Abstract
Purpose
Although both bacterial and fungal communities play a substantial role in the transformation of soil nitrogen (N), it is unclear how each community contributes to soil net N mineralization during plant invasion. The current study examined the contributions of bacterial and fungal communities to soil N mineralization in soils from Moso bamboo (a natively invasive forest), mixed bamboo-broadleaf (a moderately invaded forest), and broadleaf (an uninvaded forest) forests using the bactericides and fungicides.
Methods
The incubation experiment comprised three different invasion stages of bamboo and three treatments including no biocide (control), bactericide (streptomycin), and fungicide (cycloheximide). The contributions of bacterial and fungal communities to soil net ammonification and nitrification were determined by measuring soil N mineralization rate, microbial gene abundance, community composition, and by constructing structural equation model (SEM).
Results
Compared with the broadleaf forest, the bamboo forest had 72.6% higher net ammonification in net mineralization. The net nitrification rate in the broadleaf forest was 118.2% higher than in the bamboo forest. Bactericide application reduced net ammonification rates significantly, but fungicide application raised net nitrification rates in all three forest types. In contrast to the control, bactericide decreased the alpha diversity indices of bacterial and fungal communities and altered the fungal composition. According to the SEM results, forest type had positive effects on fungal composition after adding bactericide, which reduced soil ammonification rate. In contrast, the addition of fungicide increased the bacterial abundance but decreased the fungal abundance, and changed the fungal composition. The SEM results suggested that forest type had positive effects on bacterial abundance after adding fungicide, thus increasing the soil net ammonification rate.
Conclusions
These results provide relevant experimental evidence for the role of bacterial and fungal communities in the net ammonification and nitrification of soil, indicating that the bacterial community played a leading role in soil net ammonification during the bamboo invasion.
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References
Bai SB, Zhou GM, Wang YX, Liang QQ, Chen J, Cheng YY, Shen R (2013) Plant species diversity and dynamics in forests invaded by Moso bamboo (Phyllostachys edulis) in Tianmu Mountain Nature Reserve. Biodivers Sci 21(3):288–295 (in Chinese with an English abstract). https://doi.org/10.1038/ng.475
Badalucco L, Pomarě F, Grego S, Landi L, Nannipieri P (1994) Activity and degradation of streptomycin and cycloheximide in soil. Biol Fertil Soils 18(4):334–340. https://doi.org/10.1007/BF00570637
Berg B (2014) Decomposition patterns for foliar litter—a theory for influencing factors. Soil Biol Biochem 78:222–232. https://doi.org/10.1016/j.soilbio.2014.08.005
Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75(2):139–157. https://doi.org/10.1890/04-0988
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(2):443–451. https://doi.org/10.1016/j.soilbio.2007.09.007
Castro-Díez P, Godoy O, Alonso A, Gallardo A, Saldaña A (2014) What explains variation in the impacts of exotic plant invasions on the nitrogen cycle? A Meta-Analysis Ecology Letters 17(1):1–12. https://doi.org/10.1111/ele.12197
Chapin FS, Matson PA, Vitousek PM (2011) Principles of terrestrial ecosystem ecology. Springer, New York
Chen SK, Edwards CA, Subler S (2001) Effects of the fungicides benomyl, captan and chlorothalonil on soil microbial activity and nitrogen dynamics in laboratory incubations. Soil Biol Biochem 33(14):1971–1980. https://doi.org/10.1016/S0038-0717(01)00131-6
Chen ZH, Li YC, Chang SX, Xu QF, Li YF, Ma ZL, Cai YJ (2021) Linking enhanced soil nitrogen mineralization to increased fungal decomposition capacity with Moso bamboo invasion of broadleaf forests. Sci Total Environ 771:144779. https://doi.org/10.1016/j.scitotenv.2020.144779
DeCrappeo NM, DeLorenze EJ, Giguere AT, Pyke DA, Bottomley PJ (2017) Fungal and bacterial contributions to nitrogen cycling in cheatgrass-invaded and uninvaded native sagebrush soils of the western USA. Plant and Soil 416(1):271–281. https://doi.org/10.1007/s11104-017-3209-x
Edwards IP, Upchurch RA, Zak DR (2008) Isolation of fungal cellobiohydrolase I genes from sporocarps and forest soils by PCR. Appl Environ Microbiol 74(11):3481–3489. https://doi.org/10.1128/AEM.02893-07
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Hart SC, Binkley D, Perry DA (1997) Influence of red alder on soil nitrogen transformations in two conifer forests of contrasting productivity. Soil Biol Biochem 29(7):1111–1123. https://doi.org/10.1016/S0038-0717(97)00004-7
Hu XY, Wang XM, Abbas T, Fang T, Miao DN, Li YF, Chang SX, Li YC (2021) Higher ammonium-to-nitrate ratio shapes distinct soil nitrifying community and favors the growth of Moso bamboo in contrast to broadleaf tree species. Biol Fertil Soils 57(8):1171–1182. https://doi.org/10.1007/s00374-021-01596-8
Li MY, Jiang XY, Jin HR (2020) Modes of Uptake and Translocation of NO3- Affecting Growth of Host Plants in Arbuscular Mycorrhizal Symbiosis. Acta Pedologica Sinica 57(6): 1483-1491.https://doi.org/10.11766/trxb201909090476 (in Chinese with an English abstract)
Kasel S, Bennett LT, Tibbits J (2008) Land use influences soil fungal community composition across central Victoria, south-eastern Australia. Soil Biology and Biochemistry 40(7):1724–1732. https://doi.org/10.1016/j.soilbio.2008.02.011
Knops JMH, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5(3):454–466. https://doi.org/10.1046/j.1461-0248.2002.00332.x
Kooijman AM, Bloem J, van Dalen BR, Kalbitz K (2016) Differences in activity and N demand between bacteria and fungi in a microcosm incubation experiment with selective inhibition. Appl Soil Ecol 99:29–39. https://doi.org/10.1016/j.apsoil.2015.11.011
Ling L, Fu YY, Jeewani PH, Tang CX, Pan ST, Reid BJ, Gunina A, Li YF, Li YC, Cai YJ, Kuzyakov Y, Li Y, Su WQ, Singh B, Luo Y, Xu JM (2021) Organic matter chemistry and bacterial community structure regulate decomposition processes in post-fire forest soils. Soil Biol Biochem 160:108311. https://doi.org/10.1016/j.soilbio.2021.108311
Li YC, Li YF, Chang SX, Liang X, Qin H, Chen JH, Xu QF (2017a) Linking soil fungal community structure and function to soil organic carbon chemical composition in intensively managed subtropical bamboo forests. Soil Biol Biochem 107:19–31. https://doi.org/10.1016/j.soilbio.2016.12.024
Li YC, Li YF, Chang SX, Xu QF, Guo ZY, Gao Q, Qin ZY, Yang YF, Chen JH, Liang X (2017b) Bamboo invasion of broadleaf forests altered soil fungal community closely linked to changes in soil organic C chemical composition and mineral N production. Plant Soil 418(1):507–521. https://doi.org/10.1007/s11104-017-3313-y
Li YC, Liang X, Tang CX, Li YF, Chen ZH, Chang SX, Guo ZY, Shen Y, Xu QF (2018) Moso bamboo invasion into broadleaf forests is associated with greater abundance and activity of soil autotrophic bacteria. Plant Soil 428(1):163–177. https://doi.org/10.1007/s11104-018-3648-z
Liu WT, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63(11):4516–4522. https://doi.org/10.1128/aem.63.11.4516-4522.1997
Liu XS, Siemann E, Cui C, Liu YQ, Guo XM, Zhang L (2019) Moso bamboo (Phyllostachys edulis) invasion effects on litter, soil and microbial PLFA characteristics depend on sites and invaded forests. Plant Soil 438(1):85–99. https://doi.org/10.1007/s11104-019-04010-3
Meng M, Wang B, Zhang QL, Tian Y (2021) Driving force of soil microbial community structure in a burned area of Daxing’anling. China Journal of Forestry Research 32(4):1723–1738. https://doi.org/10.1007/s11676-020-01229-0
Moore JC, McCann K, de Ruiter PC (2005) Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiologia 49(6):499–510. https://doi.org/10.1016/j.pedobi.2005.05.008
Myrold DD, Posavatz NR (2007) Potential importance of bacteria and fungi in nitrate assimilation in soil. Soil Biol Biochem 39(7):1737–1743. https://doi.org/10.1016/j.soilbio.2007.01.033
Ouyang M, Tian D, Pan JM, Chen GP, Su HJ, Yan ZB, Yang QP, Ji CJ, Tang ZY, Fang JY (2022) Moso bamboo (Phyllostachys edulis) invasion increases forest soil pH in subtropical China. CATENA 215:106339. https://doi.org/10.1016/j.catena.2022.106339
Pan YS, Wu YC, Li XZ, Zeng J, Lin XG (2019) Continuing impacts of selective inhibition on bacterial and fungal communities in an agricultural soil. Microb Ecol 78(4):927–935. https://doi.org/10.1007/s00248-019-01364-0
Rousk J, Demoling LA, Bahr A, Bååth E (2008) Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol Ecol 63(3):350–358. https://doi.org/10.1111/j.1574-6941.2008.00440.x
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85(3):591–602. https://doi.org/10.1890/03-8002
Sardar MF, Zhu C, Bing G, Ahmad HR, Song T, Li H (2021a) The fate of antibiotic resistance genes in cow manure composting: shaped by temperature-controlled composting stages. Biores Technol 320:124403. https://doi.org/10.1016/j.biortech.2020.124403
Sardar MF, Li H, Zhu C, Dar AA, Zhang B, Waqas MA (2021b) Differential effects of sulfamethoxazole concentrations on the enzymatic dynamics of aerobic composting. Biores Technol 336:125330. https://doi.org/10.1016/j.biortech.2021.125330
Ullah MR, Carrillo Y, Dijkstra FA (2021) Biocides provide a source of carbon and nitrogen directly to surviving microbes and indirectly through a pulse in microbial necromass. Appl Soil Ecol 160:103862. https://doi.org/10.1016/j.apsoil.2020.103862
Ullah MR, Dijkstra FA (2019) Fungicide and bactericide effects on carbon and nitrogen cycling in soils: a meta-analysis. Soil Systems 3(2):23. https://doi.org/10.3390/soilsystems3020023
Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7(3):737–750. https://doi.org/10.1890/1051-0761(1997)007[0737:HAOTGN]2.0.CO;2
Wang CH, Wang NN, Zhu JX, Liu Y, Xu XF, Niu SL, Yu GR, Han XG, He NP (2018) Soil gross N ammonification and nitrification from tropical to temperate forests in eastern China. Funct Ecol 32(1):83–94. https://doi.org/10.1111/1365-2435.13024
Wang CH, Wan SQ, Xing XR, Zhang L, Han XG (2006) Temperature and soil moisture interactively affected soil net N mineralization in temperate grassland in Northern China. Soil Biol Biochem 38(5):1101–1110. https://doi.org/10.1016/j.soilbio.2005.09.009
Wang J, Liu Q, Zhang JB, Cai ZC (2015) Conversion of forest to agricultural land affects the relative contribution of bacteria and fungi to nitrification in humid subtropical soils. Acta Agriculturae Scandinavica, Section B-Soil & Plant Science 65(1):83–88. https://doi.org/10.1080/09064710.2014.967714
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a Guide to Methods and Applications 18(1):315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
World Reference Base for Soil Resources (WRB) (2014) A framework for international classification, correlation and communication. Food and Agriculture Organization of the United Nations, Rome
Xiao HF, Feng YL, Schaefer DA, Yang XD (2014) Soil fungi rather than bacteria were modified by invasive plants, and that benefited invasive plant growth. Plant Soil 378(1):253–264. https://doi.org/10.1007/s11104-014-2040-x
Xu QF, Jiang PK, Wu JS, Zhou GM, Shen RF, Fuhrmann JJ (2015) Bamboo invasion of native broadleaf forest modified soil microbial communities and diversity. Biol Invasions 17(1):433–444. https://doi.org/10.1007/s10530-014-0741-y
Yuan HZ, Ge TD, Wu XH, Liu SL, Tong CL, Qin HL, Wu M, Wei WX, Wu JS (2012) Long-term field fertilization alters the diversity of autotrophic bacteria based on the ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large-subunit genes in paddy soil. Appl Microbiol Biotechnol 95(4):1061–1071. https://doi.org/10.1007/s00253-011-3760-y
Yang W, Zhang D, Cai XW, Xia L, Luo YQ, Cheng XL, An SQ (2019) Significant alterations in soil fungal communities along a chronosequence of Spartina alterniflora invasion in a Chinese Yellow Sea coastal wetland. Sci Total Environ 693:133548. https://doi.org/10.1016/j.scitotenv.2019.07.354
Yen TM, Lee JS (2011) Comparing aboveground carbon sequestration between Moso bamboo (Phyllostachys heterocycla) and China fir (Cunninghamia lanceolata) forests based on the allometric model. For Ecol Manage 261(6):995–1002. https://doi.org/10.1016/j.foreco.2010.12.015
Yu X, Dijkstra FA (2020) Carbon and nitrogen dynamics affected by litter and nitrogen addition in a grassland soil: role of fungi. Eur J Soil Biol 100:103211. https://doi.org/10.1016/j.ejsobi.2020.103211
Zhang JJ, Li YF, Chang SX, Jiang PK, Zhou GM, Liu J, Wu JS, Shen ZM (2014) Understory vegetation management affected greenhouse gas emissions and labile organic carbon pools in an intensively managed Chinese chestnut plantation. Plant Soil 376(1):363–375. https://doi.org/10.1007/s11104-013-1996-2
Zhang Y, Wang J, Dai SY, Zhao J, Huang XQ, Sun YQ, Chen J, Cai ZC, Zhang JB (2019) The effect of C: N ratio on heterotrophic nitrification in acidic soils. Soil Biol Biochem 137:107562. https://doi.org/10.1016/j.soilbio.2019.107562
Zou N, Huang L, Chen HJ, Huang XF, Song QN, Yang QP, Wang TC (2020a) Nitrogen form plays an important role in the growth of moso bamboo (Phyllostachys edulis) seedlings. PeerJ 8:e9938. https://doi.org/10.7717/peerj.9938
Zou N, Shi WM, Hou LH, Kronzucker HJ, Huang L, Gu HM, Yang QP, Deng GH, Yang GY (2020b) Superior growth, N uptake and NH4+ tolerance in the giant bamboo Phyllostachys edulis over the broad-leaved tree Castanopsis fargesii at elevated NH4+ may underlie community succession and favor the expansion of bamboo. Tree Physiol 40(11):1606–1622. https://doi.org/10.1093/treephys/tpaa086
Zuo YW, Qu HH, Xia CY, Zhang H, Zhang JH, Deng HP (2022) Moso bamboo invasion reshapes community structure of denitrifying bacteria in rhizosphere of Alsophila spinulosa. Microorganisms 10(1):180. https://doi.org/10.3390/microorganisms10010180
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This work was financially supported by National Natural Science Foundation of China (32071742, 31670618) and Natural Science Foundation of Zhejiang Province, China (LZ22C160005).
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Miao, D., Peng, X., Teng, Q. et al. Different contributions of bacterial and fungal communities to nitrogen mineralization in Moso bamboo-invaded subtropical forests. J Soils Sediments 23, 1123–1134 (2023). https://doi.org/10.1007/s11368-022-03380-z
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DOI: https://doi.org/10.1007/s11368-022-03380-z