Abstract
Background and aims
Litter decomposition and nitrogen metabolism are the key determinants of nutrient cycling in forest ecosystems. However, how processes and functional groups are affected by mixed litter decomposition is poorly understood. The aim of this research is to determine how the microbial functional pathways involved in nitrogen cycling varied according to the changes in the microbial community composition induced by mixing of litter.
Methods
The fallen leaf litters were collected on days 60, 150, 270, and 360 in Larix, Sassafras, and Larix/Sassafras plantations. The nitrogen properties, enzyme activities, microbial communities, and nitrogen metabolism pathways were evaluated during decomposition of three litter types.
Results
The pH, nitrate content, and organic nitrogen degradative enzyme activities of mixed litter were higher than those of Larix litter. Mixed litter promoted the abundances and potential nitrogen metabolism functions of Sphingomonas, and Janthinobacterium versus Larix litter during decomposition. The abundances of genes associated with microbial organic nitrogen degradation and assimilatory nitrate reduction differed significantly according to litter types. The abundance of microbial functional genes related to the production of ammonium was significantly higher in mixed litter than in Larix litter. Co-occurrence network analyses showed that mixed litter had a less complex but more stable microbial co-occurrence pattern versus monospecific litter. The difference of litter pH and nitrate content between mixed litter and Larix litter are determinants of changes in microbial functional potentials of nitrogen metabolism.
Conclusions
Mixing Sassafras/Larix litter would selectively modulate nitrogen metabolism related bacterial groups, together with functional pathways of organic nitrogen degradation and assimilatory nitrate reduction processes. These changes were mainly driven by litter pH and nitrate content.
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References
Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439. https://doi.org/10.2307/3546886
Aerts R, De Caluwe H, Beltman B (2003) Plant community mediated vs. nutritional controls on litter decomposition rates in grasslands. Ecology 84:3198–3208. https://doi.org/10.1890/02-0712
Bai S, Li J, He Z et al (2013) GeoChip-based analysis of the functional gene diversity and metabolic potential of soil microbial communities of mangroves. Appl Microbiol Biotechnol 97:7035–7048. https://doi.org/10.1007/s00253-012-4496-z
Balser TC, Firestone MK (2005) Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest. Biogeochemistry 73:395–415. https://doi.org/10.1007/s10533-004-0372-y
Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576. https://doi.org/10.1038/s41579-018-0024-1
Bedmar EJ, Robles EF, Delgado MJ (2005) The complete denitrification pathway of the symbiotic, nitrogen-fixing bacterium Bradyrhizobium japonicum. Biochem Soc Trans 33:141–144. https://doi.org/10.1042/BST0330141
Bissett A, Brown MV, Siciliano SD, Thrall PH (2013) Microbial community responses to anthropogenically induced environmental change: towards a systems approach. Ecol Lett 16:128–139. https://doi.org/10.1111/ele.12109
Bowen JL, Ward BB, Morrison HG, Hobbie JE, Valiela I, Deegan LA, Sogin ML (2011) Microbial community composition in sediments resists perturbation by nutrient enrichment. ISME J 5:1540–1548. https://doi.org/10.1038/ismej.2011.22
Byun T, Blinkovsky A (2004) Glycyl aminopeptidase (Sphingomonas). Handbook of Proteolytic Enzymes. Elsevier, In, pp 470–471
Cardenas E, Orellana LH, Konstantinidis KT, Mohn WW (2018) Effects of timber harvesting on the genetic potential for carbon and nitrogen cycling in five north American forest ecozones. Sci Rep 8:3142. https://doi.org/10.1038/s41598-018-21197-0
Cardona C, Weisenhorn P, Henry C, Gilbert JA (2016) Network-based metabolic analysis and microbial community modeling. Curr Opin Microbiol 31:124–131. https://doi.org/10.1016/j.mib.2016.03.008
Condron L, Stark C, O’Callaghan M et al (2010) The role of microbial communities in the formation and decomposition of soil organic matter. In: Soil microbiology and sustainable crop production. Springer Netherlands, Dordrecht, pp 81–118
Costello EK, Stagaman K, Dethlefsen L et al (2012) The application of ecological theory toward an understanding of the human microbiome. Science 336(80):1255–1262. https://doi.org/10.1126/science.1224203
Du J, Niu J, Gao Z et al (2019) Catena E ff ects of rainfall intensity and slope on interception and precipitation partitioning by forest litter layer. Catena 172:711–718. https://doi.org/10.1016/j.catena.2018.09.036
Fan K, Weisenhorn P, Gilbert JA, Chu H (2018) Wheat rhizosphere harbors a less complex and more stable microbial co-occurrence pattern than bulk soil. Soil Biol Biochem 125:251–260. https://doi.org/10.1016/j.soilbio.2018.07.022
Fang W, Yan D, Wang X, Huang B, Wang X, Liu J, Liu X, Li Y, Ouyang C, Wang Q, Cao A (2018) Responses of nitrogen-cycling microorganisms to Dazomet fumigation. Front Microbiol 9:2529. https://doi.org/10.3389/fmicb.2018.02529
Galloway JN, Dentener FJ, Capone DG et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226. https://doi.org/10.1007/s10533-004-0370-0
Garibaldi LA, Semmartin M, Chaneton EJ (2007) Grazing-induced changes in plant composition affect litter quality and nutrient cycling in flooding Pampa grasslands. Oecologia 151:650–662. https://doi.org/10.1007/s00442-006-0615-9
Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246. https://doi.org/10.1111/j.0030-1299.2004.12738.x
Geisseler D, Horwath WR, Joergensen RG et al (2010) Pathways of nitrogen utilization by soil microorganisms – a review. Soil Biol Biochem 42:2058–2067. https://doi.org/10.1016/j.soilbio.2010.08.021
Gower ST, Richards JH (1990) Larixes: deciduous conifers in an Evergreen world. Bioscience 40:818–826. https://doi.org/10.2307/1311484
Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296. https://doi.org/10.1038/nature06592
Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218. https://doi.org/10.1146/annurev.ecolsys.36.112904.151932
He Z, Xu M, Deng Y, Kang S, Kellogg L, Wu L, van Nostrand J, Hobbie SE, Reich PB, Zhou J (2010) Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. Ecol Lett 13:564–575. https://doi.org/10.1111/j.1461-0248.2010.01453.x
Herbert RA (1999) Nitrogen cycling in coastal marine ecosystems. FEMS Microbiol Rev 23:563–590. https://doi.org/10.1111/j.1574-6976.1999.tb00414.x
Hu YL, Wang SL, Zeng DH (2006) Effects of single Chinese fir and mixed leaf litters on soil chemical, microbial properties and soil enzyme activities. Plant Soil 282:379–386. https://doi.org/10.1007/s11104-006-0004-5
Huang X, Dong W, Wang H, Feng Y (2018) Role of acid/alkali-treatment in primary sludge anaerobic fermentation: insights into microbial community structure, functional shifts and metabolic output by high-throughput sequencing. Bioresour Technol 249:943–952. https://doi.org/10.1016/j.biortech.2017.10.104
Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J (2010) Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. ISME J 4:450–454. https://doi.org/10.1038/ismej.2009.125
Kandeler E (1999) Xylanase, invertase and protease at the soil–litter interface of a loamy sand. Soil Biol Biochem 31:1171–1179. https://doi.org/10.1016/S0038-0717(99)00035-8
Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:277–280. https://doi.org/10.1093/nar/gkh063
Keiblinger KM, Hall EK, Wanek W, Szukics U, Hämmerle I, Ellersdorfer G, Böck S, Strauss J, Sterflinger K, Richter A, Zechmeister-Boltenstern S (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency. FEMS Microbiol Ecol 73:430–440. https://doi.org/10.1111/j.1574-6941.2010.00912.x
Kourtev P, Ehrenfeld J, Huang W (2002) Enzyme activities during litter decomposition of two exotic and two native plant species in hardwood forests of New Jersey. Soil Biol Biochem 34:1207–1218. https://doi.org/10.1016/S0038-0717(02)00057-3
Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JM, McCulley R, la Pierre K, Risch AC, Seabloom EW, Schütz M, Steenbock C, Stevens CJ, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci 112:10967–10972. https://doi.org/10.1073/pnas.1508382112
Lin Y, Ye G, Kuzyakov Y et al (2019) Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biol Biochem 134:187–196. https://doi.org/10.1016/j.soilbio.2019.03.030
Liu S, Ren H, Shen L et al (2015) pH levels drive bacterial community structure in sediments of the Qiantang River as determined by 454 pyrosequencing. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.00285
Liu D, Keiblinger KM, Leitner S et al (2016) Is there a convergence of deciduous leaf litter stoichiometry, biochemistry and microbial population during decay? Geoderma 272:93–100. https://doi.org/10.1016/j.geoderma.2016.03.005
Lowell JL, Gordon N, Engstrom D, Stanford JA, Holben WE, Gannon JE (2009) Habitat heterogeneity and associated microbial community structure in a small-scale floodplain Hyporheic flow path. Microb Ecol 58:611–620. https://doi.org/10.1007/s00248-009-9525-9
Lv Y, Wang C, Jia Y et al (2014) Effects of sulfuric, nitric, and mixed acid rain on litter decomposition, soil microbial biomass, and enzyme activities in subtropical forests of China. Appl Soil Ecol 79:1–9. https://doi.org/10.1016/j.apsoil.2013.12.002
Ma B, Lv X, Cai Y et al (2018) Liming does not counteract the influence of long-term fertilization on soil bacterial community structure and its co-occurrence pattern. Soil Biol Biochem 123:45–53. https://doi.org/10.1016/j.soilbio.2018.05.003
Magasanik B (1993) The regulation of nitrogen utilization in enteric bacteria. J Cell Biochem 51:34–40. https://doi.org/10.1002/jcb.240510108
Mandakovic D, Rojas C, Maldonado J, Latorre M, Travisany D, Delage E, Bihouée A, Jean G, Díaz FP, Fernández-Gómez B, Cabrera P, Gaete A, Latorre C, Gutiérrez RA, Maass A, Cambiazo V, Navarrete SA, Eveillard D, González M (2018) Structure and co-occurrence patterns in microbial communities under acute environmental stress reveal ecological factors fostering resilience. Sci Rep 8:5875. https://doi.org/10.1038/s41598-018-23931-0
Menge DNL, Hedin LO, Pacala SW (2012) Nitrogen and phosphorus limitation over long-term ecosystem development in terrestrial ecosystems. PLoS One 7:e42045. https://doi.org/10.1371/journal.pone.0042045
Mooshammer M, Wanek W, Hämmerle I, Fuchslueger L, Hofhansl F, Knoltsch A, Schnecker J, Takriti M, Watzka M, Wild B, Keiblinger KM, Zechmeister-Boltenstern S, Richter A (2014) Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling. Nat Commun 5:3694. https://doi.org/10.1038/ncomms4694
Moreno-Vivián C, Cabello P, Martínez-Luque M, Blasco R, Castillo F (1999) Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181:6573–6584. https://doi.org/10.3846/bm.2012.131
Nelson MB, Berlemont R, Martiny AC, Martiny JBH (2015) Nitrogen cycling potential of a grassland litter microbial community. Appl Environ Microbiol 81(20):7012–7022. https://doi.org/10.1128/aem.02222-15
Nelson MB, Martiny AC, Martiny JBH (2016) Global biogeography of microbial nitrogen-cycling traits in soil. Proc Natl Acad Sci 113:8033–8040. https://doi.org/10.1073/pnas.1601070113
Olofsson J, Oksanen L (2002) Role of litter decomposition for the increased primary production in areas heavily grazed by reindeer: a litterbag experiment. Oikos 96:507–515. https://doi.org/10.1034/j.1600-0706.2002.960312.x
Pereira APA, Durrer A, Gumiere T et al (2019) Mixed Eucalyptus plantations induce changes in microbial communities and increase biological functions in the soil and litter layers. For Ecol Manag 433:332–342. https://doi.org/10.1016/j.foreco.2018.11.018
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. https://doi.org/10.1111/j.1462-2920.2011.02679.x
Philippot L, Spor A, Hénault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron PA (2013) Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–1619. https://doi.org/10.1038/ismej.2013.34
Prescott CE, Hope GD, Blevins LL (2003) Effect of gap size on litter decomposition and soil nitrate concentrations in a high-elevation spruce–fir forest. Can J For Res 33:2210–2220. https://doi.org/10.1139/x03-152
Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, MetaHIT Consortium, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65. https://doi.org/10.1038/nature08821
Remy E, Wuyts K, Verheyen K et al (2018) Altered microbial communities and nitrogen availability in temperate forest edges. Soil Biol Biochem 116:179–188. https://doi.org/10.1016/j.soilbio.2017.10.016
Riggs CE, Hobbie SE (2016) Mechanisms driving the soil organic matter decomposition response to nitrogen enrichment in grassland soils. Soil Biol Biochem 99:54–65. https://doi.org/10.1016/j.soilbio.2016.04.023
Sabri NSA, Zakaria Z, Mohamad SE, Jaafar AB, Hara H (2018) Importance of soil temperature for the growth of temperate crops under a tropical climate and functional role of soil microbial diversity. Microbes Environ 33(2):144–150. https://doi.org/10.1264/jsme2.me17181
Schneider T, Keiblinger KM, Schmid E, Sterflinger-gleixner K (2012) Who is who in litter decomposition ? Metaproteomics reveals major microbial players and their biogeochemical functions 1749–1762. https://doi.org/10.1038/ismej.2012.11
Semmartin M, Aguiar MR, Distel RA et al (2004) Litter quality and nutrient cycling affected by grazing-induced species replacements along a precipitation gradient. Oikos 107:148–160. https://doi.org/10.1111/j.0030-1299.2004.13153.x
Song K, Yu Q, Shang K, Yang T, da LJ (2011) The spatio-temporal pattern of historical disturbances of an evergreen broadleaved forest in East China: a dendroecological analysis. Plant Ecol 212:1313–1325. https://doi.org/10.1007/s11258-011-9907-1
Strickland MS, Osburn E, Lauber C et al (2009) Litter quality is in the eye of the beholder: initial decomposition rates as a function of inoculum characteristics. Funct Ecol 23:627–636. https://doi.org/10.1111/j.1365-2435.2008.01515.x
Summers EA, Paoletti MG, Beggio M et al (2013) Comparative microbial community composition from secondary carbonate (moonmilk) deposits: implications for the Cansiliella servadeii cave hygropetric food web. Int J Speleol 42:181–192. https://doi.org/10.5038/1827-806X.42.3.2
Sun S, Badgley BD (2019) Changes in microbial functional genes within the soil metagenome during forest ecosystem restoration. Soil Biol Biochem 135:163–172. https://doi.org/10.1016/j.soilbio.2019.05.004
Tang Y, Yu G, Zhang X et al (2018) Changes in nitrogen-cycling microbial communities with depth in temperate and subtropical forest soils. Appl Soil Ecol 124:218–228. https://doi.org/10.1016/j.apsoil.2017.10.029
Temu T, Mann M, Räschle M, Cox J (2016) Homology-driven assembly of NOn-redundant protEin sequence sets (NOmESS) for mass spectrometry. Bioinformatics 32:1417–1419. https://doi.org/10.1093/bioinformatics/btv756
Tu Q, Yu H, He Z, Deng Y, Wu L, van Nostrand J, Zhou A, Voordeckers J, Lee YJ, Qin Y, Hemme CL, Shi Z, Xue K, Yuan T, Wang A, Zhou J (2014) GeoChip 4: a functional gene-array-based high-throughput environmental technology for microbial community analysis. Mol Ecol Resour 14:914–928. https://doi.org/10.1111/1755-0998.12239
Tu Q, He Z, Wu L et al (2017) Metagenomic reconstruction of nitrogen cycling pathways in a CO2-enriched grassland ecosystem. Soil Biol Biochem 106:99–108. https://doi.org/10.1016/j.soilbio.2016.12.017
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. https://doi.org/10.1016/j.soilbio.2015.02.011
Vaieretti MV, Cingolani AM, Pérez Harguindeguy N, Cabido M (2013) Effects of differential grazing on decomposition rate and nitrogen availability in a productive mountain grassland. Plant Soil 371:675–691. https://doi.org/10.1007/s11104-013-1831-9
Wang C, Guo P, Han G, Feng X, Zhang P, Tian X (2010) Effect of simulated acid rain on the litter decomposition of Quercus acutissima and Pinus massoniana in forest soil microcosms and the relationship with soil enzyme activities. Sci Total Environ 408:2706–2713. https://doi.org/10.1016/j.scitotenv.2010.03.023
Wang W, Chen D, Sun X et al (2019) Impacts of mixed litter on the structure and functional pathway of microbial community in litter decomposition. Appl Soil Ecol 144:72–82. https://doi.org/10.1016/j.apsoil.2019.07.006
Wong KH, Hynes MJ, Davis MA (2008) Recent advances in nitrogen regulation: a comparison between Saccharomyces cerevisiae and filamentous fungi. Eukaryot Cell 7:917–925. https://doi.org/10.1128/EC.00076-08
Xiao X, Yin X, Lin J, Sun L, You Z, Wang P, Wang F (2005) Chitinase genes in lake sediments of Ardley Island, Antarctica. Appl Environ Microbiol 71:7904–7909. https://doi.org/10.1128/AEM.71.12.7904-7909.2005
Xie J, He Z, Liu X, Liu X, van Nostrand J, Deng Y, Wu L, Zhou J, Qiu G (2011) GeoChip-based analysis of the functional gene diversity and metabolic potential of microbial communities in acid mine drainage. Appl Environ Microbiol 77:991–999. https://doi.org/10.1128/AEM.01798-10
Xiong Y, Fan P, Fu S et al (2013) Slow decomposition and limited nitrogen release by lower order roots in eight Chinese temperate and subtropical trees. Plant Soil 363:19–31. https://doi.org/10.1007/s11104-012-1290-8
Xu M, Zhang Q, Xia C, Zhong Y, Sun G, Guo J, Yuan T, Zhou J, He Z (2014) Elevated nitrate enriches microbial functional genes for potential bioremediation of complexly contaminated sediments. ISME J 8:1932–1944. https://doi.org/10.1038/ismej.2014.42
Xu J, Liu S, Song S et al (2018) Arbuscular mycorrhizal fungi influence decomposition and the associated soil microbial community under different soil phosphorus availability. Soil Biol Biochem 120:181–190. https://doi.org/10.1016/j.soilbio.2018.02.010
Zeng L, He W, Teng M, Luo X, Yan Z, Huang Z, Zhou Z, Wang P, Xiao W (2018) Effects of mixed leaf litter from predominant afforestation tree species on decomposition rates in the three gorges reservoir, China. Sci Total Environ 639:679–686. https://doi.org/10.1016/j.scitotenv.2018.05.208
Zeng Q, Liu Y, Zhang H, An S (2019) Fast bacterial succession associated with the decomposition of Quercus wutaishanica litter on the loess plateau. Biogeochemistry 144:119–131. https://doi.org/10.1007/s10533-019-00575-4
Zhalnina K, Dias R, de Quadros PD, Davis-Richardson A, Camargo FA, Clark IM, McGrath S, Hirsch PR, Triplett EW (2015) Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69:395–406. https://doi.org/10.1007/s00248-014-0530-2
Zhang L, Adams JM, Dumont MG et al (2019a) Distinct methanotrophic communities exist in habitats with different soil water contents. Soil Biol Biochem 132:143–152. https://doi.org/10.1016/j.soilbio.2019.02.007
Zhang W, Yang K, Lyu Z, Zhu J (2019b) Microbial groups and their functions control the decomposition of coniferous litter: a comparison with broadleaved tree litters. Soil Biol Biochem. https://doi.org/10.1016/j.soilbio.2019.03.009
Zhou J, He Z, Yang Y et al (2015) High-throughput metagenomic technologies for complex microbial community analysis: open and closed formats. MBio 6:e02288–e02214. https://doi.org/10.1128/mBio.02288-14
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This research was funded by The National Key Research and Development Program of China (Project no. 2017YFD0600401).
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Wang, W., Chen, D., Zhang, Q. et al. Effects of mixed coniferous and broad-leaved litter on bacterial and fungal nitrogen metabolism pathway during litter decomposition. Plant Soil 451, 307–323 (2020). https://doi.org/10.1007/s11104-020-04523-2
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DOI: https://doi.org/10.1007/s11104-020-04523-2