Abstract
Purpose
The invasive weed common ragweed (Ambrosia artemisiifolia [L.]) has become notorious in China as a major weed in agriculture. Soil microbial communities play important roles in invasive plant growth by potentially mediating nutrient cycling in soil. However, knowledge regarding the soil microbial communities in common ragweed remains limited.
Methods
In this study, a long-term field experiment was conducted to comparatively study the microbial community compositions in the rhizosphere soil of invasive common ragweed and two native plants, Chenopodium serotinum and Setaria viridis.
Results
We found that the bacterial and fungal community compositions differed significantly between common ragweed and two native plants. Invasion by common ragweed selectively accumulated microorganisms, such as Exopiala, RB41, Cnuella, Dinghuibacter and Funneliformis, that can enhance carbon and nitrogen cycling and the absorption of phosphorus in the rhizosphere environment. Moreover, the relative abundances of these microorganisms were significantly related to the soil pH and ammonium contents. Furthermore, we found that microbial inoculants from rhizosphere of common ragweed promote growth of both common ragweed and S. viridis.
Conclusions
Our results show that common ragweed constructs a unique rhizosphere microbial community that distinguishes it from local plants, which could contribute to its growth and expansion by providing a stronger ability to use carbon, nitrogen, and phosphorus. This study offers fundamental explanation to explain how the underground microbial community facilitate the invasion of common ragweed on an ecosystem-level.
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References
Aulakh M (2001) Characterization of root exudates at different growth stages of ten Rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148
Badri DV, Vivanco JM (2010) Regulation and function of root exudates. Plant Cell Environ 32:666–681
Bazzaz AF (1979) The physiological ecology of plant succession. Ann Rev Ecol System 10:351–371
Belova SE, Ravin NV, Pankratov TA, Rakitin AL, Ivanova AA, Beletsky AV, Mardanov AV, Sinninghe Damsté JS, Dedysh SN (2018) Hydrolytic capabilities as a key to environmental success: Chitinolytic and cellulolytic Acidobacteria from acidic sub-arctic soils and boreal peatlands. Front Microbiol 9:2775
Berendsen RL, Pieterse C, Bakker P (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Berthelot C, Blaudez D, Beguiristain T, Chalot M, Leyval C (2018) Co-inoculation of Lolium perenne with Funneliformis mosseae and the dark septate endophyte Cadophora sp. in a trace element-polluted soil. Mycorrhiza 28:301–314
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143
Coats VC, Rumpho ME (2014) The rhizosphere microbiota of plant invaders: an overview of recent advances in the m crobiomics of invasive plants. Front Microbiol 5:ARTN 368. https://doi.org/10.3389/fmicb.2014.00368
Crowley DE, Rengel Z, Rengel Z (1999) Biology andchemistry of nutrient availability in the rhizosphere. Biology and chemistry of nutrient availability in therhizosphere. Mineral nutrition of crops: fundamentalmechanisms and implications 12:1–40
Das S, Nurunnabi R, Parveen R, Mou AN, Rahman (2019) Isolation and characterization of indole acetic acid producing Bacteria from rhizosphere soil and their effect on seed germination. Int J Curr Microbiol App Sci 8:1237–1245
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Eichorst SA, Trojan D, Roux S, Herbold C, Rattei T, Woebken D (2018) Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments. Environ Microbiol 20:1041–1063
Eisenhauer N, Lanoue A, Strecker T, Scheu S, Steinauer K, Thakur MP, Mommer L (2017) Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci Rep-Uk 7:44641
Eivazi F, Tabatabai MA (1977) Phosphatases in soils. Soil Biol Biochem 9:167–172
Fu Y, Kumar A, Chen L, Jiang Y, Xu J (2021) Rhizosphere microbiome modulated effects of biochar on ryegrass 15N uptake and rhizodeposited 13C allocation in soil. Plant Soil 463:359–377
Gui H, Witoon P, Hyde KD, Xu J, Mortimer PE (2017) The arbuscular mycorrhizal fungus Funneliformis mosseae alters bacterial communities in subtropical Forest soils during litter decomposition. Front Microbiol 8:1120
Hao C, Dungait JA, Wei X, Ge T, Kuzyakov Y, Cui Z, Tian J, Zhang F (2022) Maize root exudate composition alters rhizosphere bacterial community to control hotspots of hydrolase activity in response to nitrogen supply. Soil Biol Biochem 170:108717
Herbien S, Neal J (1990) Soil pH and phosphatase activity. Commun Soil Sci Plan 21:439–456
Hu J, Wei Z, Kowalchuk GA, Xu Y, Shen Q, Jousset A (2020) Rhizosphere microbiome functional diversity and pathogen invasion resistance build up during plant development. Environ Microbiol 22:5005–5018
Huang X-F, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92:267–275
Im WT, Choi KD, Siddiqi MZ, Shafi SM (2016) Compostibacter hankyongensis gen. Nov., sp. nov., isolated from compost. Int J Syst Evol Micr 66:3681
Knapp TR (1978) Canonical correlation analysis: a general parametric significance-testing system. Psychol Bull 85:410
Kong L, Chen X, Yerger EH, Li Q, Chen F, Xu H, Zhang F (2022) Arbuscular mycorrhizal fungi enhance the growth of the exotic species Ambrosia artemisiifolia. J Plant Ecol 15:581–595
Kruskal JB (1964) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115–129
Li Q, Xiang P, Zhang T, Wu Q, Bao Z, Tu W, Li L, Zhao C (2022) The effect of phosphate mining activities on rhizosphere bacterial communities of surrounding vegetables and crops. Sci Total Environ 821:153479
Lu R (1999) Analyse methods of soil and agrochemistry. Soil Science Society of China Chinese Agricultural Science and Technology Press, Beijing (in Chinese)
Lv YY, Wang J, Chen M-H, You J, Qiu L-H (2016) Dinghuibacter silviterrae gen. nov., sp nov., isolated from forest soil. Int J Syst Evol Micr 66:1785–1791
Marisavljevic D, Cakmak D, Pavlovic D, Dolovac EP, Radivojevic L (2012) Preliminary examination of the adoption of various forms of nitrogen in the early growth stages of ragweed https://www.researchgate.net/publication/335942218_Preliminary_examination_of_the_adoption_of_various_forms_of_nitrogen_in_the_early_growth_stages_of_ragweed
Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663
Miethling R, Wieland G, Tebbe HBC (2000) Variation of microbial rhizosphere communities in response to crop species, soil origin, and inoculation with Sinorhizobium meliloti L33. Microbial Ecol 40:43–56
Mitich LW (1996) Ragweeds (Ambrosia spp.)—the hay fever weeds. Weed Technol 10:236–240
Mushinski RM, Zhou Y, Gentry TJ, Boutton TW (2018) Bacterial metataxonomic profile and putative functional behavior associated with C and N cycle processes remain altered for decades after forest harvest. Soil Biol Biochem 119:184–193
Nadira UA, Ahmed IM, Wu F, Zhang G (2016) The regulation of root growth in response to phosphorus deficiency mediated by phytohormones in a Tibetan wild barley accession. Acta Physiol Plant 38:1–11
Ozaslan C, Onen H, Farooq S, Gunal H, Akyol N (2016) Common ragweed: an emerging threat for sunflower production and human health in Turkey. Weed Biology and Management 16:42–55
Qian L, Yu WJ, Cui JQ, Jie WG, Cai BY (2015) Funneliformis mosseae affects the root rot pathogen fusarium oxysporum in soybeans. Acta Agric Scand 65:321–328
Qu Q, Zhang Z, Peijnenburg W, Liu W, Qian H (2020) Rhizosphere microbiome assembly and its impact on plant growth. J Agr Food Chem 68:5024–5038
Richard J, Manuela P, Antonella S, Anna K, Stanislav K (2017) The role of soil microorganisms in plant mineral nutrition—current knowledge and future directions. Frontiers in Plant ence 8:1617
Sasse J, Martinoia E, Northen T (2018) Feed your friends: do Plant exudates shape the root microbiome? - ScienceDirect. Trends Plant Sci 23:25–41
Schüâler A, Walker C (2010) The Glomeromycota, a species list with new families and new genera. The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University. www.amf-phylogeny.com
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
Sun J, Yang L, Wei J, Quan J, Yang X (2020) The responses of soil bacterial communities and enzyme activities to the edaphic properties of coal mining areas in Central China. PLoS One 15:e0231198
Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. International Journal of Systematic & Evolutionary Microbiology 51:1405–1417
Tourna M, Stieglmeier M, Spang A, Kdnneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A (2011) Nitrososphaera viennensis an ammonia oxidizing archaeon from soil. P Natl Acad Sci USA 108:8420–8425
Wang ML, Tang XF, Sun XQ, Jia BB, Xu H, Jiang S, Siemann E, Lu XM (2021) An invasive plant rapidly increased the similarity of soil fungal pathogen communities. Ann Bot-London 127:327–336. https://doi.org/10.1093/aob/mcaa191
Ward NL, Challacombe JF, Janssen PH, Henrissat B, Kuske CR (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microb 75:2046–2056
Williams A, Vries FTD (2020) Plant root exudation under drought: implications for ecosystem functioning. New Phytol 225:1899–1905
Xu R, Li T, Shen M, Yang ZL, Zhao ZW (2020) Evidence for a dark septate endophyte ( Exophiala Pisciphila , H93) enhancing phosphorus absorption by maize seedlings. Plant Soil 452:249–266
Zeng K, Zhu YQ, Liu JX (2010) Research progress on ragweed (Ambrosia). Acta Pratacul Sin 19:212–219
Zhang F, Li Q, Yerger EH, Chen X, Shi Q, Wan F (2018) AM fungi facilitate the competitive growth of two invasive plant species, Ambrosia artemisiifolia and Bidens pilosa. Mycorrhiza 28:703–715. https://doi.org/10.1007/s00572-018-0866-4
Zhang J, Zhou D, Yuan X, Xu Y, Chen C, Zhao L (2022) Soil microbiome and metabolome analysis reveals beneficial effects of ginseng–celandine rotation on the rhizosphere soil of ginseng-used fields. Rhizosphere-Neth 23:100559
Zhang F, Sun J, Wang C, Li C, Chen F, Xu H, Chen X (2023) Bacillus benefits the competitive growth ofAmbrosia artemisiifolia by increasing availablenutrient levels. Front Plant Sci 13:1069016
Zhao M, Sun B, Wu L, Gao Q, Wang F, Wen C, Wang M, Liang Y, Hale L, Zhou J (2016) Zonal soil type determines soil microbial responses to maize cropping and fertilization. MSystems 1:e00075–e00016
Acknowledgements
We would like to thank Daliang Ning for assistance on R codes. This research was supported by grants to Mengxin Zhao by the National Key R&D Program of China (2021YFC2600400, 2021YFD1400100), and by National Science Foundation of China (42207162).
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WL and MZ developed the study concept and design. QL collected the samples. HZ performed data analyses and drafted the initial manuscript. JG guided the feedback experiment design. WS, JG, WL, and MZ revised the manuscript. All authors read and approved the final manuscript.
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Zhang, H., Li, Q., Sun, W. et al. Microbial communities in the rhizosphere soil of Ambrosia artemisiifolia facilitate its growth. Plant Soil 492, 353–365 (2023). https://doi.org/10.1007/s11104-023-06181-6
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DOI: https://doi.org/10.1007/s11104-023-06181-6