Solidago canadensis invasion affects soil N-fixing bacterial communities in heterogeneous landscapes in urban ecosystems in East China

https://doi.org/10.1016/j.scitotenv.2018.03.061Get rights and content

Highlights

  • S. canadensis invasion significantly alters the community structure of SNB.

  • Landscape heterogeneity significantly affects the diversity and richness of SNB.

  • Landscape heterogeneity significantly affects the community structure of SNB.

  • Community invasibility of farmland wasteland was highest in the urban ecosystems.

Abstract

Soil nitrogen-fixing bacterial communities (SNB) can increase the level of available soil N via biological N-fixation to facilitate successful invasion of several invasive plant species (IPS). Meanwhile, landscape heterogeneity can greatly enhance regional invasibility and increase the chances of successful invasion of IPS. Thus, it is important to understand the soil micro-ecological mechanisms driving the successful invasion of IPS in heterogeneous landscapes. This study performed cross-site comparisons, via metagenomics, to comprehensively analyze the effects of Solidago canadensis invasion on SNB in heterogeneous landscapes in urban ecosystems. Rhizospheric soil samples of S. canadensis were obtained from nine urban ecosystems [Three replicate quadrats (including uninvaded sites and invaded sites) for each type of urban ecosystem]. S. canadensis invasion did not significantly affect soil physicochemical properties, the taxonomic diversity of plant communities, or the diversity and richness of SNB. However, some SNB taxa (i.e., f_Micromonosporaceae, f_Oscillatoriaceae, and f_Bacillaceae) changed significantly with S. canadensis invasion. Thus, S. canadensis invasion may alter the community structure, rather than the diversity and richness of SNB, to facilitate its invasion process. Of the nine urban ecosystems, the diversity and richness of SNB was highest in farmland wasteland. Accordingly, the community invasibility of farmland wasteland may be higher than that of the other types of urban ecosystem. In brief, landscape heterogeneity, rather than S. canadensis invasion, was the strongest controlling factor for the diversity and richness of SNB. One possible reason may be the differences in soil electrical conductivity and the taxonomic diversity of plant communities in the nine urban ecosystems, which can cause notable shifts in the diversity and richness of SNB.

Graphical abstract

S. canadensis invasion may likely alter the community structure of soil nitrogen-fixing bacterial communities rather than the diversity or richness to facilitate its invasion process. The community invasibility of farmland wasteland may be higher than that of the other types of urban ecosystem. Meanwhile, landscape heterogeneity, rather than S. canadensis invasion, was the strong controlling factor that triggered pronounced effects on the diversity and richness of soil nitrogen-fixing bacterial communities.

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Introduction

Invasive plant species (IPS) have been shown to introduce obvious shifts in the structure and functions of invaded ecosystems (Kamutando et al., 2017; Wang et al., 2017a, Wang et al., 2017b, Wang et al., 2018a; Vieites-Blanco and González-Prieto, 2018). Furthermore, the invasion processes of numerous IPS are strongly associated with significant changes in soil microbial communities via plant-soil feedback in the rhizosphere, a process that can raise the possibility of successful colonization of those invaders in new ecosystems (Kamutando et al., 2017; Rodríguez-Caballero et al., 2017; Wang et al., 2017a, Wang et al., 2017b, Wang et al., 2017c, Wang et al., 2018b).

Soil nitrogen (N) availability is considered one of the most important factors for successful invasion of some IPS in a variety of ecosystems (Ehrenfeld, 2003; Davidson et al., 2011; Matzek, 2012). More importantly, IPS appears to be more efficient at absorbing and utilizing nutrients (especially N) compared with natives (Davidson et al., 2011; Matzek, 2012). However, N is a key limiting nutrient in many terrestrial ecosystems (Bobbink et al., 2010; Boonstra et al., 2017; van den Elzen et al., 2018). Significantly, soil N-fixing bacterial communities (SNB) can increase the levels of available soil N via biological N-fixation (Xu et al., 2012; Huang et al., 2016; Kamutando et al., 2017). Meanwhile, the degree of invasiveness of some IPS is closely associated with the available level of soil nutrients (particularly N) (Ehrenfeld, 2003; Kamutando et al., 2017). Accordingly, SNB play a crucial role in the successful invasion of a wide range of IPS (Ehrenfeld, 2003; Xu et al., 2012; Kamutando et al., 2017).

Since the mid-20th century, one of the most significant environmental problems in urban ecosystems has been an increase in landscape heterogeneity driven by increased urbanization (Trentanovi et al., 2013; El-Barougy et al., 2017). However, landscape heterogeneity can greatly enhance regional invasibility and increase the chances of successful invasion of IPS (Kellner and Hastings, 2009; Ricotta et al., 2010; El-Barougy et al., 2017). This is mainly due to the greater adaptability of IPS in heterogeneous environments compared to NPS (Xu et al., 2014; Keser et al., 2015). In addition, the reduced competitiveness of established species mediated by urbanization is another driver that may create a favorable habitat for many IPS via shifts in the availability of resources (Trentanovi et al., 2013; El-Barougy et al., 2017). Thus, it is important to address the effects of IPS invasion on the community structure of SNB in heterogeneous landscapes in urban ecosystems to better understand the soil micro-ecological mechanisms driving the successful invasion of IPS.

In the present study we used metagenomics based on high-throughput sequencing technology to comprehensively analyze the effects of Solidago canadensis L. invasion on the community structure of SNB in heterogeneous landscapes in urban ecosystems. S. canadensis is an herbaceous perennial plant that is native to North America. S. canadensis was introduced to Shanghai, China, as a horticultural plant in the early 1930s. At present, the species has become naturalized in most parts of China and is considered to be one of the most destructive and widespread IPS in China (Abhilasha et al., 2008; Liao et al., 2011; S.Y. Zhao et al., 2015). Currently, the IPS grow mainly in meadows and pastures, farmland, along roads, ditches, upland forests, savannas, and limestone glades (Abhilasha et al., 2008).

This study proposes the following hypotheses. First, the diversity and richness of SNB will increase during S. canadensis invasion compared with an uninvaded area. Second, the diversity and richness of SNB vary among urban ecosystem types.

Section snippets

Study design

S. canadensis was chosen as the target IPS. In mid-July 2017, samples of S. canadensis and coexisting NPS were obtained from nine urban ecosystems in Zhenjiang, characterized by a sampling area with a subtropical and humid climate. The annual mean temperature of the area is approximately 15.9 °C with monthly mean temperatures reaching a maximum of 28 °C in July and a minimum of 2.9 °C in January. The annual precipitation is approximately 1101.4 mm, with a monthly mean precipitation accumulation

Soil physicochemical properties, the relative abundance of S. canadensis, and the taxonomic diversity of plant communities

Soil EC was significantly lower in the garden scenic area than in farmland wasteland and wetland waterfront (P < 0.05; Fig. 1). The highest value of the relative abundance of S. canadensis was observed in traffic land and the lowest value of the relative abundance of S. canadensis was observed in municipal land and urban green space (P < 0.05; Fig. 1). Shannon's diversity of plant communities was significantly higher in wetland waterfront than in the other urban ecosystems (except for farmland

Discussion

Numerous results show that a wide range of IPS (including S. canadensis) can trigger a shift in the physicochemical properties of soil (especially pH) mainly due to the selective absorption of N forms [strong preference for ammonium (NH4+) over nitrate (NO3)] (Chen et al., 2012; Huangfu et al., 2016) and/or the alkaline substances in the litters and/or root exudates of IPS (Dassonville et al., 2011; Chen et al., 2012). However, S. canadensis invasion did not create noticeable effects on soil

Conclusions

The purpose of this study was to gain insights into the effects of the invasive plant S. canadensis in urban ecosystems with heterogeneous landscapes on the community structure of SNB. Our results showed that S. canadensis invasion did not cause significantly shifts in soil physicochemical properties, the taxonomic diversity of plant communities, and the diversity and richness of SNB. However, some SNB taxa (i.e., f_Micromonosporaceae, f_Oscillatoriaceae, and f_Bacillaceae) changed

Acknowledgements

We greatly appreciate to TinyGene Technologies Co., Ltd., Shanghai, China for the determination of soil N-fixing bacterial community structure using high-throughput sequencing. This study was supported by State Key Research Development Program of China (2017YFC1200103), National Natural Science Foundation of China (31300343), Open Science Research Fund of Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering (Fudan University), China (2017-FDU-01), and Jiangsu

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