三叶鬼针草与狗尾草竞争改变了土壤微生物组成和土壤生态功能

doi:10.1016/j.jia.2023.07.025

摘要/Abstract

摘要：

三叶鬼针草（Bidens pilosa）是中国的主要入侵植物之一，其入侵给农业、林业、畜牧业和生物多样性造成了严重损失。土壤生态系统在外来植物入侵中起着重要作用。土壤微生物是植物与土壤生态功能之间的中介，对土壤酶活性和养分动态具有调节作用。了解入侵植物、土壤微生物和土壤生态过程之间的相互作用对管理和减轻入侵物种对环境的影响至关重要。本研究对三叶鬼针草和入侵地常见的本地伴生植物狗尾草(Setaria viridis)进行了系统分析。为了模拟三叶鬼针草的入侵过程，我们构建了三叶鬼针草和狗尾草分别单种和两者混合种植的同质园小区。分别采集了外来植物三叶鬼针草和本土植物狗尾草的根际土壤和非根际土壤。在本研究中，我们重点研究了三叶鬼针草成功入侵的土壤生态功能机制。为此我们分析了三叶鬼针草对土壤微生物群落组成和土壤生态功能的影响。结果表明，三叶鬼针草入侵使其生物量增加了27.51%，而狗尾草的生物量则显著降低了66.56%。三叶鬼针草根际和非根际土壤中的有机质含量为本地植物土壤中的1.30倍左右。三叶鬼针草根际土壤中TN和NO₃^-的含量是本地植物土壤中的1.30-2.71倍。三叶鬼针草根际土壤中酸性磷酸酶、碱性磷酸酶和脲酶的活性是本地植物的1.98-2.25倍。通过对16S rRNA基因的高通量测序，结果发现三叶鬼针草改变了土壤微生物群落的组成，具体而言，三叶鬼针草生长的土壤中富集了大量放线菌门（Actinobacteria）和变形菌门（Proteobacteria）的菌属。相关性分析结果显示这些属与土壤养分和酶活性显著正相关。植物生物量、土壤pH以及有机质、TN、NO₃^-、TP、AP、TK和AK的含量是影响土壤微生物群落的主要因素。本研究表明，三叶鬼针草入侵导致了土壤微生物群落组成的显著变化，这些变化与植物性状以及土壤理化性质的改变密切相关。三叶鬼针草入侵的土壤中富集了一些与碳氮磷循环相关的微生物。这些发现为外来植物成功入侵的“土壤-微生物反馈假说”提供了支持，同时也为土壤微生物促进三叶鬼针草成功入侵提供了生态学机制的新见解。总之，本研究有助于更好地理解入侵植物、土壤微生物群落和生态系统动态之间复杂的相互作用。

Abstract: Bidens pilosa is recognized as one of the major invasive plants in China. Its invasion has been associated with significant losses in agriculture, forestry, husbandry, and biodiversity. Soil ecosystems play an important role in alien plant invasion. Microorganisms within the soil act as intermediaries between plants and soil ecological functions, playing a role in regulating soil enzyme activities and nutrient dynamics. Understanding the interactions between invasive plants, soil microorganisms, and soil ecological processes is vital for managing and mitigating the impacts of invasive species on the environment. In this study, we conducted a systematic analysis focusing on B. pilosa and Setaria viridis, a common native companion plant in the invaded area. To simulate the invasion process of B. pilosa, we constructed homogeneous plots consisting of B. pilosa and S. viridis grown separately as monocultures, as well as in mixtures. The rhizosphere and bulk soils were collected from the alien plant B. pilosa and the native plant S. viridis. In order to focus on the soil ecological functional mechanisms that contribute to the successful invasion of B. pilosa, we analyzed the effects of B. pilosa on the composition of soil microbial communities and soil ecological functions. The results showed that the biomass of B. pilosa increased by 27.51% and that of S. viridis was significantly reduced by 66.56%. The organic matter contents in the bulk and rhizosphere soils of B. pilosa were approximately 1.30 times those in the native plant soils. The TN and NO₃^– contents in the rhizosphere soil of B. pilosa were 1.30 to 2.71 times those in the native plant soils. The activities of acid phosphatase, alkaline phosphatase, and urease in the rhizosphere soil of B. pilosa were 1.98–2.25 times higher than in the native plant soils. Using high-throughput sequencing of the 16S rRNA gene, we found that B. pilosa altered the composition of the soil microbial community. Specifically, many genera in Actinobacteria and Proteobacteria were enriched in B. pilosa soils. Further correlation analyses verified that these genera had significantly positive relationships with soil nutrients and enzyme activities. Plant biomass, soil pH, and the contents of organic matter, TN, NO₃^–, TP, AP, TK, and AK were the main factors affecting soil microbial communities. This study showed that the invasion of B. pilosa led to significant alterations in the composition of the soil microbial communities. These changes were closely linked to modifications in plant traits as well as soil physical and chemical properties. Some microbial species related to C, N and P cycling were enriched in the soil invaded by B. pilosa. These findings provide additional support for the hypothesis of soil-microbe feedback in the successful invasion of alien plants. They also offer insights into the ecological mechanism by which soil microbes contribute to the successful invasion of B. pilosa. Overall, our research contributes to a better understanding of the complex interactions between invasive plants, soil microbial communities, and ecosystem dynamics.

Key words: plant invasion , Bidens pilosa , soil microbial composition , soil properties , soil enzyme activities

. 三叶鬼针草与狗尾草竞争改变了土壤微生物组成和土壤生态功能[J]. Journal of Integrative Agriculture, 2024, 23(1): 267-282.

Qiao Li, Jianying Guo, Han Zhang, Mengxin Zhao.

The competition between Bidens pilosa and Setaria viridis alters soil microbial composition and soil ecological function [J]. Journal of Integrative Agriculture, 2024, 23(1): 267-282.

参考文献

Ahmad R, Khuroo A A, Hamid M, Rashid I. 2020. Plant invasion alters the physico-chemical dynamics of soil system: Insights from invasive Leucanthemum vulgare in the Indian Himalaya. Environmental Monitoring and Assessment, 191, 792.

Becarelli S, Chicca I, La China S, Siracusa G, Bardi A, Gullo M, Petroni G, Levin D B, Di Gregorio S. 2021. A new Ciboria sp. for soil mycoremediation and the bacterial contribution to the depletion of total petroleum hydrocarbons. Frontiers in Microbiology, 12, 647373.

Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society (Series B: Methodological), 57, 289–300.

Bremner J M. 1965. Chemical and microbiological properties. In: Black C A, ed., Methods of Soils Analysis. American Society of Agronomy, Madison, WI, USA. pp. 1149–1178.

Callaway R, Thelen G, Rodriguez A, Holben W. 2004. Soil biota and exotic plant invasion. Nature, 427, 731–733.

Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Huntley J, Fierer N, Owens S M, Betley J, Fraser L, Bauer M, Gormley N, Gilbert J A, Smith G, Knight R. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The International Society for Microbial Ecology Journal, 6, 1621–1624.

Caporaso J G, Lauber C L, Walters W A, Berg-Lyons D, Lozupone C A, Turnbaugh P J, Fierer N, Knight R. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of the Sciences of the United States of America, 108(Suppl. 1), 4516–4522.

Chauhan B S, Ali H H, Florentine S. 2019. Seed germination ecology of Bidens pilosa and its implications for weed management. Scientific Reports, 9, 16004.

Chen J, Zhang Y, Kuzyakov Y, Wang D, Olesen J E. 2023. Challenges in upscaling laboratory studies to ecosystems in soil microbiology research. Global Change Biology, 29, 569–574.

Chen L, Li H N, Yang M H, Wan F H. 2011. Influence of invasion of Mikania micrantha and Bidens pilosa to the bacterial community in the root soils. Chinese Agricultural Science Bulletin, 27, 63–68. (in Chinese)

Chen W B, Chen B M. 2019. Considering the preferences for nitrogen forms by invasive plants: A case study from a hydroponic culture experiment. Weed Research, 59, 49–57.

Coonan E C, Kirkby C A, Kirkegaard J A, Amidy M R, Strong C L, Richardson A E. 2020. Microorganisms and nutrient stoichiometry as mediators of soil organic matter dynamics. Nutrient Cycling in Agroecosystems, 117, 273–298.

Datt N, Singh D. 2019. Enzymes in relation to soil biological properties and sustainability. In: Meena R S, Kumar S, Bohra J S, Jat M L, eds., Sustainable Management of Soil and Environment. Springer Singapore, Singapore. pp. 383–406.

Du F Y, Zhang M M, Ma D W, Zhou X K, Zhong L W. 2007. Preliminary study on the allelopathic effects of Bidens pilosa. China Plant Protection, 27, 8–11. (in Chinese)

Duda J J, Freeman D C, Emlen J M, Belnap J, Kitchen S G, Zak J C, Sobek E, Tracy M, Montante J. 2003. Differences in native soil ecology associated with invasion of the exotic annual chenopod, Halogeton glomeratus. Biology and Fertility of Soils, 38, 72–77.

Edgar R C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460–2461.

Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27, 2194–2200.

Ehrenfeld J G. 2003. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems, 6, 503–523.

Fahey C, Koyama A, Antunes P M, Dunfield K, Flory S L. 2020. Plant communities mediate the interactive effects of invasion and drought on soil microbial communities. The International Society for Microbial Ecology Journal, 14, 1396–1409.

Gertrude M T, Jeannette Y, Gabriel T H, Mbida M. 2022. Assessment of in situ anthelminthic activity of ethanolic extract of Bidens pilosa against adult’s gastro-intestinal strongyle of small ruminants. American Journal of Plant Sciences, 13, 433–442.

Guan S Y, Zhang D, Zhang Z. 1986. Soil Enzyme and Its Research Methods. Chinese Agricultural Press, Beijing. (in Chinese)

He B, Li R, Luo M, Wei H, Zhang H, Ma D. 2013. Effects of Bidens pilosa of invasive plant on soil ecological system at different developmental stages. Southwest China Journal of Agricultural Sciences, 26, 1953–1956. (in Chinese)

Heng T, Yang L, Hermansen C, de Jonge L W, Zhang Z, Wu B, Chen J, Zhao L, Yu J, He X. 2022. Linking microbial community compositions to cotton nitrogen utilization along soil salinity gradients. Field Crops Research, 288, 108697.

Hierro J L, Maron J L, Callaway R M. 2005. A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. Journal of Ecology, 93, 5–15.

Isaac R A, Johnson W C. 1983. High speed analysis of agricultural samples using inductively coupled plasma-atomic emission spectroscopy. Spectrochimica Acta (Part B: Atomic Spectroscopy), 38, 277–282.

Jian S, Li J, Chen J, Wang G, Mayes M A, Dzantor K E, Hui D, Luo Y. 2016. Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: A meta-analysis. Soil Biology and Biochemistry, 101, 32–43.

Kompała-Bąba A, Bierza W, Sierka E, Błońska A, Besenyei L, Woźniak G. 2021. The role of plants and soil properties in the enzyme activities of substrates on hard coal mine spoil heaps. Scientific Reports, 11, 5155.

Kourtev P S, Ehrenfeld J G, Häggblom M. 2002. Exotic plant species alter the microbial community structure and function in the soil. Ecology, 83, 3152–3166.

Kourtev P S, Ehrenfeld J G, Häggblom M. 2003. Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biology and Biochemistry, 35, 895–905.

Kourtev P S, Huang W Z, Ehrenfeld J G. 1999. Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species. Biological Invasions, 1, 237–245.

Kox M A R, Aalto S L, Penttilä T, Ettwig K F, Jetten M S M, van Kessel M A H J. 2018. The influence of oxygen and methane on nitrogen fixation in subarctic Sphagnum mosses. AMB Express, 8, 76.

Li P, Liu J, Saleem M, Li G, Luan L, Wu M, Li Z. 2022. Reduced chemodiversity suppresses rhizosphere microbiome functioning in the mono-cropped agroecosystems. Microbiome, 10, 108.

Li Q, Chen J, Feng J, Wu J, Zhang Q, Jia W, Lin Q, Cheng X. 2020. How do biotic and abiotic factors regulate soil enzyme activities at plot and microplot scales under afforestation? Ecosystems, 23, 1408–1422.

Li Q, Wan F H, Zhao M X. 2022. Distinct soil microbial communities under Ageratina adenophora invasions. Plant Biology, 24, 430–439.

Li Y N, Gu Y S, Li M Z, Huo G J, Wang X P, Xu Z J, Yue J, Du D, Geng M G. 2021. Comparison on the phytoextraction efficiency of Bidens pilosa at heavy metal contaminated site in natural and electrokinetic conditions. Journal of Groundwater Science and Engineering, 9, 121–128.

Ling W, Ma B, Zhang W. 2022. Editorial: Rhizosphere microbiology: Toward a clean and healthy soil environment. Frontiers in Microbiology, 13, 991356.

Liu B, Liu X, Huo S, Chen X, Wu L, Chen M, Zhou K, Li Q, Peng L. 2017. Properties of root exudates and rhizosphere sediment of Bruguiera gymnorrhiza (L.). Journal of Soils and Sediments, 17, 1–11.

Lu R K. 1999. Analyse Methods of Soil and Agrochemistry. Chinese Agricultural Science and Technology Press, Beijing. (in Chinese)

Luo M, Moorhead D L, Ochoa-Hueso R, Mueller C W, Ying S C, Chen J. 2022. Nitrogen loading enhances phosphorus limitation in terrestrial ecosystems with implications for soil carbon cycling. Functional Ecology, 36, 2845–2858.

Makonde H, Mwirichia R, Osiemo Lagat Z, Boga H, Klenk H P. 2015. 454 Pyrosequencing-based assessment of bacterial diversity and community structure in termite guts, mounds and surrounding soils. SpringerPlus, 4, 471.

Margalef O, Sardans J, Fernández-Martínez M, Molowny-Horas R, Janssens I A, Ciais P, Goll D, Richter A, Obersteiner M, Asensio D, Peñuelas J. 2017. Global patterns of phosphatase activity in natural soils. Scientific Reports, 7, 1337.

Marilley L, Vogt G, Blanc M, Aragno M. 1998. Bacterial diversity in the bulk soil and rhizosphere fractions of Lolium perenne and Trifolium repens as revealed by PCR restriction analysis of 16S rDNA. Plant and Soil, 198, 198.

Nelson D, Sommers L E. 1983. Total carbon, organic carbon, and organic matter. In: Page A L, ed., Methods of Soil Analysis: Part 2. Chemical and Microbiological Properties. American Society of Agronomy and Soil Science, Madison, WI, USA. pp. 539–579.

Nelson D W, Sommers L E. 1973. Determination of total nitrogen in plant material. Agronomy Journal, 65, 109–112.

Nikitin D A, Semenov M V, Chernov T I, Ksenofontova N A, Zhelezova A D, Ivanova E A, Khitrov N B, Stepanov A L. 2022. Microbiological indicators of soil ecological functions: A review. Eurasian Soil Science, 55, 221–234.

Olsen S R, Cole C V, Watanabe F S, Dean L. 1954. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate. US Department of Agriculture, Washington, D. C.

Peng R M, Peng Y, Xiang G H, Yang Z L. 2021. Rhizosphere soil nutrients, enzyme activities and microbial characteristics of different invasive plants. Jiangsu Agricultural Sciences, 49, 217–223. (in Chinese)

Reinhart K O, Callaway R M. 2006. Soil biota and invasive plants. New Phytologist, 170, 445–457.

Rice E L. 1983. Allelopathy. 2nd ed. Academic Press, New York.

Richardson D M, Allsopp N, D’Antonio C M, Milton S J, Rejmánek M. 2000. Plant invasions - the role of mutualisms. Biological Reviews of the Cambridge Philosophical Society, 75, 65–93.

Roiloa S R, Yu F H, Barreiro R. 2020. EDITORIAL: Plant invasions: Mechanisms, impacts and management. Flora, 267, 151603.

Rousk J, Bååth E, Brookes P, Lauber C, Lozupone C, Caporaso J, Knight R, Fierer N. 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. The International Society for Microbial Ecology Journal, 4, 1340–1351.

Saggar S, McIntosh P D, Hedley C B, Knicker H. 1999. Changes in soil microbial biomass, metabolic quotient, and organic matter turnover under Hieracium (H. pilosella L.). Biology and Fertility of Soils, 30, 232–238.

Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W S, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biology, 12, R60.

Silva F L, Fischer D C, Tavares J F, Silva M S, de Athayde-Filho P F, Barbosa-Filho J M. 2011. Compilation of secondary metabolites from Bidens pilosa L. Molecules, 16, 1070–1102.

Suela Silva M, Naves Sales A, Teixeira Magalhães-Guedes K, Ribeiro Dias D, Schwan R F. 2013. Brazilian cerrado soil actinobacteria ecology. BioMed Research International, 2013, 503805.

Tabatabai M, Dick W. 2002. Enzymes in Soil. Chemical Rubber Company Press, Boca Raton.

Tan K H. 1995. Soil Sampling, Preparation, and Analysis. Chemical Rubber Company Press, Boca Raton.

Tao H Z, Tian X J, Xia F, Shen Y M. 2015. Allelopathic effect of Bidens pilosa extracts on germination and seedling growth of Taraxacum mongolicum. Northern Horticulture, 39, 87–90. (in Chinese)

Trivedi P, Batista B D, Bazany K E, Singh B K. 2022. Plant–microbiome interactions under a changing world: Responses, consequences and perspectives. New Phytologist, 234, 1951–1959.

Vogelsang K M, Bever J D. 2009. Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology, 90, 399–407.

Wan F H, Guo J Y, Wang D H. 2002. Alien invasive species in China: Their damages and management strategies. Biodiversity Science, 10, 119–125.

Wan F H, Zheng X B, Guo J Y. 2003. Biology and Management of Invasive Alien Species in Agriculture and Forestry. Science Press, Beijing. (in Chinese)

Wang H, Wang B, Dong W W, Hu X K. 2016. Co-acclimation of bacterial communities under stresses of hydrocarbons with different structures. Scientific Reports, 6, 34588.

Wang Y, Li C, Kou Y, Wang J, Tu B, Li H, Li X, Wang C, Yao M. 2017. Soil pH is a major driver of soil diazotrophic community assembly in Qinghai-Tibet alpine meadows. Soil Biology and Biochemistry, 115, 547–555.

Weber E, Sun S G, Li B. 2008. Invasive alien plants in China: Diversity and ecological insights. Biological Invasions, 10, 1411–1429.

Wei H J, Chen B M. 2023. Competition shifts the advantage of the invasive plant Bidens alba to a disadvantage under soil ammonia nitrogen. Biological Invasions, 25, 2277–2292.

Woods M J, Attea G K, McEwan R W. 2021. Resprouting of the woody plant Pyrus calleryana influences soil ecology during invasion of grasslands in the American Midwest. Applied Soil Ecology, 166, 103989.

Yan J, Zhang X Y, Chen X, Wang Y, Zhang F J, Wan F H. 2016. Effects of rhizosphere soil microorganisms and soil nutrients on competitiveness of Bidens pilosa with different native plants. Biodiversity Science, 24, 1381–1389. (in Chinese)

Yu H, Le Roux J J, Jiang Z, Sun F, Peng C, Li W. 2021. Soil nitrogen dynamics and competition during plant invasion: Insights from Mikania micrantha invasions in China. New Phytologist, 229, 3440–3452.

Zhang K M, Shen Y M, Zhou X Q, Fang Y M, Liu Y, Ma L Q. 2016. Photosynthetic electron-transfer reactions in the gametophyte of Pteris multifida reveal the presence of allelopathic interference from the invasive plant species Bidens pilosa. Journal of Photochemistry and Photobiology (B: Biology), 158, 81–88.

Zhang M M, Li X Y, Shi C, Qiu Z L, Han J H, Wang K F, Zheng P F, Shi F C. 2022. Driving factors, co-occurrence networks, and metabolic profiles of soil bacterial communities within the root proximity of Amaranthus palmeri. Journal of Soil Science and Plant Nutrition, 22, 1928–1941.

Zhang R, Vivanco J M, Shen Q. 2017. The unseen rhizosphere root–soil–microbe interactions for crop production. Current Opinion in Microbiology, 37, 8–14.

Zhao M X, Lu X F, Zhao H X, Yang Y F, Hale L, Gao Q, Liu W X, Guo J Y, Li Q, Zhou J Z, Wan F H. 2019. Ageratina adenophora invasions are associated with microbially mediated differences in biogeochemical cycles. Science of the Total Environment, 677, 47–56.

Zhou Y, Staver A C. 2019. Enhanced activity of soil nutrient-releasing enzymes after plant invasion: A meta-analysis. Ecology, 100, e02830.