Elsevier

Ecological Engineering

Volume 98, January 2017, Pages 32-39
Ecological Engineering

Responses of soil N-fixing bacteria communities to invasive species over a gradient of simulated nitrogen deposition

https://doi.org/10.1016/j.ecoleng.2016.10.073Get rights and content

Abstract

Soil N-fixing bacteria (SNB) play an important role in the invasion by invasive plant species (IPS). Meanwhile, progressive increases in the level of anthropogenic N deposition can change both soil physicochemical properties and the ecological characteristics of soil microbial communities, with particular impact on SNB. This can impact the soil micro-ecological mechanisms of invasion. This study used new-generation high throughput sequencing technology to determine the effects of invasive plant species Amaranthus retroflexus L. on the structure and diversity of SNB communities over a gradient of simulated N deposition (SND). The study found that soil pH decreased but soil electrical conductivity increased under A. retroflexus invasion. The diversity and richness of SNB decreased under A. retroflexus invasion, due to the altered soil nutrient content mediated by the root exudates released from A. retroflexus, and/or the decreased soil pH triggered by the invasion of A. retroflexus. SND at low levels (2.5–25 g N m−2 yr−1) decreased soil pH but SND at high levels (50 g N m−2 yr−1) increased soil pH significantly via soil secondary salinization. Thus, atmospheric N deposition may exert soil acidification at levels of atmospheric N deposition below critical values but soil alkalization when the level of N exceeds a critical threshold. To a certain extent, SND can increase the species number and the richness of SNB. SND at high levels (50 g N m−2 yr−1) significantly increased the diversity of SNB but significantly decreased the dominance of SNB. Amaranthus retroflexus invasion with SND can decrease the species number, diversity, and richness of SNB and increase the dominance of SNB. The interaction of these effects can produce a neutralizing effect on the diversity and richness of SNB. Thus, the invasion of A. retroflexus may be reduced under SND as a result of the decreased diversity and richness of SNB.

Introduction

Invasive plant species (IPS) can threaten the structure and functioning of the native ecosystems in which invasions occur (Kuebbing et al., 2014, Wang et al., 2016a). Some IPS can trigger pronounced shifts in soil microbial communities in the rhizosphere via plant-soil feedback, increasing the possibility of successful colonization of those invaders (Xu et al., 2012, Souza-Alonso et al., 2015).

Soil nitrogen (N) availability is considered as the main driver of successful invasion of some IPS in certain habitats (Ehrenfeld, 2003, Davidson et al., 2011, Matzek, 2012). First, soil N availability is the main determining factor affecting the outcome of interspecific competition in many ecosystems (Laungani and Knops, 2009, Sanon et al., 2012). Second, many IPS enjoy a strong competitive advantage conferred by rapid absorption of nutrients (especially N) and fast growth rates (Davidson et al., 2011, Matzek, 2012) and soil N-fixing bacteria communities (SNB) can increase soil N availability via N-fixation (Xu et al., 2012, Svensson et al., 2013). Indeed, a very strong positive correlation between the degree of invasion by IPS and soil nutrients (especially N) was detected via a meta-analysis (Ehrenfeld, 2003). Meanwhile, the N utilized by some IPS (i.e. Spartina alterniflora) is mainly derived from N-fixation mediated by SNB (Bagwell and Lovell, 2000). Consequently, SNB play an important role in the successful invasion process of some IPS (Bagwell and Lovell, 2000, Xu et al., 2012).

Currently, one of the most significant global environmental problems is the increase in atmospheric N deposition driven by the emission of nitrogenous compounds to the atmosphere via the combustion of fossil fuels, production and consumption of chemical N fertilizers, and rapid development of animal husbandry (Schlesinger, 2009, Bobbink et al., 2010). East Asia (mainly China) has been listed as one of the world’s three largest areas with the highest rates of N deposition (Wang et al., 2007a, Liu et al., 2013). The rapid increase of deposition of atmospheric N will continue over the next few decades (Schlesinger, 2009, Liu et al., 2013). Even ecosystems in unpopulated regions are exposed to the increased anthropogenic N via long-distance transport and scatter (Wolfe et al., 2006). The rapid increase in deposition of atmospheric N has had a great impact on ecosystem functions, leading to soil acidification (Wang et al., 2011, Wang et al., 2016b, Lv et al., 2013a, Lv et al., 2013b), changes in plant species composition and growth (van den Berg et al., 2011, Wang et al., 2016b), plant-microbe interactions (Wei et al., 2013), and soil microbial communities (Edwards et al., 2011), and enhanced invasiveness of some IPS (Sparrius and Kooijman, 2011, Wang et al., 2016b). Progressive increases in the level of anthropogenic N deposition can affect the soil micro-ecological mechanisms of successful invasion of IPS by impacting both soil physicochemical properties and the ecological characteristics of the soil microbial community, especially SNB. It is important to elucidate the effects of IPS on the structure and diversity of SNB in order to better illuminate the soil micro-ecological mechanisms of successful plant invasions.

This study used new-generation metagenomics based on new-generation high throughput sequencing technology to comprehensively analyze the effects of the invasive plant Amaranthus retroflexus L. on the structure and diversity of SNB across a gradient of simulated N deposition (SND). Amaranthus retroflexus is a summer annual weed native to America (Mandák et al., 2011, Yang et al., 2011). Amaranthus retroflexus has been classified as the third most common dicotyledonous weed due to the fact that this species has spread to most regions of the world (Yang et al., 2011, Ma et al., 2012). The successful colonization of A. retroflexus occurs in many habitats, including orchards, roadside verges, fields, woods, and scrubland in China (Ma et al., 2012, Yan et al., 2014). The results of this study may contribute to an important theoretical foundation and carry practical significance for the effective prevention and control of A. retroflexus invasion.

This study tests the following hypotheses: First, the diversity and richness of SNB will increase under A. retroflexus invasion. Second, SND exerts a positive effect on the diversity and richness of SNB. Third, the diversity and richness of SNB may be increased under A. retroflexus invasion treatment with SND.

Section snippets

Experimental design

In this study, A. retroflexus was chosen as the target IPS because this species has been listed as a destructive and widespread invasive species in China (Yang et al., 2011, Ma et al., 2012). Seeds of A. retroflexus were collected from Zhenjiang (32.20°N, 119.51°E). The sampling area has a subtropical humid climate. The annual mean temperature in the area is approximately 15.6 °C, and its monthly mean temperature reaches a maximum of approximately 25 °C in July and decreases to a minimum of

Soil physicochemical properties

Differences were observed among soil physicochemical properties under different treatments (Table 1). In particular, the mean value of soil pH increased with different types of plant cultivation, in the following order: independent cultivation of invasive A. retroflexus, co-cultivation of invasive A. retroflexus and native A. tricolor, and independent cultivation of native A. tricolor (Table 1). By contrast, the mean value of soil electrical conductivity decreased over the same order of plant

Discussion

Some studies have found that some IPS can mediate soil alkalization (Fan et al., 2010, Kuebbing et al., 2014) mainly due to the selective absorption of N forms required for plants (Ehrenfeld, 2003, Chen et al., 2012) and/or the released alkaline substances originating from the litters and/or root exudates of IPS (Dassonville et al., 2011, Chen et al., 2012). Amaranthus retroflexus invasion increased the acidification of the soil in this study, although the change was not substantial. This

Conclusions

The purpose of this study was to gain insights into the effects of the invasive plant A. retroflexus on the structure and diversity of SNB across a gradient of SND. Results showed that the diversity and richness of SNB decreased under A. retroflexus invasion. The reason may be due to the altered soil nutrient content mediated by the root exudates released from A. retroflexus, and/or the decreased soil pH triggered by the invasion of A. retroflexus. OTU richness, the ACE index, and the Chao1

Acknowledgements

We greatly appreciate to BioMarker Technologies Co., Ltd., Beijing, China for the determination of soil N-fixing bacteria community structure using high throughput sequencing. This study was supported by National Natural Science Foundation of China (31300343, 31570414), Natural Science Foundation of Jiangsu Province, China (BK20130500), Open Science Research Fund of State Key Laboratory of State Key Laboratory of Soil and Sustainable Agriculture, China (Y20160023), Jiangsu Collaborative

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