Abstract
Aims
Exotic plant invasion often drives soil microorganisms to affect soil organic carbon (SOC), whereas microbial taxa that played a key role in the SOC changes and the related mechanisms remain unclear.
Methods
In this study, a long-term simulation of the invasion process of exotic plants, Ambrosia artemisiifolia and Bidens pilosa, was carried out to evaluate the relationships between soil microorganisms and SOC during the invasion of exotic plants. A metagenomic method was conducted to study the microbial communities and carbon metabolic pathways in the rhizosphere soil.
Results
Our results showed that the invasion of two exotic plants significantly increased the concentrations of soil microbial biomass carbon (MBC) and SOC by shifting carbon metabolic pathways mediated by key microbial taxa. The dominant carbon metabolic pathways were transformed into the tricarboxylic acid cycle, glyoxylate and dicarboxylate metabolism, and dicarboxylate-hydroxybutyrate cycle in the rhizosphere soil of two exotic species after long-time interaction, and these three pathways were closely correlated to Bradyrhizobium, Mycobacterium, and Sphingomonas. The structural equation model revealed that the invasion of A. artemisiifolia and B. pilosa were more likely to affect the SOC via affecting MBC concentration rather than directly affecting SOC, suggesting MBC played a key role in SOC accumulation in the exotic plant’s rhizosphere.
Conclusions
The similar microbial mechanism of SOC in two exotic species, suggests that exotic plant invasion may affect the SOC cycle by adjusting soil microbiota and microbial metabolic activities.
This is a preview of subscription content, log in via an institution to check access.
Data availability
The data in this study is metagenomic data, which has been submitted to the NCBI. The bioproject accession number is PRJNA899702.
References
Ajanaku CO, Echeme JO, MordI RC, Ajani OO, Okere DU, Kayode YAA (2019) Antimicrobial and GC-MS analyses of stem and root extracts of Bidens pilosa linn. Orient J Chem 35(2):1–10. https://doi.org/10.13005/ojc/350247
Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8(2):217–230. https://doi.org/10.1007/s10530-004-3856-8
Bhagwath SG (1997) Optimization and scale-up of thiarubrine a production from hairy root cultures of Ambrosia artemisiifolia. Louisiana State University and Agricultural & Mechanical College
Castro-Díez P, Alonso Á, Romero-Blanco A (2019) Effects of litter mixing on litter decomposition and soil properties along simulated invasion gradients of non-native trees. Plant Soil 442(1–2):79–96. https://doi.org/10.1007/s11104-019-04160-4
Chen L, Liu L, Qin S, Yang G, Fang K, Zhu B, Kuzyakov Y, Chen P, Xu Y, Yang Y (2019) Regulation of priming effect by soil organic matter stability over a broad geographic scale. Nat Commun 10(1):5112. https://doi.org/10.1038/s41467-019-13119-z
Cheng C, Liu Z, Zhang Y, He Q, Li B, Wu J (2022) Leaf litter decomposition and its drivers differ between an invasive and a native plant: Management implications. Ecol Appl 34(1):e2739. https://doi.org/10.1002/eap.2739
Chung HH, Ting HM, Wang WH, Chao YT, Hsieh CH, Maria KA, Sung YC, Lin SS, Hu FY, Shyur LF (2021) Elucidation of enzymes involved in the biosynthetic pathway of bioactive polyacetylenes in Bidens pilosa using integrated omics approaches. J Exp Bot 72:525–541. https://doi.org/10.1093/jxb/eraa457
Cui QG, He WM (2009) Soil biota, but not soil nutrients, facilitate the invasion of Bidens pilosa relative to a native species Saussurea deltoidea. Weed Res 49(2):201–206. https://doi.org/10.1111/j.1365-3180.2008.00679.x
Ferencz E, Spengler G, Zupkó I, Vollár M, Zomborszki ZP, Kúsz N, Hohmann J, Kovács B, Csupor D, Laczkó-Zöld E, Csupor-Löffler B (2023) Isolation of compounds from the roots of Ambrosia artemisiifolia and their effects on human cancer cell lines. Zeitschrift Für Naturforschung C 78:299–305. https://doi.org/10.1515/znc-2022-0239
Gao GF, Peng D, Zhang Y, Li Y, Fan K, Tripathi BM, Adams JM, Chu H (2021) Dramatic change of bacterial assembly process and co-occurrence pattern in Spartina alterniflora salt marsh along an inundation frequency gradient. Sci Total Environ 755:142546. https://doi.org/10.1016/j.scitotenv.2020.142546
He Y, Zhou X, Cheng W, Zhou L, Zhang G, Zhou G, Liu R, Shao J, Zhu K, Cheng W (2018) Linking improvement of soil structure to soil carbon storage following invasion by a C4 plant Spartina alterniflora. Ecosystems 22(4):859–872. https://doi.org/10.1007/s10021-018-0308-3
He Z, Deng Y, Xu M, Li J, Liang J, **ong J, Yu H, Wu B, Wu L, Xue K, Shi S, Carrillo Y, Van Nostrand JD, Hobbie SE, Reich PB, Schadt CW, Kent AD, Pendall E, Wallenstein M, Luo Y, Yan Q, Zhou J (2020) Microbial functional genes commonly respond to elevated carbon dioxide. Environ Int 144:106068. https://doi.org/10.1016/j.envint.2020.106068
Huang Q, Huang Y, Wang B, Dippold MA, Li H, Li N, Jia P, Zhang H, An S, Kuzyakov Y (2022) Metabolic pathways of CO2 fixing microorganisms determined C-fixation rates in grassland soils along the precipitation gradient. Soil Biol Biochem 172:108764. https://doi.org/10.1016/j.soilbio.2022.108764
Inderjit SD, Kaur H, Kalisz S, Bezemer TM (2021) Novel chemicals engender myriad invasion mechanisms. New Phytol 232(3):1184–1200. https://doi.org/10.1111/nph.17685
Jiang HM, Jiang JP, Jia Y, Li FM, Xu JZ (2006) Soil carbon pool and effects of soil fertility in seeded alfalfa fields on the semi-arid Loess Plateau in China. Soil Biol Biochem 38(8):2350–2358. https://doi.org/10.1016/j.soilbio.2006.02.008
Kato-Noguchi H, Kurniadie D (2024) The invasive mechanisms of the noxious alien plant species Bidens pilosa. Plants 13:356. https://doi.org/10.3390/plants13030356
Lankau RA (2011) Intraspecific variation in allelochemistry determines an invasive species’ impact on soil microbial communities. Oecologia 165(2):453–463. https://doi.org/10.1007/s00442-010-1736-8
Li J, Yuan X, Ge L, Li Q, Li Z, Wang L, Liu Y (2020) Rhizosphere effects promote soil aggregate stability and associated organic carbon sequestration in rocky areas of desertification. Agr Ecosyst Environ 304(304):107126. https://doi.org/10.1016/j.agee.2020.107126
Li J, Wang C, Liang W, Liu S (2021) Rhizosphere microbiome: The emerging barrier in plant-pathogen interactions. Front Microbiol 12:772420. https://doi.org/10.3389/fmicb.2021.772420
Li S, **e D, Ge X, Dong W, Luan J (2022) Altered diversity and functioning of soil and root-associated microbiomes by an invasive native plant. Plant Soil 473(1–2):235–249. https://doi.org/10.1007/s11104-022-05338-z
Liang C, Kästner M, Joergensen RG (2020) Microbial necromass on the rise: the growing focus on its role in soil organic matter development. Soil Biol Biochem 150:108000. https://doi.org/10.1016/j.soilbio.2020.108000
Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: A meta-analysis. New Phytol 177(3):706–714. https://doi.org/10.1111/j.1469-8137.2007.02290.x
Liu X, Qi C, Quan Q (2016) Effect of invasive plants Ambrosia artemisiifolia L. on soil carbon and nitrogen transition. Acta Agric Zhejiangensis 28:297–301. https://doi.org/10.3969/j.issn.1004-1524.2016.02.19
Liu Z, Sun Y, Zhang Y, Feng W, Lai Z, Fa K, Qin S (2018) Metagenomic and 13C tracing evidence for autotrophic atmospheric carbon absorption in a semiarid desert. Soil Biol Biochem 125:156–166. https://doi.org/10.1016/j.soilbio.2018.07.012
Liu ZX, Zhang N, Ma A, Zhang T, Li X, Tian G, Feng YL, An T (2022) Sesquiterpenes from Ambrosia artemisiifolia and their allelopathy. Front Plant Sci 13:996498. https://doi.org/10.3389/fpls.2022.996498
Liu Q, Tang L, Sun H, Kong X, Wu W, Li S, Shen Y (2024) Responses of the fungal-bacterial community and network to surface mulching and nitrogen fertilization in the Loess Plateau. Plant Soil 494(1):111–126. https://doi.org/10.1007/s11104-023-06260-8
Lorenz M, Hofmann D, Steffen B, Fischer K, Thiele-Bruhn S (2021) The molecular composition of extractable soil microbial compounds and their contribution to soil organic matter vary with soil depth and tree species. Sci Total Environ 781:146732. https://doi.org/10.1016/j.scitotenv.2021.146732
Makoto K, Bryanin SV, Lisovsky VV, Kushida K, Wada N (2015) Dwarf pine invasion in an alpine tundra of discontinuous permafrost area: effects on fine root and soil carbon dynamics. Trees 30(2):431–439. https://doi.org/10.1007/s00468-015-1192-5
McLeod ML, Bullington L, Cleveland CC, Rousk J, Lekberg Y (2021) Invasive plant-derived dissolved organic matter alters microbial communities and carbon cycling in soils. Soil Biol Biochem 156:108–191. https://doi.org/10.1016/j.soilbio.2021.108191
Meisner A, Gera Hol WH, de Boer W, Krumins JA, Wardle DA, van der Putten WH (2014) Plant-soil feedbacks of exotic plant species across life forms: A meta-analysis. Biol Invasions 16(12):2551–2561. https://doi.org/10.1007/s10530-014-0685-2
Mitchell A, Romano GH, Groisman B, Yona A, Dekel E, Kupiec M, Dahan O, Pilpel Y (2009) Adaptive prediction of environmental changes by microorganisms. Nature 460(7252):220–224. https://doi.org/10.1038/nature08112
Patoine G, Eisenhauer N, Cesarz S, Phillips HRP, Xu X, Zhang L, Guerra CA (2022) Drivers and trends of global soil microbial carbon over two decades. Nat Commun 13(1):4195. https://doi.org/10.1038/s41467-022-31833-z
Peter A, Zlabur JS, Suric J, Voca S, Purgar DD, Pezo L, Voca N (2021) Invasive plant species biomass-evaluation of functional value. Molecules 26(13):3814. https://doi.org/10.3390/molecules26133814
Probst AJ, Castelle CJ, Singh A, Brown CT, Anantharaman K, Sharon I, Hug LA, Burstein D, Emerson JB, Thomas BC, Banfield JF (2017) Genomic resolution of a cold subsurface aquifer community provides metabolic insights for novel microbes adapted to high CO2 concentrations. Environ Microbiol 19(2):459–474. https://doi.org/10.1111/1462-2920.13362
Quevauviller P (1998) Operationally defined extraction procedures for soil and sediment analysis I. Standardization. Trends Anal Chem 17(5):289–298
Ren M, Zhang Z, Wang X, Zhou Z, Chen D, Zeng H, Zhao S, Chen L, Hu Y, Zhang C, Liang Y, She Q, Zhang Y, Peng N (2018) Diversity and contributions to nitrogen cycling and carbon fixation of soil salinity shaped microbial communities in Tarim Basin. Front Microbiol 9:431. https://doi.org/10.3389/fmicb.2018.00431
Rodríguez-Caballero G, Roldán A, Caravaca F (2020) Invasive Nicotiana glauca shifts the soil microbial community composition and functioning of harsh and disturbed semiarid Mediterranean environments. Biol Invasions 22(10):2923–2940. https://doi.org/10.1007/s10530-020-02299-1
Shang CQ, Zhu XZ (2019) Invasion mechanisms, control and utilization of alien plant species Bidens pilosa. Pratacultural science 36:47–60. https://doi.org/10.11829/j.issn.1001-0629.2018-0136
Smercina DN, Bailey VL, Hofmockel KS (2021) Micro on a macroscale: relating microbial-scale soil processes to global ecosystem function. Fems Microbiol Ecol 97(7):091. https://doi.org/10.1093/femsec/fiab091
Smith M, Cecchi L, Skjoth CA, Karrer G, Sikoparija B (2013) Common ragweed: a threat to environmental health in Europe. Environ Int 61:115–126. https://doi.org/10.1016/j.envint.2013.08.005
Stanek M, Kushwaha P, Murawska-Wlodarczyk K, Stefanowicz AM, Babst-Kostecka A (2023) Quercus rubra invasion of temperate deciduous forest stands alters the structure and functions of the soil microbiome. Geoderma 430:116328. https://doi.org/10.1016/j.geoderma.2023.116328
Stone BW, Li J, Koch BJ, Blazewicz SJ, Dijkstra P, Hayer M, Hofmockel KS, Liu XA, Mau RL, Morrissey EM, Pett-Ridge J, Schwartz E, Hungate BA (2021) Author Correction: Nutrients cause consolidation of soil carbon flux to small proportion of bacterial community. Nat Commun 12(1):4052. https://doi.org/10.1038/s41467-021-24314-2
Sun C, Li Q, Han L, Chen X, Zhang F (2022) The effects of allelochemicals from root exudates of Flaveria bidentis on two Bacillus species. Front Plant Sci 13:1001208. https://doi.org/10.3389/fpls.2022.1001208
Theuerl S, Buscot F (2010) Laccases: toward disentangling their diversity and functions in relation to soil organic matter cycling. Biol Fert Soils 46(3):215–225. https://doi.org/10.1007/s00374-010-0440-5
Tian XK, Wang MY, Meng P, Zhang JS, Zhou BZ, Ge XG, Yu FH, Li MH (2020) Native Bamboo invasions into subtropical forests alter microbial communities in litter and soil. Forests 11(3):314. https://doi.org/10.3390/f11030314
Tran PQ, Bachand SC, McIntyre PB, Kraemer BM, Vadeboncoeur Y, Kimirei IA, Tamatamah R, McMahon KD, Anantharaman K (2021) Depth-discrete metagenomics reveals the roles of microbes in biogeochemical cycling in the tropical freshwater Lake Tanganyika. ISME 15(7):1971–1986. https://doi.org/10.1038/s41396-021-00898-x
Wang Q, Zhang Q, Han Y, Zhang D, Zhang C, Hu C (2022) Carbon cycle in the microbial ecosystems of biological soil crusts. Soil Biol Biochem 171:108–729. https://doi.org/10.1016/j.soilbio.2022.108729
Wong HL, MacLeod FI, White RA 3rd, Visscher PT, Burns BP (2020) Microbial dark matter filling the niche in hypersaline microbial mats. Microbiome 8:135. https://doi.org/10.1186/s40168-020-00910-0
**ang J, Liu D, Ding W, Yuan J, Lin Y (2015) Invasion chronosequence of Spartina alterniflora on methane emission and organic carbon sequestration in a coastal salt marsh. Atmos Environ 112:72–80. https://doi.org/10.1016/j.atmosenv.2015.04.035
**ao KQ, Ge TD, Wu XH, Peacock CL, Zhu ZK, Peng J, Bao P, Wu JS, Zhu YG (2021) Metagenomic and 14C tracing evidence for autotrophic microbial CO2 fixation in paddy soils. Environ Microbiol 23(2):924–933. https://doi.org/10.1111/1462-2920.15204
Xu X, Schimel JP, Thornton PE, Song X, Yuan F, Goswami S (2014) Substrate and environmental controls on microbial assimilation of soil organic carbon: a framework for Earth system models. Ecol Lett 17(5):547–555. https://doi.org/10.1111/ele.12254
Xu H, Liu Q, Wang S, Yang G, Xue S (2022) A global meta-analysis of the impacts of exotic plant species invasion on plant diversity and soil properties. Sci Total Environ 810:152286. https://doi.org/10.1016/j.scitotenv.2021.152286
Xun W, Liu Y, Li W, Ren Y, **ong W, Xu Z, Zhang N, Miao Y, Shen Q, Zhang R (2021) Specialized metabolic functions of keystone taxa sustain soil microbiome stability. Microbiome 9(1):35. https://doi.org/10.1186/s40168-020-00985-9
Yan J, Zhang X, Chen X, Wang Y, Zhang F, Wan F (2016) Effects of rhizosphere soil microorganisms and soil nutrients on competitiveness of Bidens pilosa with different native plants. Biodiversity Science 24(12):1381–1389. https://doi.org/10.17520/biods.2015365
Yan J, Wang L, Hu Y, Tsang YF, Zhang Y, Wu J, Fu X, Sun Y (2018) Plant litter composition selects different soil microbial structures and in turn drives different litter decomposition pattern and soil carbon sequestration capability. Geoderma 319:194–203. https://doi.org/10.1016/j.geoderma.2018.01.009
Yuan J, Liu D, Ji Y, **ang J, Lin Y, Wu M, Ding W, Bielefeld Nardoto G (2019) Spartina alterniflora invasion drastically increases methane production potential by shifting methanogenesis from hydrogenotrophic to methylotrophic pathway in a coastal marsh. J Ecol 107(5):2436–2450. https://doi.org/10.1111/1365-2745.13164
Zhang N, Liu W, Yang H, Yu X, Gutknecht JL, Zhang Z, Wan S, Ma K (2013) Soil microbial responses to warming and increased precipitation and their implications for ecosystem C cycling. Oecologia 173(3):1125–1142. https://doi.org/10.1007/s00442-013-2685-9
Zhang P, Nie M, Li B, Wu J (2017) The transfer and allocation of newly fixed C by invasive Spartina alterniflora and native Phragmites australis to soil microbiota. Soil Biol Biochem 113:231–239. https://doi.org/10.1016/j.soilbio.2017.06.003
Zhang G, Bai J, Jia J, Wang W, Wang X, Zhao Q, Lu Q (2019) Shifts of soil microbial community composition along a short-term invasion chronosequence of Spartina alterniflora in a Chinese estuary. Sci Total Environ 657:222–233. https://doi.org/10.1016/j.scitotenv.2018.12.061
Zhang P, Li B, Wu J, Hu S (2019) Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta-analysis. Ecol Lett 22(1):200–210. https://doi.org/10.1111/ele.13181
Zhang CB, Liu WL, Luo B, Guan M, Wang J, Ge Y, Chang J (2020) Spartina alterniflora invasion impacts denitrifying community diversity and functioning in marsh soils. Geoderma 375:114456. https://doi.org/10.1016/j.geoderma.2020.114456
Zhang H, Li Q, Sun W, Guo J, Liu W, Zhao M (2023) Microbial communities in the rhizosphere soil of Ambrosia artemisiifolia facilitate its growth. Plant Soil 492(1–2):353–365. https://doi.org/10.1007/s11104-023-06181-6
Zhao K, Kong W, Wang F, Long XE, Guo C, Yue L, Yao H, Dong X (2018) Desert and steppe soils exhibit lower autotrophic microbial abundance but higher atmospheric CO2 fixation capacity than meadow soils. Soil Biol Biochem 127:230–238. https://doi.org/10.1016/j.soilbio.2018.09.034
Zhou J, Sun T, Shi L, Kurganova I, Lopes de Gerenyu V, Kalinina O, Giani L, Kuzyakov Y (2023) Organic carbon accumulation and microbial activities in arable soils after abandonment: A chronosequence study. Geoderma 435:116496. https://doi.org/10.1016/j.geoderma.2023.116496
Acknowledgements
This research was funded by the National Key Research and Development Plan (grant no. 2022YFC2601004), National Natural Science Foundation of China (grant nos. 31972343 and 32272562), and Hebei Natural Science Foundation (grant no. C2022201032).
Author information
Authors and Affiliations
Contributions
The Research was designed by Fengjuan Zhang. All analyses were performed by Chaofang Sun. The manuscript was written by Chaofang Sun with signifcant contributions from all co-authors.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Responsible Editor: Eric Paterson.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sun, C., Gu, J., Wu, C. et al. The shift of carbon metabolic pathways mediated by key rhizosphere microbes of exotic plants affects organic carbon. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06834-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11104-024-06834-0