Abstract
Aims
Late-successional trees have a relatively high growth rate at low temperature, which is important for their competitive advantage over mid-successional trees. However, we have a limited understanding of the underlying mechanism for such an advantage.
Methods
We transplanted two mid-successional tree seedlings (Castanopsis chinensis and Schima superba) and two late-successional species (Machilus chinensis and Cryptocarya chinensis) from Dinghushan (subtropical forest) to South China Normal University. The seedlings were incubated in pots with the same soil and routinely managed with regular watering and weeding. After 7 years of seedling culture, five pots of each tree species were selected for greenhouse cultivation to simulate the effect of low temperature (16 °C) on the studied tree species. A control treatment (ambient temperature) was also established.
Results
After 3 years, low temperatures changed the bacterial and diazotrophic communities, decreased the relative abundance of Actinobacteria in the mid-successional species Schima superba and Castanopsis chinensis, and increased the relative abundance of Rubrivivax in the late-successional species Machilus chinensis and Cryptocarya chinensis. In the low-temperature treatment, late-successional M. chinensis and Cryptocarya chinensis increased N fixation and net N mineralization rates compared with those in mid-successional S. superba and Castanopsis chinensis. Meanwhile, the relative abundance of the fungal community changed insignificantly, indicating that bacteria play a major regulatory role in nutrient cycling at low temperatures.
Conclusions
Our results suggest that shifts in the bacterial community and changes in functional group structures may play a key role in soil nitrogen cycling during the succession of evergreen broadleaf forest ecosystems at low temperatures during the dry season.
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Data availability
The data will be made available on request.
References
Adams MA, Polglase PJ, Attiwill PM, Weston CJ (1989) In situ studies of nitrogen mineralization and uptake in forest soils: some comments on methodology. Soil Biol Biochem 21:423–429
Ahlawat A, Jain V, Nainawatee HS (1998) Effect of low temperature and rhizospheric application of naringenin on pea-Rhizobium leguminosarum biovar viciae symbiosis. J Plant Biochem Biot 7:35–38
Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42
Andersen KM, Mayor JR, Turner BL (2017) Plasticity in nitrogen uptake among plant species with contrasting nutrient acquisition strategies in a tropical forest. Ecology 98:1388–1398
Bai J, Jia J, Huang C, Wang Q, Wang W, Zhang G, Cui B, Liu X (2017) Selective uptake of nitrogen by Suaeda salsa under drought and salt stresses and nitrogen fertilization using 15 N. Ecol Eng 102:542–545
Batterman SA, Hedin LO, van Breugel M, Ransijn J, Craven DJ, Hall JS (2013) Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502:224–227
Bojόrquez A, Martínez-Yrízar A, Alvarez-Yépiz JC (2021) A landscape assessment of frost damage in the northmost Neotropical dry forest. Agr Forest Meteorol 308–309:108562
Boubekri K, Soumare A, Mardad I, Lyamlouli K, Ouhdouch Y, Hafidi M, Kouisni L (2022) Multifunctional role of Actinobacteria in agricultural production sustainability: A review. Microbiol res 261:127059
Boyer JS (1982) Plant productivity and environment. Science 218:443–448
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583
Cavanaugh KC, Kellner JR, Forde AJ, Gruner DS, Parker JD, Rodriguez W, Feller IC (2013) Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events. P Natl Acad Sci USA 111:723–727
Chen L, Swenson NG, Ji NN, Mi XC, Ren HB, Guo LD, Ma KP (2019) Differential soil fungus accumulation and density dependence of trees in a subtropical forest. Science 366:124–128
Clements FE (1916) Plant succession: an analysis of the development of vegetation. Carnegie Institution of Washington Publishing, Washington
Fu X, Ma Y, Wang D, Zhan L, Guo Z, Fan K, Yang T, Chu H (2023) Long-term chemical fertilization results in a loss of temporal dynamics of diazotrophic communities in the wheat rhizosphere. Sci Total Environ 875:162663
Gremer JR, Kimball S, Angert AL, Venable DL, Huxman TE (2012) Variation in photosynthetic response to temperature in a guild of winter annual plants. Ecology 93:2693–2704
Hardy RW, Holsten R, Jackson E, Burns R (1968) The acetyleneethylene assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207
Hedley MJ, Stewart JWB, Chauhan BS (1982) Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–976
Hilliard JH, West SH (1970) Starch accumulation associated with growth reduction at low temperatures in a tropical plant. Science 168:494–496
Hou YP, Zhang MF, Liu SR, Sun PS, Yin LH, Yang TL, Li YD, Li Q, Wei XH (2018) The hydrological impact of extreme weather-induced forest disturbances in a tropical experimental watershed in South China. Forest 9:734
Huang JG, Guo X, Rossi S, Zhai L, Yu B, Zhang S, Zhang M (2018) Intra-annual wood formation of subtropical Chinese red pine shows better growth in dry season than wet season. Tree Physiol 38:1225–1236
Huang W, Zhang SB, Cao KF (2010) The different effects of chilling stress under moderate light intensity on photosystem II compared with photosystem I and subsequent recovery in tropical tree species. Photosynth Res 103:175–182
Jiang C, Ryu Y, Wang H, Keenan TF (2020) An optimality-based model explains seasonal variation in C3 plant photosynthetic capacity. Glob Chang Biol 26:6493–6510
Jiang S, Xing Y, Liu G, Hu C, Wang X, Yan G, Wang Q (2021) Changes in soil bacterial and fungal community composition and functional groups during the succession of boreal forests. Soil Biol Biochem 161:108393
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066
Li N, Chang R, Jiang H, Tariq A, Sardans J, Peñuelas J, Sun F, Zhou X (2022a) Combined livestock grazing-exclusion and global warming decreases nitrogen mineralization by changing soil microbial community in a Tibetan alpine meadow. Catena 219:106589
Li X, Luo X, Wang A, Chen W, Huang Q (2023) Control factors of soil diazotrophic community assembly and nitrogen fixation rate across eastern China. Geoderma 432:116410
Li X, Zhang YJ, Gao H, Ding T (2022b) Extreme cold wave in early November 2021 in China and the influences from the meridional pressure gradient over East Asia. Adv Clim Chang Res 13:797–802
Liu C, Gong X, Dang K, Li J, Yang P, Gao X, Deng X, Feng B (2020) Linkages between nutrient ratio and the microbial community in rhizosphere soil following fertilizer management. Environ Res 184:109261
Li SX, Wang ZH, Stewart BA (2013) Responses of crop plants to ammonium and nitrate N. Adv Agron 118:205–397
Liu Y, Evans SE, Friesen ML, Tiemann LK (2022) Root exudates shift how N mineralization and N fixation contribute to the plant-available N supply in low fertility soils. Soil Biology Biochem 165:108541
Liu YF, Qi MF, Li TL (2012) Photosynthesis, photoinhibition, and antioxidant system in tomato leaves stressed by low night temperature and their subsequent recovery. Plant Sci 196:8–17
Luo L, Zhao C, Zheng D, Wang E, Liang J, Yin C (2023) Nitrogen uptake preference and allocation in Populus cathayana in response to drought stress. Environ Exp Bot 213:105415
Macduff JH, Jackson SB (1991) Growth and preferences for ammonium or nitrate uptake by barley in relation to root termperature. J Exp Bot 42:521–530
Manucharova NA, Vlasenko AN, Stepanov AL (2007) Temperature as an autoecological factor of chitinolytic microbial complex formation in soils. Biol Bull 34:163–169
Meiners SJ, Cadotte MW, Fridley JD, Pickett STA, Walker LR, Thompson K (2015) Is successional research nearing its climax? New approaches for understanding dynamic communities. Funct Ecol 29:154–164
Menge Duncan NL, Levin Simon A, Hedin Lars O (2009) Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am Nat 174:465–477
Mesquita RdCG, Massoca PEdS, Jakovac CC, Bentos TV, Williamson GB (2015) Amazon rain forest succession: stochasticity or land-use legacy? Bioscience 65:849–861
Midolo G, De Frenne P, Holzel N, Wellstein C (2019) Global patterns of intraspecific leaf trait responses to elevation. Glob Chang Biol 25:2485–2498
Miller BD, Carter KR, Reed SC, Wood TE, Cavaleri MA (2021) Only sun-lit leaves of the uppermost canopy exceed both air temperature and photosynthetic thermal optima in a wet tropical forest. Agr Forest Meteorol 301–302:108347
Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol S 42:489–512
Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. Peer J 4:e2584
Wu X, Liu T, Zhang Y, Duan F, Neuhäuser B, Ludewig U, Schulze WX, Yuan L (2019) Ammonium and nitrate regulate NH4+ uptake activity of Arabidopsis ammonium transporter AtAMT1;3 via phosphorylation at multiple C-terminal sites. J Exp Bot 70:4919–4930
Wu X, Xing H, Wang X, Yang J, Chen J, Liu X, Dai D, Zhang M, Yang Q, Dong S, Liu Y (2023) Changes in soil microbial communities are linked to metal elements in a subtropical forest. Appl Soil Ecol 188:104919
Xiao D, He X, Xu Z, Bai SH, Zhang W, Hu P, Chen M, Wang K (2023) Strong cooperations among diazotroph and arbuscular mycorrhizal fungi taxa promote free-living nitrogen fixation at soil-rock mixing layer. Geoderma 437:116600
Yan JH, Zhang YP, Yu GR, Zhou GY, Zhang LM, Li K, Tan ZH, Sha LQ (2013) Seasonal and inter-annual variations in net ecosystem exchange of two old-growth forests in southern China. Agri Forest Meteorol 182–183:257–265
Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microb 77:4618–4625
Yu ZC, Lin W, Zheng XT, Chow WS, Luo YN, Cai ML, Peng CL (2020) The relationship between anthocyanin accumulation and photoprotection in young leaves of two dominant tree species in subtropical forests in different seasons. Photosynth Res 149:41–55
Yu ZC, Zheng XT, Lin W, Yan GZ, He W, Luo YN, Lin XL, Zhu H, Peng CL (2023) Differences in leaf photoprotection strategies of tree species at different successional stages in subtropical forests under seasonal climate change and their relationship to construction cost strategies. Environ Exp Bot 207:105230
Yu ZC, Lin W, Zheng XT, Cai ML, Zhang TJ, Luo YN, Peng CL (2021) Interpretation of the difference in shade tolerance of two subtropical forest tree species of different successional stages at the transcriptome and physiological levels. Tree Physiol 41:1669–1684
Zenova GM, Kozhevin PA, Manucharova NA, Dubrova MS, Zvyagintsev DG (2012) Temperature as a factor of development of psychrotolerant mycelial bacteria complexes in soils of north regions. Biol Bull 39:416–422
Zhang J, Zheng M, Zhang Y, Wang J, Shen H, Lin Y, Tang X, Hui D, Lambers H, Sardans J, Peñuelas J, Liu Z (2021) Soil phosphorus availability affects diazotroph communities during vegetation succession in lowland subtropical forests. Appl Soil Ecol 166:104009
Zhang S, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595–1602
Zheng M, Chen H, Li D, Luo Y, Mo J (2020) Substrate stoichiometry determines nitrogen fixation throughout succession in southern Chinese forests. Ecol Lett 23:336–347
Zhou G, Peng C, Li Y, Liu S, Zhang Q, Tang X, Liu J, Yan J, Zhang D, Chu G (2013) A climate change-induced threat to the ecological resilience of a subtropical monsoon evergreen broad-leaved forest in Southern China. Glob Chang Biol 19:1197–1210
Acknowledgements
This work was supported by the National Natural Science Foundation of China (32171493).
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CL Peng conceived the ideas and designed methodology; F Sun collected the data, analyzed the data and led the writing of the manuscript; W Lin collected the data, review & editing. All authors contributed critically to the drafts and gave final approval for publication.
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Sun, F., Lin, W., Deng, G. et al. Low temperature-mediated changes in soil free-living nitrogen fixation functional groups in tree species at different successional stages in subtropical forests. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06724-5
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DOI: https://doi.org/10.1007/s11104-024-06724-5