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The invasive Alternanthera philoxeroides modifies the sediment microbiome in urban and periurban river wetlands

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Abstract

Few studies have evaluated the invasive effects on soil properties in urban ecosystems. In this study, population density and impervious surface area were used to divide the two river wetlands of Qingdao City, China— River Zhangcun and River Wenquan—into urban and periurban types. Sediments were sampled from plots colonized by the invasive Alternanthera philoxeroides and the native Typha angustifolia in these two river wetlands. The sediment properties, including fertility, stoichiometry, microbial diversity indices (observed species, Chao1, Shannon’s diversity index and Simpson’s diversity index) and species composition, were evaluated and compared. We found similar fertility and stoichiometry between sediments derived from invasive and native species. A greater bacterial diversity was found in the sediment derived from A. philoxeroides in the periurban river, while a greater fungal diversity was merely shown for the Shannon’s diversity index of A. philoxeroides regardless of river types. In addition, more microbes relevant to nutrient cycling processes, such as denitrification, accumulated in response to invasion, which may have decreased the habitat quality and impeded the invasion of T. angustifolia into A. philoxeroides populations. The discrepancy in urbanization status affected the impact of plant colonization on sediment properties, and the opposite results were shown for the comparisons of sediment nitrogen availability and bacterial diversity between the two species. Urbanization discriminated the impact of invasion to some degree. The invasion of A. philoxeroides altered the sediment microbiome, and the potential plant‒soil feedback needs further investigation.

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References

  • Bills JS, Jacinthe PA, Tedesco LP (2010) Soil organic carbon pools and composition in a wetland complex invaded by reed canary grass. Biol Fert Soils 46:697–706

    Article  CAS  Google Scholar 

  • Cadotte MW, Yasui SLE, Livingstone S, MacIvor JS (2017) Are urban systems beneficial, detrimental, or indifferent for biological invasion? Biol Invasions 19:3489–3503

    Article  Google Scholar 

  • Calfapietra C, Peñuelas J, Niinemets Ü (2015) Urban plant physiology: adaptation-mitigation strategies under permanent stress. Trends Plant Sci 20:72–75

    Article  CAS  PubMed  Google Scholar 

  • Chapuis-Lardy L, Vanderhoeven S, Dassonville N, Koutika LS, Meerts P (2006) Effect of the exotic invasive plant Solidago gigantea on soil phosphorus status. Biol Fert Soils 42:481–489

    Article  Google Scholar 

  • Chen J, Nan J, Xu DL, Mo L, Zheng YX, Chao LM, Qu HT, Guo YQ, Li FS, Bao YY (2020) Response differences between soil fungal and bacterial communities under opencast coal mining disturbance conditions. CATENA 194:104779

    Article  Google Scholar 

  • Chen L, Xiang WH, Ouyang S, Wu HL, Xia Q, Ma JN, Zeng YL, Lei PF, Xiao WF, Li SG, Kuzyakov Y (2021) Tight coupling of fungal community composition with soil quality in a Chinese fir plantation chronosequence. Land Degrad Dev 32:1164–1178

    Article  Google Scholar 

  • Comandini O, Rinaldi AC, Kuyper TW (2012) Chap. 9: measuring and estimating ectomycorrhizal fungal diversity: a continuous challenge. In: Pagano M (ed) Mycorrhiza: occurrence in Natural and restored environments. Nova Science Publishers Inc, Hauppauge, NY, pp 165–200

    Google Scholar 

  • Cruz C, Vishwakarma K, Choudhary DK, Varma A (2021) Soil Nitrogen Ecology. Springer Nature Switzerland AG

  • Dalu T, Wasserman RJ, Magoro ML, Froneman PW, Weyl OLF (2019) River nutrient water and sediment measurements inform on nutrient retention, with implications for eutrophication. Sci Tot Env 684:296–302

    Article  CAS  Google Scholar 

  • Dong M (2018) Urban Wetland Ecosystem Ecology. Science, Beijing, China. (in Chinese)

    Google Scholar 

  • Duda JJ, Freeman DC, Emlen JM, Belnap J, Kitchen SG, Zak JC, Sobek E, Tracy M, Montante J (2003) Differences in native soil ecology associated with invasion of the exotic annual chenopod, Halogeton glomeratus. Biol Fert Soils 38:72–77

    Article  CAS  Google Scholar 

  • Elgersma KJ (2014) Soils suppressing and promoting non-native plant invasions. In: Dighton J, Krumins JA (eds) Interactions in soil: promoting Plant Growth. Springer Science + Business Media, Dordrecht, pp 181–202

    Chapter  Google Scholar 

  • Eppinga MB, Rietkerk M, Dekker SC, De Ruiter PC, Van der Putten WH (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114:168–176

    Article  ADS  Google Scholar 

  • Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96

    Article  CAS  Google Scholar 

  • Fu GP, Wu JF, Han JY, Zhao L, Chan G, Leong KF (2020) Effects of substrate type on denitrification efficiency and microbial community structure in constructed wetlands. Bioresource Technol 307:123222

    Article  CAS  Google Scholar 

  • Gaggini L, Rusterholz H, Baur B (2018) The invasive plant Impatiens glandulifera affects soil fungal diversity and the bacterial community in forests. Appl Soil Ecol 124:335–343

    Article  Google Scholar 

  • Grella C, Renshaw A, Wright IA (2018) Invasive weeds in urban riparian zones: the influence of catchment imperviousness and soil chemistry across an urbanization gradient. Urban Ecosyst 21:505–517

    Article  Google Scholar 

  • He CQ, Cheng LY, Wang DY, Zhao ZZ, Wang ZY, Wang FF, Wang XX, Zhang P, Chen XP, Liu XY (2021) Spartina alterniflora raised soil sulfide content by regulating sulfur cycle-associated bacteria in the Jiuduansha Wetland of China. Plant Soil 69:107–121

    Article  Google Scholar 

  • Hulme PE, Brundu G, Carboni M et al (2019) Integrating invasive species policies across ornamental horticulture supply chains to prevent plant invasions. J Appl Ecol 55:92–98

    Article  Google Scholar 

  • Johnston CA (1991) Sediment and nutrient retention by freshwater wetlands: effects on surface water quality. Crit Rev Env Sci Tec 21:491–565

    Google Scholar 

  • Kalisz S, Kivlin SN, Bialic-Murphy L (2021) Allelopathy is pervasive in invasive plants. Biol Invasions 23:367–371

    Article  Google Scholar 

  • Kalwij JM, Milton SJ, McGeoch MA (2008) Road verges as invasion corridors? A spatial hierarchical test in an arid ecosystem. Landsc Ecol 23:439–451

    Article  Google Scholar 

  • Kowarik I (2008) On the role of alien species in urban flora and vegetation. In: Marzluff JM, Shulenberger E, Endlicher W, Alberti M, Bradley G, Ryan C, ZumBrunnen C, Simon U (eds) Urban Ecology: an International Perspective on the Interaction between humans and nature. Springer Science + Business Media, LLC, New York, USA, pp 321–338

    Chapter  Google Scholar 

  • Landeweert R, Hoffland E, Finlay RD, Kuyper TW, Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254

    Article  CAS  PubMed  Google Scholar 

  • Li SY, Xie D, Ge XG, Dong W, Luan JW (2022) Altered diversity and functioning of soil and root-associated microbiomes by an invasive native plant. Plant Soil 473:235–249

    Article  CAS  Google Scholar 

  • Liendo D, García-Mijangos I, Campos JA, López-Muniain U, Biurrun I (2016) Drivers of plant invasion at broad and fine scale in short temperate streams. River Res Appl 32:1730–1739

    Article  Google Scholar 

  • Looney BP, Meidl P, Piatek MJ, Miettinen O, Martin FM, Matheny PB, Labbé JL (2018) Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates. New Phytol 218:54–65

    Article  CAS  PubMed  Google Scholar 

  • Luo RY, Kuzyakov Y, Liu DY, Fan JL, Luo JF, Lindsey S, He JS, Ding WX (2020) Nutrient addition reduces carbon sequestration in a tibetan grassland soil: disentangling microbial and physical controls. Soil Biol Biochem 144:107764

    Article  CAS  Google Scholar 

  • Majewska ML, Rola K, Stefanowicz AM, Nobis M, Błaszkowski J, Zubek S (2018) Do the impacts of alien invasive plants differ from expansive native ones? An experimental study on arbuscular mycorrhizal fungi communities. Biol Fert Soils 54:631–643

    Article  Google Scholar 

  • Mangla S, Inderjit, Callaway RM (2008) Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J Ecol 96:58–67

    Article  Google Scholar 

  • McDonnell MJ, Pickett STA, Groffman P, Bohlen P, Pouyat RV, Zipperer WC, Parmelee RW, Carreiro MM, Medley K (2008) Ecosystem processes along an urban-to-rural gradient. In: Marzluff JM, Shulenberger E, Endlicher W, Alberti M, Bradley G, Ryan C, ZumBrunnen C, Simon U (eds) Urban Ecology: an International Perspective on the Interaction between humans and nature. Springer Science + Business Media, LLC, New York, USA, pp 299–314

    Chapter  Google Scholar 

  • McKinney ML (2002) Urbanization, Biodiversity, and conservation: the impacts of urbanization on native species are poorly studied, but educating a highly urbanized human population about these impacts can greatly improve species conservation in all ecosystems. Bioscience 52:883–890

    Article  Google Scholar 

  • Moro MF, Castro ASF (2015) A check list of plant species in the urban forestry of Fortaleza, Brazil: where are the native species in the country of megadiversity? Urban Ecosyst 18:47–71

    Article  Google Scholar 

  • Müllerová A, Řehounková K, Prach K (2020) What is a reasonable plot size for sampling aquatic vegetation? Aquat Sci 82:68

    Article  Google Scholar 

  • Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P (2010) HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria Graminis. Plant Cell 22:3130–3141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oduor AMO, Adomako MO, Yuan YG, Li JM (2022) Older populations of the invader Solidago canadensis exhibit stronger positive plant-soil feedbacks and competitive ability in China. Am J Bot 109:1230–1241

    Article  CAS  PubMed  Google Scholar 

  • Oertli B, Boissezon A, Rosset V et al (2018) Alien aquatic plants in wetlands of a large European city (Geneva, Switzerland): from diagnosis to risk assessment. Urban Ecosyst 21:245–261

    Google Scholar 

  • Osburn ED, McBride SG, Aylward FO, Badgley BD, Strahm BD, Knoepp JD, Barrett JE (2019) Soil bacterial and fungal communities exhibit distinct long-term responses to disturbance in temperate forests. Front Microbiol 10:2872

    Article  PubMed  PubMed Central  Google Scholar 

  • Parra-Tabla V, Arceo-Gómez G (2021) Impacts of plant invasions in native plant-pollinator networks. New Phytol 230:2117–2128

    Article  PubMed  Google Scholar 

  • Paul MJ, Meyer JL (2008) Streams in the urban landscape. In: Marzluff JM, Shulenberger E, Endlicher W, Alberti M, Bradley G, Ryan C, ZumBrunnen C, Simon U (eds) Urban Ecology: an International Perspective on the Interaction between humans and nature. Springer Science + Business Media, LLC., New York, USA, pp 207–232

    Chapter  Google Scholar 

  • Planillo A, Kramer-Schadt S, Buchholz S, Gras P, von der Lippe M, Radchuk V (2021) Arthropod abundance modulates bird community responses to urbanization. Divers Distrib 27:34–49

    Article  Google Scholar 

  • Ramsar (2008) Resolution X 27. http://www.ramsar.org/document/resolution-x27-wetlands-and-urbanizati on [2016-9-10]

  • Ravichandran KR, Thangavelu M (2017) Role and influence of soil microbial communities on plant invasion. Ecol Quest 3:9–23

    Google Scholar 

  • Sapsford SJ, Wakelin A, Peltzer DA, Dickie IA (2022) Pine invasion drives loss of soil fungal diversity. Biol Invasions 24:401–414

    Article  Google Scholar 

  • Scherr KD, Jamieson MA (2021) Abiotic and biotic drivers of strawberry productivity across a rural-urban gradient. Basic Appl Ecol 57:65–77

    Article  Google Scholar 

  • Seto KC, Parnell S, Elmqvist T (2013) Chap. 1 a global outlook on urbanization. In: Elmqvist T, Fragkias M, Goodness J, Güneralp B, Marcotullio PJ, McDonald RI, Parnell S, Schewenius M, Sendstad M, Seto KC, Wilkinson C (eds) Urbanization, Biodiversity and Ecosystem Services: challenges and opportunities. Springer, Dordrecht Heidelberg New York London, pp 1–12

    Google Scholar 

  • Stefanowicz AM, Stanek M, Nobis M, Zubek S (2016) Species-specific effects of plant invasions on activity, biomass, and composition of soil microbial communities. Biol Fert Soils 52:841–852

    Article  CAS  Google Scholar 

  • Tasker SJL, Foggo A, Bilton DT (2022) Quantifying the ecological impacts of alien aquatic macrophytes: a global meta-analysis of effects on fish, macroinvertebrate and macrophyte assemblages. Freshw Biol 67:1847–1860

    Article  Google Scholar 

  • Unger IM, Kremer RJ, Veum KS, Goyne KW (2022) Immediate and long-term effects of invasive plant species on soil characteristics. Soil Ecol Lett 4:276–288

    Article  Google Scholar 

  • United Nations (2013) Sustainable development challenges, world economic and social survey. United Nations, New York

    Book  Google Scholar 

  • Urakawa H, Bernhard AE (2017) Wetland management using microbial indicators. Ecol Eng 108:456–476

    Article  Google Scholar 

  • van Kleunen M, Essl F, Pergl J et al (2018) The changing role of ornamental horticulture in alien plant invasions. Biol Rev 93:1421–1437

    Article  PubMed  Google Scholar 

  • Wang T, Hu JT, Wang RQ, Liu CH, Yu D (2018) Tolerance and resistance facilitate the invasion success of Alternanthera philoxeroides in disturbed habitats: a reconsideration of the disturbance hypothesis in the light of phenotypic variation. Environ Exp Bot 153:135–142

    Article  CAS  Google Scholar 

  • Wen ZH, White PJ, Shen JB, Lambers H (2021) Linking root exudation to belowground economic traits for resource acquisition. New Phytol 233:1620–1635

    Article  PubMed  Google Scholar 

  • 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

    Article  ADS  CAS  Google Scholar 

  • Zhang GL, Bai JH, Tebbe CC, Huang LB, Jia J, Wang W, Wang X, Yu L, Zhao QQ (2021) Spartina alterniflora invasions reduce soil fungal diversity and simplify co-occurrence networks in a salt marsh ecosystem. Sci Tot Env 758:143667

    Article  CAS  Google Scholar 

  • Zhou Y, Staver AC (2019) Enhanced activity of soil nutrient-releasing enzymes after plant invasion: a meta-analysis. Ecology 100:e02830

    Article  PubMed  Google Scholar 

  • Zubek S, Majewska ML, Błaszkowski J, Stefanowicz AM, Nobis M, Kapusta P (2016) Invasive plants affect arbuscular mycorrhizal fungi abundance and species richness as well as the performance of native plants grown in invaded soils. Biol Fert Soils 52:879–893

    Article  Google Scholar 

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Acknowledgements

We deeply appreciate the precious comments from the editor and two anonymous reviewers on our manuscript and the technological assistances from Novogene Co., Ltd. for soil microbial analyses and from Nanjing Institute of Geography & Limnology, Chinese Academy of Sciences for soil elemental analyses. The present research was supported by the Cooperative Program of Shandong Territorial Spatial Planning Institute (660/2422218) the National Natural Science Foundation of China (31800299), the Qingdao Agricultural University Doctoral Start-Up Fund (663/1121009).

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  1. Tong Wang and Jinming Yang contributed equally to this manuscript and should be considered shared first authors.

Authors and Affiliations

  1. Department of Forestry, College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao, 266109, China

    Tong Wang, Jinming Yang, Yongfeng Zhu, Zeyu Zhang, Xiaolong Chi, Zhen Sun, Chunlin Wang, Lizheng Fang, Hongrui Dou, Zhenghao Fan & Shimei Li

  2. Department of Ecology, College of Life Sciences, The National Field Station of Liangzi Lake Ecosystem, Wuhan University, Wuhan, 430072, China

    Chunhua Liu

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Contributions

T.W. proposed the idea, designed the experiment, acquired the funds and wrote the main manuscript. J.Y. made the visualization and prepared the figures. Y.Z, Z.Z, X.C., Z.S., C.W., L.F., H.D. and Z.F. made the field investigation, collected the samples and analyzed the data. S.L. acquired the fund and revised the draft. C.L. commented on the earlier version of manuscript and revised the draft. All authors reviewed the manuscript and agreed the submission.

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Correspondence to Tong Wang or Shimei Li.

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Wang, T., Yang, J., Zhu, Y. et al. The invasive Alternanthera philoxeroides modifies the sediment microbiome in urban and periurban river wetlands. Urban Ecosyst (2024). https://doi.org/10.1007/s11252-024-01534-0

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