisa JA, Tobias CR (2014) Linking DNRA community structure and activity in a shallow lagoonal estuarine system. Front Microbiol 5:460

    Article  PubMed  PubMed Central  Google Scholar 

  • Srikanthasamy T, Leloup J, N'Dri A, Barot S, Gervaix J, Koné AW, Koffi K, Le Roux X, Raynaud X, Lata JC (2018) Contrasting effects of grasses and trees on microbial N-cycling in an African humid savanna. Soil Biol Biochem 117:153–163

    Article  CAS  Google Scholar 

  • Staelens J, Rütting T, Huygens D, Schrijver AD, Müller C, Verheyen K, Boeckx P (2011) In situ gross nitrogen transformations differ between temperate deciduous and coniferous forest soils. Biogeochem 108:259–277

    Article  CAS  Google Scholar 

  • Stone MM, Kan JJ, Plante AF (2015) Parent material and vegetation influence bacterial community structure and nitrogen functional genes along deep tropical soil profiles at the Luquillo critical zone observatory. Soil Biol Biochem 80:273–282

    Article  CAS  Google Scholar 

  • Talbot JM, Treseder KK (2012) Interactions among lignin, cellulose, and nitrogen drive litter chemistry–decay relationships. Ecol 93:345–354

    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  CAS  Google Scholar 

  • Uroz S, Buée M, Deveau A, Mieszkin S, Martin F (2016) Ecology of the forest microbiome: highlights of temperate and boreal ecosystems. Soil Biol Biochem 103:471–488

    Article  CAS  Google Scholar 

  • van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276

    Article  Google Scholar 

  • Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart - how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484

    Article  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  CAS  PubMed  Google Scholar 

  • Wear EK, Wilbanks EG, Nelson CE (2018) Primer selection impacts specific population abundances but not community dynamics in a monthly time-series 16S rRNA gene amplicon analysis of coastal marine bacterio plankton. Environ Microbiol 20:2709–2726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao HY, Gao YM, Nicol GW, Campbell CD, Prosser JI, Zhang LM, Han WY, Singh BK (2014) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77:4618–4625

    Article  CAS  Google Scholar 

  • Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecol 84:2042–2050

    Article  Google Scholar 

  • Zhang YS, Ding H, Zheng XZ, Cai ZC, Misselbrook T, Carswell A, Müller C, Zhang J (2018) Soil N transformation mechanisms can effectively conserve N in soil under saturated conditions compared to unsaturated conditions in subtropical China. Biol Fertil Soils 54:495–507

    Article  CAS  Google Scholar 

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Acknowledgements

We sincerely appreciate the sampling processing and laboratory assistance from Lei Wang and Tao Wang. We thank the three anonymous reviewers and editor for improving the scope and the quality of the manuscript. This research was financially supported by the National Natural Science Foundation of China (41907022, 31741024 and 31901165), and the National Science Foundation for Distinguished Young Scholars (31625007). The study was carried out in collaboration with the German Science foundation research unit DASIM (DFG FOR 2337). The authors declare no conflict of interest.

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Shi, X., Wang, J., Müller, C. et al. Dissimilatory nitrate reduction to ammonium dominates soil nitrate retention capacity in subtropical forests. Biol Fertil Soils 56, 785–797 (2020). https://doi.org/10.1007/s00374-020-01457-w

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