Next Article in Journal
Study on the Parameters of Strengthening Soft Surrounding Rock by Electric Pulse Grouting in the Mining Face
Next Article in Special Issue
Effects of Exiguobacterium sp. DYS212, a Saline-Alkaline-Tolerant P-Solubilizing Bacterium, on Suaeda salsa Germination and Growth
Previous Article in Journal
Soil Amendment with a Lignite-Derived Humic Substance Affects Soil Properties and Biomass Maize Yield
Previous Article in Special Issue
Soil Microbial Communities in Desert Grassland around Rare Earth Mine: Diversity, Variation, and Response Patterns
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 15
Issue 3
10.3390/su15032315
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Comparison of Bacterial Diversity in the Rhizosphere of Chromolaena odorata (L.) R.M. King and H.Rob. in Different Habitats

by
Xinying Ni
1,2,
Caiyun Zhao
1,*,
Junsheng Li
3,
Bai Li
1 and
Jinfang Zhu
1
1
State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China
2
School of Ecology, Lanzhou University, Lanzhou 730000, China
3
China National Accreditation Service for Conformity Assessment, Beijing 100062, China
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(3), 2315; https://doi.org/10.3390/su15032315
Submission received: 9 December 2022 / Revised: 17 January 2023 / Accepted: 19 January 2023 / Published: 27 January 2023
(This article belongs to the Special Issue Biodiversity Conservation and Environmental Sustainability)
Browse Figures
Review Reports Versions Notes

Abstract

:
The invasion of Chromolaena odorata (L.) R.M. King and H.Rob. affects microbial community structure, but seldom do studies focus on bacterial diversity in the rhizosphere of C. odorata from different habitats. To reveal the impacts of C. odorata on bacterial communities in different habitats, diversity and functional groups of bacteria were compared in the rhizosphere soil of C. odorata collected from three habitats: abandoned land, a mature eucalyptus forest (eight-years), and a young eucalyptus forest (one-year). In this study, 3701 OTUs (operational taxonomic units) were obtained by next-generation sequencing. Simpson diversity indexes of bacteria in eucalyptus forests were significantly higher than that in abandoned land. Based on PCoA analysis, significant differences in the composition of bacterial communities were observed among the three habitats. Significant differences in bacterial communities among the three habitats were also demonstrated by biomarkers based on linear discriminant analysis effect size (LEfSe) analysis. Functional prediction analysis showed that the abundance of nitrogen-fixing functional genes in eucalyptus forests was greater than that in abandoned land. Canonical correspondence analysis (CCA) found that the biomass of C. odorata, soil pH, and total phosphorus were the main factors that impacted the microbial community structure. The results highlight the microbial community varied with habitats invaded by C. odorata, providing new evidence for understanding the invasion of C. odorata in different habitats.

1. Introduction

Biological invasion is recognized globally as the second largest cause of biodiversity loss [1]. It directly threatens biodiversity and natural resource management in the invaded areas, especially in nature reserves [2]. Successful invasion is determined by various factors such as habitat type, human activities, and climatic conditions, as well as their interaction [3]. Soil microbial communities play an essential role in the successful invasion process of alien plants [4,5,6]. The enhanced mutualism hypothesis postulates that invasive plants promote self-growth by enriching beneficial microbes to establish positive soil feedback [7,8]. Microbes can facilitate nutrient acquisition in plants [9,10], defend against pests and diseases [11], and help plants withstand abiotic stresses [12]. Plant–soil feedback (PSF) is a plant-induced change in the abiotic soil environment and the soil community structure and function, which in turn affects the subsequent establishment and growth of plants [13]. Callaway et al. [14] found that the invasive plant Centaurea maculosa auct. non Lam. developed a unique rhizosphere microbial community that promoted its invasion. Plant-growth-promoting rhizobacteria (PGPR) is a class of naturally occurring beneficial soil bacteria that colonize the rhizosphere of plants. Many PGPR, such as Bacillus, Klebsiella, and Pseudomonas, have been found to promote plant growth through nitrogen fixation, production of phytohormones (e.g., gibberellins), and increased abiotic stress tolerance [15,16,17,18,19,20]. However, the relationship between invasive plants and rhizosphere symbiotic microorganisms can cause functional differences due to habitat differences, geographical isolation, and competitive relationships [21]. A study of the aquatic invasive plant Zizania latifolia (Griseb.) Turcz.ex Stapf found that rhizosphere microorganisms varied widely among the four habitats and may have contributed to its invasion [22]. Research on the rhizosphere microorganisms of the same plant in different habitats deepens the understanding of the mechanism for the successful invasion of alien plants.
Chromolaena odorata, a perennial herb of the family Asteraceae, originated in southern Mexico, Central and South America, and the West Indies. It is considered a harmful invasive weed to agriculture and forestry in many countries in Asia, Oceania, and Africa [23]. Previous studies on the invasion mechanism of C. odorata have focused on phenotypic plasticity aspects, genetic differentiation, chemosensory effects, and microorganisms [24,25]. Among them, the evolution of increased competitive ability (EICA) hypothesis and the novel weapons hypothesis (NWH) are the main mechanisms for the invasion of C. odorata. C. odorata may evolve enhanced competitive ability by increasing the production of new allelochemicals [26]. The evolution of increased competitive ability can also be associated with soil microorganisms. Previous studies have compared the rhizosphere microbes of C. odorata with those of other invasive and native plants and found that the invasion of C. odorata can increase the number of bacteria associated with soil nutrient cycling, thus enhancing the ability of C. odorata to utilize soil nutrients and promote its growth and competition [27]. However, habitat heterogeneity of rhizosphere microorganisms and functional bacteria of C. odorata was still not reported, especially in nature reserves.
In this research, we hypothesized that the diversity and composition of bacterial communities in the rhizosphere of C. odorata varied with habitats. Concomitantly, we also hypothesized the invasion of C. odorata benefits from different bacterial functional groups in different habitats. Moreover, we supposed that the invasion of C. odorata and habitat characteristics all impacted the bacterial communities within three habitats. All these hypotheses were examined by collecting the rhizosphere soil of C. odorata, which had invaded three types of habitats in Guangxi Encheng National Nature Reserve: mature eucalyptus forests, young eucalyptus forests, and abandoned lands.

2. Materials and Methods

2.1. Study Area and Sampling

Our sampling site is located in Guangxi Encheng National Nature Reserve (106°58′16″~107°15′36″ E, 22°36′29″~22°50′5″ N) in southwest China (Figure 1). The reserve area is 258.176 km2. The nature reserve has a northern tropical monsoon climate. Due to the complex and changeable terrain of the nature reserve, the climate differs in the low mountains, peaks, valleys, and depressions. The annual average sunshine hours are 1597 h, the annual average temperature is 21.3 °C, the annual average precipitation is 1362 mm, and there are obvious dry and rainy seasons. It is one of the areas with a serious invasion of C. odorata [28]. C. odorata invasion often form dominant communities not only in abandoned lands but also in plantation forests.
In July 2021, we selected three habitats in Encheng Nature Reserve: a young eucalyptus forest, a mature eucalyptus forest, and abandoned land. These three habitats are located in the experimental area and at lower altitudes (Table 1) with similar climate environments. In each habitat, three 4 × 4 m plots were set up in the invaded community of C. odorata and three 1 × 1 m subplots were sampled randomly. A total of 3 C. odorata individual samples were randomly selected in each subplot, and rhizospheric soil was collected after shaking the loose soil from the roots, resulting in a total of 27 soil samples. Then, the rhizospheric soil samples of three C. odorata individuals in each subplot were mixed into one soil sample. Thus, a total of 9 rhizospheric soil samples were finally collected. All the whole plants of C. odorata in the quadrate were pulled up, and the attached soil was shaken off and taken back to the laboratory. Then, three medium-sized C. odorata were selected and brought back to the laboratory. The whole plant was dried to a constant weight in an oven at 65 °C for 120 h until reaching a constant weight. Then the dry weight was used to calculate the total biomass of C. odorata in the quadrat. The number of individual C. odorata in each subplot was also counted as the density of C. odorata. The rhizosphere soil of C. odorata in the abandoned land was named A, that of C. odorata in the young eucalyptus forest was named B, and that of C. odorata in the mature eucalyptus forest was named C. The rhizosphere soils were stored at −20 ℃ for microbial analyses. The fine roots and impurities in each sample were removed by sieving (2 mm) and prepared for use. The physical and chemical parameters of the soil samples, including pH, soil organic carbon (SOC), total nitrogen (TN), ammonium nitrogen (NH4+-N), nitrate nitrogen (NO3−-N), total phosphorus (TP), and total potassium (TK), were measured. Soil pH was determined by the electrode method (distilled water extract, soil–water ratio of 1:5); SOC was determined by the potassium dichromate volumetric method; TN was determined using the Kjeldahl method; NH4+ and NO3− were determined by KCl solution extraction spectrophotometry; TP was determined using NaOH alkali fusion–molybdenum antimony spectrophotometry; and TK was determined by hydrofluoric acid–perchloric acid solution decoction and flame photometry [29,30].

2.2. Soil Microbe Determination and Analysis

Total DNA was extracted from 200~–500 mg of each homogenized soil sample using the E.Z.N.A™ Mag-Bind Soil DNA Kit. DNA integrity was tested on agarose gels, and DNA sample concentration was quantified by Qubit. The V3–V4 region of the bacterial 16S rRNA gene was amplified using region universal primers (341F: 5’-CCTACGGGNGGCWGCAG-3’, 805R: 5’-GACTACHVGGGTATCTAATCC-3’). The original image data files obtained from Illumina Miseq™ 400 platformwere converted into sequenced reads by base calling analysis, and the sequenced sequences contained barcode sequences, as well as primer and splice sequences added during sequencing. Using Usearch, non-redundant sequences were extracted from the optimized sequences of each sample to facilitate the reduction of redundant computations in the middle of the analysis [31]. After the redundant sequences of all samples were combined, the non-redundant sequences (excluding single sequences) were clustered in an operational taxonomic unit (OTU) according to 97% similarity, and the chimeras were removed in the clustering process to obtain the representative sequences of the OTU. All the optimized sequences were compared to the OTU representative sequences, and sequences with 97% or more similarity to the representative sequences were selected to generate OTU tables. The RDP database was compared using the RDP classifier, which is based on Bergey’s taxonomy, and the naïve Bayesian assignment algorithm was used to calculate the probability value of each sequence at different levels of the hierarchy for its assignment to a particular level [32]. All the above sequencing work was completed by Sangon Biotech (Shanghai, China) Co., Ltd.

2.3. Statistical Analysis

Stacked bar graphs with clustering trees were drawn at the phylum level. Select OTUs with relative abundance greater than 1% were analyzed at the genus level, and the rest were defined as others, then the relative abundance heat map was plotted [29]. Phylum and genus level analyses were performed on Tutools platform (https://www.cloudtutu.com (accessed on 5 January 2023)), an online data analysis website. The species richness, Shannon-Winner, Simpson index, and Pielou index were all used in the analysis of α-diversity, and only the distinguished and different index was presented in the text. Statistically significant differences in soil physicochemical properties and microbial community diversity indices among sample groups were assessed by ANOVA followed by Tukey’s honest significant difference (HSD) post hoc test for multiple comparisons in SPSS v26.0. A principal coordinate analysis (PCoA) of microbial community composition was conducted to examine the differences between the microbial communities. Non-metric multidimensional scaling (NMDS) was used to evaluate the shifts of soil microbial community functions in different habitats. Weighted-normalized UniFrac distances were used in the PCoA and NMDS. We performed canonical correspondence analysis (CCA) with a forwarding selection of soil variables by variance inflation factors (VIFs) < 20. The above analyses were performed using the vegan package in R (version 4.2.1). The potential functions of the rhizosphere bacterial communities in different habitats were predicted using FAPROTAX analysis software(version 4.2.1); subsequently, the top ten functional annotated information of relative abundance were selected to plot the relative abundance heat map. Linear discriminant analysis (LDA) used LEfSe software for biomarkers with statistical differences (LDA score > 3).

3. Results

3.1. Invasion Characteristics and Soil Physicochemical Properties of Chromolaena odorata in Three Habitats

The results of the soil physicochemical analysis showed that soil TK, pH, NH4+, and NO3− differed among the three habitats. TK and pH were significantly higher in the abandoned land habitat than in the two eucalyptus forest habitats and lower in the mature eucalyptus forest than in the young eucalyptus forest. NH4+ was significantly higher in the young eucalyptus forest than in the other two habitats, and NO3− was significantly higher in the mature eucalyptus forest than in the other two habitats. No difference was found for the SOC among the three habitats (Table 2). The biomass of C. odorata was highest in the abandoned land, reaching 0.64 ± 0.09 kg/m2, followed by the mature eucalyptus forest. The density of C. odorata was highest in the mature eucalyptus forest, reaching 97.33 ± 32.04, and lowest in the abandoned land, 10.56 ± 2.99.

3.2. Community Composition of Rhizosphere Bacteria of Chromolaena odorata

The microbial sequencing data of the soil samples were processed to obtain 715,672 total bacterial sequences with an average sequence length of 415.12 bp. A total of 3701 OTUs were obtained from the sequence partitioning, with 1335 OTUs in the three habitats, including 549 OTUs specific to abandoned land, 177 OTUs specific to young eucalyptus forest, and 204 OTUs specific to mature eucalyptus forest, 310 OTUs shared between abandoned land and young eucalyptus forest, 229 OTUs shared between abandoned land and mature eucalyptus forest, and 897 OTUs shared between the two eucalyptus forests (Figure 2).
The results showed that the number of phyla measured in the three habitats was similar with Proteobacteria, Acidobacteria, Actinobacteria, Verrucomicrobia and Planctomycetes as the dominant phyla (Figure 3A). However, the relative abundances of Acidobacteria and Planctomycetes in the rhizosphere soil of C. odorata in the abandoned land were lower than those in both the young and mature eucalyptus forests.
The results of the rhizosphere bacteria genus level analysis of C. odorata in the three habitats showed that the bacterial abundance of the two eucalyptus plantations was similar, with GP1, unclassified Rhizobiales, Burkholderia, Bradyrhizobium, and GP2 as the dominant genera. The abundance of bacteria in the abandoned land was significantly different from that in the eucalyptus forests. The relative abundance of Sphingomonas, unclassified_Bacteria, unclassified Betaproteobacteria, GP6, and GP4 in the abandoned land was relatively high (Figure 3B).

3.3. Diversity of Rhizosphere Bacterial Community of Chromolaena odorata

One-way ANOVA showed that the Simpson index was significantly lower in the abandoned land (0.9849 ± 0.0033) than in the young eucalyptus forest (0.9929 ± 0.0004, p = 0.027) and the mature eucalyptus forest (0.9924 ± 0.0002, p = 0.034), while there was no significant difference between the two eucalyptus forests (p = 0.861). The other indices were not significantly different (Figure 4A). The results of the principal coordinate analysis (Figure 4B) showed that the sum of the two principal axes explained 83.57% of the variation in microbial diversity. The rhizospheric bacterial communities of C. odorata in the different habitats did not overlap with each other, indicating differences in the species composition of C. odorata and rhizospheric bacteria in the different habitats. The young and mature eucalyptus forest samples are clustered to each other in the figure, which indicates a more similar species composition between the two types of soil.

3.4. Functional Prediction of Rhizosphere Bacteria of Chromolaena odorata

The functional compositions of all samples from the three habitats were essentially unchanged, but there were differences in the relative abundance of different functional genes (Figure 5A). Chemoheterotrophy, aerobic chemoheterotrophy, nitrate reduction, chitinolysis, nitrification, etc., were mainly present in the three habitats. The sequencing of predicted metabolic functions indicated that the functional genes varied significantly between the eucalyptus forests and the abandoned land (Figure 5B).
In the LEfSe analysis plot (Figure 5C), the biomarkers of significant differences in the abandoned land were concentrated in GP6, GP4, Ilumatobacter, Gaiella, Solirubrobacter, Chryseolinea, Sphingomonas, Povalibacter, and Lysobacter. The biomarkers with significant differences in the young eucalyptus forest were concentrated in WPS-2 genera incertae sedis, unclassified Rhodospirillales, unclassified Rhizobiales, GP3, Mycobacterium, unclassified streptosporangneae, while the biomarkers in the mature eucalyptus forest were concentrated in Alphaproteobacteria, unclassified Nannocystineae, Bacillus, and Rhizomicrobium.

3.5. Analysis of Influence Factors of Rhizosphere Bacterial Community

In the CCA analysis of the C. odorata rhizospheric soil microbiome, Axis 1 explained 41.28% of the total variance, while Axis 2 explained 13.28% (Figure 6). The results showed that soil pH, the biomass of C. odorata, and TP showed stronger correlations with the first canonical axis (CCA1). The biomass of C. odorata, soil pH, and TP had strong positive correlation effects on the bacterial community structure of the rhizosphere soil samples from the abandoned land. In contrast, these environmental factors negatively correlated with the bacterial community structures of the two eucalyptus forests.

4. Discussion

Soil microorganisms often change their communities to adapt to the physical and chemical environment of their habitats for better growth and development [33], and the rhizosphere microorganisms of invasive species are not only influenced by their habitats but also closely related to the invasive species [22]. In this study, the Simpson diversity index was found to be significantly lower in the abandoned land than in the eucalyptus forests, indicating higher diversity in the eucalyptus forests. High plant rhizosphere bacterial diversity can improve plant nutrient use efficiency and increase plant biomass through synergistic interactions between different microorganisms [34]. The experimental results of Zhang et al. similarly showed that invasive plants were able to influence the soil biotope through the root system, thereby enhancing the effect of plant invasion on the abundance or biomass of certain components of the community and enhancing nutrient cycling, thus facilitating the invasion of invasive alien plants [35].
Linear discriminant analysis effect size (LEfSe) can help reveal differences between groups across different samples or environments, and find biomarkers with statistical differences among groups [36]. Based on LEfSe analysis, it was evident that the rhizosphere of C. odorata in different habitats contains specific microbiomes. In addition, a variety of PGPR may be associated with the successful invasion of C. odorata [37]. Plant-associated bacteria often have some plant-growth-promoting traits (PGPTs), such as nitrogen metabolism, production of IAA, and phosphorus metabolism [38]. In the analysis of key species in the mature forest of eucalyptus, mainly Bacillus and others were the key species. Among them, the Bacillus species are an important agricultural microbial resource that are commonly found in soil, animal guts, air, water, and plants, solubilizing insoluble phosphorus, potassium, and other compounds, and are defined as important beneficial bacteria [39,40]. It has been found that the invasion of Ageratina adenophora promoted an increase in Bacillus cereus, a common plant rhizosphere nitrogen-fixing bacterium, which in turn exerted a positive feedback effect on the growth of A. adenophora [41,42]. Thus, the accumulation of Bacillus in the mature eucalyptus forest may increase the efficiency of nitrogen fixation in the rhizosphere soil of C. odorata, thereby promoting growth. In contrast, the significantly different species in the abandoned land were concentrated in GP6, GP4, Gaiella, Sphingomonas, and Lysobacter. Most of these key species may help C. odorata adapt to the poor soil environment. Firstly, it has been demonstrated that Gaiella species, as beneficial bacteria in the plant rhizosphere, contribute to the ability of Boehmeria nivea to tolerate poor soils [43]. Therefore, we deduced that the enrichment of Gaiella may contribute to the successful invasion of C. odorata in abandoned land. Secondly, Acidobacteria, as one of the most abundant phyla in the plant rhizosphere, plays an important role in soil carbon and nitrogen cycling [44]. Acidobacteria is clearly defined as an oligotrophic bacterial phylum, and oligotrophic taxa dominate in soils with low organic carbon availability [45]. Gp4, isolated from African savanna soils, has shown cytoplasmic extension morphologically, thus suggesting adaptations in nutrient uptake by Gp4 in nutrient-poor environments, similar to our findings [46]. Therefore, rhizosphere aggregation of specific functional bacteria in different habitats of C. odorata could help C. odorata adapt to different environmental conditions, such as the accumulation of microorganisms more adapted to survive in poor soil environments in abandoned land, and the accumulation of microorganisms related to the nitrogen cycle in eucalyptus forests, thus promoting its invasive expansion. This is consistent with our hypothesis that the diversity and composition of bacterial communities in the rhizosphere of C. odorata varied with habitats.
FAPROTAX analysis mapped the classification annotation results of 16S rRNA amplification sequencing to the database, so as to annotate and predict the microbial community metabolism or ecologically relevant functions. Many papers have well annotated the function of soil microorganisms through FAPROTAX analysis [47]. In this study, differences were found in the function of the rhizosphere bacterial communities of C. odorata in three habitats. The abundance of nitrogen fixation function in the eucalyptus forests was greater than that in the abandoned land, which was consistent with the results of NH4+ content in the soil. In general, in the process of alien plant invasion, the functional groups of soil microorganisms play an important role because they can alter soil nutrient cycling and affect soil nitrogen mineralization [48,49]. Previous research has determined that alien plants can alter the diversity and abundance of specific functional groups of soil microorganisms [50,51]. Changes in soil microbial communities that regulate soil nutrient effectiveness may affect nutrient acquisition capacity and thus produce positive feedback on the growth of invasive plants. Invasive alien plants affect the abundance and diversity of nitrogen-fixing soil bacteria, which may cause changes in the available N content in soil [52]. For example, Acacia dealbata increases the available soil carbon source and enhances biological nitrogen fixation efficiency through a large number of dead leaves, thus changing soil nutrients and affecting the structure and function of soil microbial communities [53]. In our study, the difference in the functional abundance of nitrogen fixation may be due to the aggregation of PGPR, such as Rhizobium and Bacillus, that promote plant growth by performing nitrogen fixation in C. odorata in eucalyptus forests [54,55]. Moseman also demonstrated that the increase in the abundance and diversity of nitrogen-fixing bacteria (NFB) could facilitate plant invasion by increasing nitrogen input [56,57]. Therefore, consistent with our hypothesis, the difference of nitrogen fixation function between eucalyptus forests and abandoned land may be closely related to the difference of soil nutrient content and the growth of C. odorata.
In this study, we found that nitrate and ammonia nitrogen were significantly higher in the eucalyptus habitats than in the abandoned land habitat, and light intensity was lower in the eucalyptus forests than in the abandoned land, while C. odorata was able to adjust and respond positively to changes in light intensity in some physiological characteristics (e.g., regulation of photosynthetic capacity, biomass allocation, and phenotypic plasticity) [25,58]. Because the shaded environmental conditions of the eucalyptus forests were not conducive to the growth of C. odorata, we can deduce that more complex bacterial communities are needed to promote the soil N use efficiency of C. odorata in eucalyptus forests. In the present study, we also found that the nitrogen-fixing functional group increased significantly in the eucalyptus forests, so it is possible that the nitrogen-fixing bacterial community enhanced the soil fast-acting N content and allocated more N to photosynthesis [29], thus facilitating the adaptation of C. odorata to unfavorable environmental conditions [59]. In previous studies, nitrogen-fixing bacteria played a key role in the process of plant invasion; for example, Mikania micrantha-enriched microorganisms participated in the N cycle and led to increased nitrogen effectiveness, which, then, increased the N content of the plants’ photosynthetic tissues, thus promoting the growth of M. micrantha [60]. The key roles of soil characteristics and plant species in shaping rhizosphere microbial communities have been mentioned in many studies. Therefore, the differences in the rhizosphere bacteria in this study may be explained by a combination of habitat and C. odorata invasion, and the differences in the functional bacterial communities, especially the enrichment of nitrogen-fixing bacteria in eucalyptus forests, may promote the adaptation of C. odorata to different habitats.
Of course, some limitations still existed in this study. First, although we found bacterial communities varied in different habitats related to the biomass of C. odorata and soil physicochemical properties, such as total phosphorus and pH, we cannot disentangle the effects of the habitats and invasion of C. odorata. Controlled experiments were needed to explore the relationship between rhizosphere microorganisms and invasion of C. odorata. Second, it remained unclear whether changes of soil bacterial communities induced feedback to the growth of the invader. Therefore, future large-scale studies are required to test whether the rhizospheric soil of C. odorata promotes plant growth compared to non-rhizospheric soil.

5. Conclusions

Our study found that the diversity and composition of the rhizosphere soil bacterial communities of C. odorata in the three habitats differed significantly and that the composition of the functional groups might help C. odorata adapt to different habitats, which is consistent with our hypothesis. The results suggested that C. odorata invasion can accumulate different functional bacteria to adapt to different habitat conditions, alter soil nutrient cycling, especially N use, and thus facilitate invasion. We also found that the biomass of C. odorata can explain the variation of soil bacterial communities in different habitats. This result indicates the various impacts of the invasion of C. odorata. However, knowledge of the plant-soil feedback between bacterial communities and C. odorata must be improved. We suggest that considering a habitat’s heterogeneity of plant-soil feedbacks can help to understand the successful invasion of C. odorata. Moreover, the response of native plants and ecosystems to the modifications of the soil environment initiated by invasions of C. odorata should be studied in the future.

Author Contributions

Conceptualization, C.Z. and X.N.; methodology, J.L.; software, X.N. and J.Z.; formal analysis, X.N.; investigation, X.N. and B.L.; data curation, X.N. and J.Z.; writing—original draft preparation, X.N.; writing—review and editing, X.N. and C.Z.; visualization, X.N. and J.Z.; supervision, C.Z. and J.L.; project administration, J.L. and C.Z.; funding acquisition, J.L. and C.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Key Research and Development Program of China (2020YFC1806300, 2016YFC1201100, 2017YFC0506200) and the Special Fund of Chinese Central Government for Basic Scientific Research Operation in Commonweal Research Institutes (2022YSKY-08).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author (e-mail: [email protected]).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Bellard, C.; Cassey, P.; Blackburn, T.M. Alien species as a driver of recent extinctions. Biol. Lett. 2016, 12, 20150623. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Foxcroft, L.C.; Pysek, P.; Richardson, D.M.; Pergl, J.; Hulme, P.E. The Bottom Line: Impacts of Alien Plant Invasions in Protected Areas. In Plant Invasions in Protected Areas: Patterns, Problems and Challenges; Foxcroft, L.C., Pysek, P., Richardson, D.M., Genovesi, P., Eds.; Invading Nature-Springer Series in Invasion Ecology; Springer: Berlin/Heidelberg, Germany, 2013; Volume 7, pp. 19–41. [Google Scholar]
  3. Milbau, A.; Stout, J.C.; Graae, B.J.; Nijs, I. A hierarchical framework for integrating invasibility experiments incorporating different factors and spatial scales. Biol. Invasions 2009, 11, 941–950. [Google Scholar] [CrossRef]
  4. Steinlein, T. Invasive Alien Plants and Their Effects on Native Microbial Soil Communities. In Progress in Botany 74; Luttge, U., Beyschlag, W., Francis, D., Cushman, J., Eds.; Progress in Botany; Springer: Berlin/Heidelberg, Germany, 2013; Volume 74, pp. 293–319. [Google Scholar]
  5. Zhang, Z.; Liu, Y.; Brunel, C.; van Kleunen, M. Soil-microorganism-mediated invasional meltdown in plants. Nat. Ecol. Evol. 2020, 4, 1612–1621. [Google Scholar] [CrossRef] [PubMed]
  6. Bates, S.E.; Wandrag, E.M.; Barrett, L.G.; Thrall, P.H.; Duncan, R.P. Soil biotic effects and competition; What are the mechanisms behind being a successful invader? Pedobiologia 2021, 87–88, 150749. [Google Scholar] [CrossRef]
  7. Bever, J.D. Soil community feedback and the coexistence of competitors: Conceptual frameworks and empirical tests. New Phytol. 2003, 157, 465–473. [Google Scholar] [CrossRef] [Green Version]
  8. Reinhart, K.O.; Callaway, R.M. Soil biota facilitate exotic Acer invasions in Europe and North America. Ecol. Appl. 2004, 14, 1737–1745. [Google Scholar] [CrossRef] [Green Version]
  9. Richardson, A.E.; Barea, J.-M.; McNeill, A.M.; Prigent-Combaret, C. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 2009, 321, 305–339. [Google Scholar] [CrossRef]
  10. Ahemad, M.; Kibret, M. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. J. King Saud Univ. Sci. 2014, 26, 1–20. [Google Scholar] [CrossRef] [Green Version]
  11. Yu, K.; Pieterse, C.M.J.; Bakker, P.A.H.M.; Berendsen, R.L. Beneficial microbes going underground of root immunity. Plant Cell Environ. 2019, 42, 2860–2870. [Google Scholar] [CrossRef] [Green Version]
  12. Marasco, R.; Rolli, E.; Ettoumi, B.; Vigani, G.; Mapelli, F.; Borin, S.; Abou-Hadid, A.F.; El-Behairy, U.A.; Sorlini, C.; Cherif, A.; et al. A Drought Resistance-Promoting Microbiome Is Selected by Root System under Desert Farming. PLoS ONE 2012, 7, e48479. [Google Scholar] [CrossRef]
  13. Van der Putten, W.H.; Bardgett, R.D.; Bever, J.D.; Bezemer, T.M.; Casper, B.B.; Fukami, T.; Kardol, P.; Klironomos, J.N.; Kulmatiski, A.; Schweitzer, J.A.; et al. Plant-soil feedbacks: The past, the present and future challenges. J. Ecol. 2013, 101, 265–276. [Google Scholar] [CrossRef]
  14. Callaway, R.M.; Thelen, G.C.; Rodriguez, A.; Holben, W.E. Soil biota and exotic plant invasion. Nature 2004, 427, 731–733. [Google Scholar] [CrossRef]
  15. Vacheron, J.; Desbrosses, G.; Bouffaud, M.-L.; Touraine, B.; Moenne-Loccoz, Y.; Muller, D.; Legendre, L.; Wisniewski-Dye, F.; Prigent-Combaret, C. Plant growth-promoting rhizobacteria and root system functioning. Front. Plant Sci. 2013, 4, 356. [Google Scholar] [CrossRef] [Green Version]
  16. Hoque, M.N.; Hannan, A.; Imran, S.; Paul, N.C.; Mondal, M.F.; Sadhin, M.M.R.; Bristi, J.M.; Dola, F.S.; Abu Hanif, M.; Ye, W.; et al. Plant Growth-Promoting Rhizobacteria-Mediated Adaptive Responses of Plants Under Salinity Stress. J. Plant Growth Regul. 2022. [Google Scholar] [CrossRef]
  17. Yadegari, M.; Rahmani, H.A.; Noormohammadi, G.; Ayneband, A. Plant Growth Promoting Rhizobacteria Increase Growth, Yield and Nitrogen Fixation in Phaseolus vulgaris. J. Plant Nutr. 2010, 33, 1733–1743. [Google Scholar] [CrossRef]
  18. Cassan, F.; Vanderleyden, J.; Spaepen, S. Physiological and Agronomical Aspects of Phytohormone Production by Model Plant-Growth-Promoting Rhizobacteria (PGPR) Belonging to the Genus Azospirillum. J. Plant Growth Regul. 2014, 33, 440–459. [Google Scholar] [CrossRef]
  19. Backer, R.; Rokem, J.S.; Ilangumaran, G.; Lamont, J.; Praslickova, D.; Ricci, E.; Subramanian, S.; Smith, D.L. Plant Growth-Promoting Rhizobacteria: Context, Mechanisms of Action, and Roadmap to Commercialization of Biostimulants for Sustainable Agriculture. Front. Plant Sci. 2018, 9, 1473. [Google Scholar] [CrossRef] [Green Version]
  20. Chen, L.; Li, K.; Shang, J.; Wu, Y.; Chen, T.; Wanyan, Y.; Wang, E.; Tian, C.; Chen, W.; Chen, W.; et al. Plant growth-promoting bacteria improve maize growth through reshaping the rhizobacterial community in low-nitrogen and low-phosphorus soil. Biol. Fertil. Soils 2021, 57, 1075–1088. [Google Scholar] [CrossRef]
  21. Rout, M.E.; Callaway, R.M. Interactions between exotic invasive plants and soil microbes in the rhizosphere suggest that ‘everything is not everywhere’. Ann. Bot. 2012, 110, 213–222. [Google Scholar] [CrossRef] [Green Version]
  22. Zhou, B.; Liu, Z.; Yang, G.; He, H.; Liu, H. Microbial activity and diversity in the rhizosphere soil of the invasive species Zizania latifolia in the wetland of Wuchang Lake, China. Mar. Freshw. Res. 2020, 71, 1702–1713. [Google Scholar] [CrossRef]
  23. Goodall, J.M.; Erasmus, D.J. Review of the status and integrated control of the invasive alien weed, Chromolaena odorata, in South Africa. Agric. Ecosyst. Environ. 1996, 56, 151–164. [Google Scholar] [CrossRef]
  24. Liao, Z.-Y.; Scheepens, J.F.; Li, Q.-M.; Wang, W.-B.; Feng, Y.-L.; Zheng, Y.-L. Founder effects, post-introduction evolution and phenotypic plasticity contribute to invasion success of a genetically impoverished invader. Oecologia 2020, 192, 105–118. [Google Scholar] [CrossRef] [PubMed]
  25. Liao, Z.-Y.; Scheepens, J.F.; Li, W.-T.; Wang, R.-F.; Zheng, Y.-L.; Feng, Y.-L. Biomass reallocation and increased plasticity might contribute to successful invasion of Chromolaena odorata. Flora 2019, 256, 79–84. [Google Scholar] [CrossRef]
  26. Zheng, Y.-L.; Feng, Y.-L.; Zhang, L.-K.; Callaway, R.M.; Valiente-Banuet, A.; Luo, D.-Q.; Liao, Z.-Y.; Lei, Y.-B.; Barclay, G.F.; Silva-Pereyra, C. Integrating novel chemical weapons and evolutionarily increased competitive ability in success of a tropical invader. New Phytol. 2015, 205, 1350–1359. [Google Scholar] [CrossRef]
  27. Zhao, J.; Cao, L. Effects of invasive plants on soil microbial properties and soil enzyme activities of poplar forest in Hung-tse Lake Wetland. Ecol. Environ. Sci. 2018, 27, 2039–2046. [Google Scholar] [CrossRef]
  28. Li, W.; Song, Q.; Huang, R.; Zhao, J.; LI, Y.; Zhou, Q. Current status and conservation of Franois’ langurs (Trachypithecus francoisi) in Encheng National Nature Reserve in Guangxi, China. Acta Theriol. Sin. 2019, 39, 623–629. [Google Scholar] [CrossRef]
  29. Li, Q.; Wan, F.; Zhao, M. Distinct soil microbial communities under Ageratina adenophora invasions. Plant Biol. 2022, 24, 430–439. [Google Scholar] [CrossRef]
  30. Xu, Q.-Y.; Wang, D.; Quan, G.-M.; Xiang, H.-M.; Zhang, J.-E. Invasive Chromolaena odorata species specifically affects growth of its co-occurring weeds. Ann. N. Y. Acad. Sci. 2020, 1470, 57–66. [Google Scholar] [CrossRef]
  31. Edgar, R.C. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 2013, 10, 996–998. [Google Scholar] [CrossRef]
  32. Wang, Q.; Garrity, G.M.; Tiedje, J.M.; Cole, J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73, 5261–5267. [Google Scholar] [CrossRef]
  33. Nunan, N. The microbial habitat in soil: Scale, heterogeneity and functional consequences. J. Plant Nutr. Soil Sci. 2017, 180, 425–429. [Google Scholar] [CrossRef] [Green Version]
  34. Chen, Q.-L.; Ding, J.; Zhu, Y.-G.; He, J.-Z.; Hu, H.-W. Soil bacterial taxonomic diversity is critical to maintaining the plant productivity. Environ. Int. 2020, 140, 105766. [Google Scholar] [CrossRef]
  35. Zhang, P.; Li, B.; Wu, J.; Hu, S. Invasive plants differentially affect soil biota through litter and rhizosphere pathways: A meta-analysis. Ecol. Lett. 2019, 22, 200–210. [Google Scholar] [CrossRef] [Green Version]
  36. Chang, F.; He, S.; Dang, C. Assisted Selection of Biomarkers by Linear Discriminant Analysis Effect Size (LEfSe) in Microbiome Data. Jove-J. Vis. Exp. 2022, 183, e61715. [Google Scholar] [CrossRef]
  37. Nihorimbere, V.; Ongena, M.; Smargiassi, M.; Thonart, P. Beneficial effect of the rhizosphere microbial community for plant growth and health. Biotechnol. Agron. Soc. Et Environ. 2011, 15, 327–337. [Google Scholar]
  38. Cheng, D.; Tian, Z.; Feng, L.; Xu, L.; Wang, H. Diversity analysis of the rhizospheric and endophytic bacterial communities of Senecio vulgaris L. (Asteraceae) in an invasive range. Peerj 2019, 6, e6162. [Google Scholar] [CrossRef] [Green Version]
  39. Calvo, P.; Zebelo, S.; McNear, D.; Kloepper, J.; Fadamiro, H. Plant growth-promoting rhizobacteria induce changes in Arabidopsis thaliana gene expression of nitrate and ammonium uptake genes. J. Plant Interact. 2019, 14, 224–231. [Google Scholar] [CrossRef] [Green Version]
  40. Thiruvengadam, R.; Gandhi, K.; Vaithiyanathan, S.; Sankarasubramanian, H.; Loganathan, K.; Lingan, R.; Rajagopalan, V.R.; Muthurajan, R.; Iyadurai, J.E.; Kuppusami, P. Complete Genome Sequence Analysis of Bacillus subtilis Bbv57, a Promising Biocontrol Agent against Phytopathogens. Int. J. Mol. Sci. 2022, 23, 9732. [Google Scholar] [CrossRef]
  41. Sun, Y.-Y.; Zhang, Q.-X.; Zhao, Y.-P.; Diao, Y.-H.; Gui, F.-R.; Yang, G.-Q. Beneficial rhizobacterium provides positive plant-soil feedback effects to Ageratina adenophora. J. Integr. Agric. 2021, 20, 1327–1335. [Google Scholar] [CrossRef]
  42. Tilak, K.; Ranganayaki, N.; Pal, K.K.; De, R.; Saxena, A.K.; Nautiyal, C.S.; Mittal, S.; Tripathi, A.K.; Johri, B.N. Diversity of plant growth and soil health supporting bacteria. Curr. Sci. 2005, 89, 136–150. [Google Scholar]
  43. Wu, S.; Xue, S.; Iqbal, Y.; Xing, H.; Jie, Y. Seasonal Nutrient Cycling and Enrichment of Nutrient-Related Soil Microbes Aid in the Adaptation of Ramie (Boehmeria nivea L.) to Nutrient-Deficient Conditions. Front. Plant Sci. 2021, 12, 644904. [Google Scholar] [CrossRef] [PubMed]
  44. Lee, S.-H.; Ka, J.-O.; Cho, J.-C. Members of the phylum Acidobacteria are dominant and metabolically active in rhizosphere soil. Fems Microbiol. Lett. 2008, 285, 263–269. [Google Scholar] [CrossRef] [PubMed]
  45. Fierer, N.; Bradford, M.A.; Jackson, R.B. Toward an ecological classification of soil bacteria. Ecology 2007, 88, 1354–1364. [Google Scholar] [CrossRef] [PubMed]
  46. Huber, K.J.; Geppert, A.M.; Wanner, G.; Foesel, B.U.; Wuest, P.K.; Overmann, J. The first representative of the globally widespread subdivision 6 Acidobacteria, Vicinamibacter silvestris gen. nov., sp nov., isolated from subtropical savannah soil. Int. J. Syst. Evol. Microbiol. 2016, 66, 2971–2979. [Google Scholar] [CrossRef]
  47. Sansupa, C.; Wahdan, S.F.M.; Hossen, S.; Disayathanoowat, T.; Wubet, T.; Purahong, W. Can We Use Functional Annotation of Prokaryotic Taxa (FAPROTAX) to Assign the Ecological Functions of Soil Bacteria? Appl. Sci. 2021, 11, 688. [Google Scholar] [CrossRef]
  48. Ni, G.; Zhao, P.; Huang, Q.; Zhu, L.; Hou, Y.; Yu, Y.; Ye, Y.; Ouyang, L. Mikania micrantha invasion enhances the carbon (C) transfer from plant to soil and mediates the soil C utilization through altering microbial community. Sci. Total Environ. 2020, 711, 135020. [Google Scholar] [CrossRef]
  49. Capek, P.; Choma, M.; Tahovska, K.; Kana, J.; Kopacek, J.; Santruckova, H. Coupling the resource stoichiometry and microbial biomass turnover to predict nutrient mineralization and immobilization in soil. Geoderma 2021, 385, 114884. [Google Scholar] [CrossRef]
  50. Zhu, X.; Li, Q.; Li, Y.; Han, H.; Ma, K. Eupatorium adenophorum invasion alters soil bacterial community and diversity. Biodivers. Sci. 2015, 23, 665–672. [Google Scholar] [CrossRef] [Green Version]
  51. Li, S.; Xie, D.; Ge, X.; Dong, W.; Luan, J. Altered diversity and functioning of soil and root-associated microbiomes by an invasive native plant. Plant Soil 2022, 473, 235–249. [Google Scholar] [CrossRef]
  52. Wu, B.; Wang, S.; Wei, M.; Zhou, J.; Jiang, K.; Du, D.; Wang, C. The invasive tree staghorn sumac affects soil N-2-fixing bacterial communities in north China. Plant Biol. 2019, 21, 951–960. [Google Scholar] [CrossRef]
  53. Kamutando, C.N.; Vikram, S.; Kamgan-Nkuekam, G.; Makhalanyane, T.P.; Greve, M.; Le Roux, J.J.; Richardson, D.M.; Cowan, D.A.; Valverde, A. The Functional Potential of the Rhizospheric Microbiome of an Invasive Tree Species, Acacia dealbata. Microb. Ecol. 2019, 77, 191–200. [Google Scholar] [CrossRef] [Green Version]
  54. Lindstroem, K.; Mousavi, S.A. Effectiveness of nitrogen fixation in rhizobia. Microb. Biotechnol. 2020, 13, 1314–1335. [Google Scholar] [CrossRef]
  55. Yousuf, J.; Thajudeen, J.; Rahiman, M.; Krishnankutty, S.; Alikunj, A.P.; Abdulla, M.H.A. Nitrogen fixing potential of various heterotrophic Bacillus strains from a tropical estuary and adjacent coastal regions. J. Basic Microbiol. 2017, 57, 922–932. [Google Scholar] [CrossRef]
  56. Moseman, S.M.; Zhang, R.; Qian, P.Y.; Levin, L.A. Diversity and functional responses of nitrogen-fixing microbes to three wetland invasions. Biol. Invasions 2009, 11, 225–239. [Google Scholar] [CrossRef]
  57. Xu, C.-W.; Yang, M.-Z.; Chen, Y.-J.; Chen, L.-M.; Zhang, D.-Z.; Mei, L.; Shi, Y.-T.; Zhang, H.-B. Changes in non-symbiotic nitrogen-fixing bacteria inhabiting rhizosphere soils of an invasive plant Ageratina adenophora. Appl. Soil Ecol. 2012, 54, 32–38. [Google Scholar] [CrossRef]
  58. Quan, G.M.; Mao, D.J.; Zhang, J.E.; Xie, J.F.; Xu, H.Q.; An, M. Response of invasive Chromolaena odorata and two coexisting weeds to contrasting irradiance and nitrogen. Photosynthetica 2015, 53, 419–429. [Google Scholar] [CrossRef]
  59. Feng, Y.-L.; Lei, Y.-B.; Wang, R.-F.; Callaway, R.M.; Valiente-Banuet, A.; Inderjit; Li, Y.-P.; Zheng, Y.-L. Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc. Natl. Acad. Sci. USA 2009, 106, 1853–1856. [Google Scholar] [CrossRef] [Green Version]
  60. Yu, H.; Le Roux, J.J.; Jiang, Z.; Sun, F.; Peng, C.; Li, W. Soil nitrogen dynamics and competition during plant invasion: Insights from Mikania micrantha invasions in China. New Phytol. 2021, 229, 3440–3452. [Google Scholar] [CrossRef]
Sustainability 15 02315 g001 550
Figure 1. Sample sites in this study.
Figure 1. Sample sites in this study.
Sustainability 15 02315 g001
Sustainability 15 02315 g002 550
Figure 2. Venn diagram of microbial OTUs in the rhizosphere (blue: abandoned land; green: young eucalyptus forest; orange: mature eucalyptus forest).
Figure 2. Venn diagram of microbial OTUs in the rhizosphere (blue: abandoned land; green: young eucalyptus forest; orange: mature eucalyptus forest).
Sustainability 15 02315 g002
Sustainability 15 02315 g003 550
Figure 3. Bacterial community composition at different taxonomic levels: (A) phylum; (B) genus. A1–A3 represent samples from the abandoned land, B1–B3 represent samples from the young eucalyptus forest, and C1–C3 represent samples from the mature eucalyptus forest.
Figure 3. Bacterial community composition at different taxonomic levels: (A) phylum; (B) genus. A1–A3 represent samples from the abandoned land, B1–B3 represent samples from the young eucalyptus forest, and C1–C3 represent samples from the mature eucalyptus forest.
Sustainability 15 02315 g003
Sustainability 15 02315 g004 550
Figure 4. Alpha diversity in different habitats (A). Principal coordinate analysis of different soil microbial communities based on OTU data (B). The letters A, B, and C represent samples from the abandoned land, young eucalyptus forest, and mature eucalyptus forest. Different lowercase letters showed significant differences in diversity index (p < 0.05).
Figure 4. Alpha diversity in different habitats (A). Principal coordinate analysis of different soil microbial communities based on OTU data (B). The letters A, B, and C represent samples from the abandoned land, young eucalyptus forest, and mature eucalyptus forest. Different lowercase letters showed significant differences in diversity index (p < 0.05).
Sustainability 15 02315 g004
Sustainability 15 02315 g005 550
Figure 5. Functional composition of the soil bacterial communities (A); NMDS analysis of different soil bacterial communities based on functional prediction data (B); LEfSe analysis of differential bacterial species (C). The letters A, B, and C represent samples from the abandoned land, young eucalyptus forest, and mature eucalyptus forest.
Figure 5. Functional composition of the soil bacterial communities (A); NMDS analysis of different soil bacterial communities based on functional prediction data (B); LEfSe analysis of differential bacterial species (C). The letters A, B, and C represent samples from the abandoned land, young eucalyptus forest, and mature eucalyptus forest.
Sustainability 15 02315 g005
Sustainability 15 02315 g006 550
Figure 6. Canonical correspondence analysis of the influencing factors of the rhizosphere microbial communities.
Figure 6. Canonical correspondence analysis of the influencing factors of the rhizosphere microbial communities.
Sustainability 15 02315 g006
Table
Table 1. Summary of sample sites.
Table 1. Summary of sample sites.
SampleLongitudeLatitudeAltitudeFunctional ZoneOther
A107.09422.778229ExperimentalThe abandonment time is unknown, without trees, and shrubs, with grazing activities.
B106.97822.798378.53ExperimentalThe trees are 8 years old, with a density of 0.342 trees/m2, understory shrubs with Mussaenda pubescens Dryand.
C106.97922.793368ExperimentalThe trees are 1 year old, with a density of 0.188 trees/m2, understory shrubs with Vernicia fordii (Hemsl.) Airy Shaw
A, abandoned land; B, young eucalyptus plantation; and C, mature eucalyptus plantation.
Table
Table 2. Comparison of invasion characteristics and soil chemical properties of C. odorata in different habitats. The letters A, B, and C represent samples from abandoned land, young eucalyptus forest, and mature eucalyptus forest. Values (mean ± SE) followed by different letters in the same column indicate a significant difference at the p < 0.05 level.
Table 2. Comparison of invasion characteristics and soil chemical properties of C. odorata in different habitats. The letters A, B, and C represent samples from abandoned land, young eucalyptus forest, and mature eucalyptus forest. Values (mean ± SE) followed by different letters in the same column indicate a significant difference at the p < 0.05 level.
SamplepHSOC (g∙kg−1)NH4+-N (mg∙kg−1)NO3−-N (mg∙kg−1)TK (g∙kg−1)Biomass (kg)Density
A8.00 ± 0.04 a40.97 ± 7.75 a8.61 ± 1.43 b2.82 ± 1.57 b12.61 ± 0.49 a0.64 ± 0.09 a10.56 ± 2.99 b
B5.37 ± 0.14 b32.58 ± 6.26 a19.72 ± 4.52 a4.25 ± 0.95 b6.29 ± 0.41 b0.04 ± 0.02 b31.00 ± 7.81 b
C4.99 ± 0.09 c40.64 ± 0.64 a17.97 ± 1 ab13.65 ± 1.92 a6.26 ± 0.09 b0.19 ± 0.02 b97.33 ± 32.04 a
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Ni, X.; Zhao, C.; Li, J.; Li, B.; Zhu, J. Comparison of Bacterial Diversity in the Rhizosphere of Chromolaena odorata (L.) R.M. King and H.Rob. in Different Habitats. Sustainability 2023, 15, 2315. https://doi.org/10.3390/su15032315

AMA Style

Ni X, Zhao C, Li J, Li B, Zhu J. Comparison of Bacterial Diversity in the Rhizosphere of Chromolaena odorata (L.) R.M. King and H.Rob. in Different Habitats. Sustainability. 2023; 15(3):2315. https://doi.org/10.3390/su15032315

Chicago/Turabian Style

Ni, Xinying, Caiyun Zhao, Junsheng Li, Bai Li, and Jinfang Zhu. 2023. "Comparison of Bacterial Diversity in the Rhizosphere of Chromolaena odorata (L.) R.M. King and H.Rob. in Different Habitats" Sustainability 15, no. 3: 2315. https://doi.org/10.3390/su15032315

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop