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Contrasting plant growth performance of invasive polyploid and native diploid Prosopis is mediated by the soil bacterial community
Ecological Processes volume 12, Article number: 12 (2023)
Abstract
Background
Soil microbial communities affect above-ground plant diversity and community composition by influencing plant growth performance. Several studies have tested the effect of soil bacterial microbiome on growth performance of native and invasive plants, but the influence of specific bacterial isolates has not been investigated. Here, we investigated the effects of soil bacterial exclusion by soil sterilization and by inoculation of Streptomyces rhizobacterial isolates on the growth performance of native and invasive Prosopis congeners.
Results
Plant growth performance of invasive P. juliflora was significantly reduced when grown in sterilized soils, whereas native P. cineraria showed enhanced growth performance in the sterilized soils. When grown in the soil inoculated with the specific Streptomyces isolate from P. juliflora (PJ1), the growth performance of invasive P. juliflora was significantly enhanced while that of native P. cineraria seedlings was significantly reduced. However, inoculation of P. cineraria and P. juliflora seedlings with Streptomyces isolate from the rhizosphere of native P. cineraria (PC1) had no significant effect on the growth performances either of P. juliflora or P. cineraria.
Conclusion
Our study reveals that invasive P. juliflora experiences positive feedback from the non-native soil bacterial community, while the native P. cineraria experiences negative feedback from its soil bacterial community. Our results provide fresh experimental evidence for the enemy release hypothesis, and further our understanding of the contrasting growth-promoting effects of differentially recruited microbial species belonging to the same genus (Streptomyces) in the rhizospheres of alien invasive and native plants.
Background
Rapid spread of invasive plants and the resulting threat to native ecosystems, ecosystem services and their biodiversity is a global concern. Global trade and human cultural exchanges have resulted in numerous plant species navigating across geographical barriers and extending to new habitats (Kleunen et al. 2015). Many of these plants have got established as invasive species in the introduced ranges and have significantly affected the ecosystem services and regional economies (Bai et al. 2013). Invasive alien species experience several ecological interactions in their introduced ranges and the relative strength of such associations can impact their invasiveness (Catford et al. 2009; Traveset and Richardson 2020). Among various theories and models of plant invasion, enemy release hypothesis (ERH) offers the most plausible explanation for the rapid growth and establishment of exotic plant species (Keane and Crawley 2002). The core notion of this hypothesis is that exotic species are less negatively impacted by enemies in newly introduced surroundings than native species because they are freed from enemies like herbivores, parasites, or pathogens that may have constrained their growth in native ecosystems. The core tenet of this hypothesis is that natural enemies play a significant role in population regulation, and that the diminished regulation of exotic species by natural enemies is the primary driver of their increased abundance and spread outside of their native areas.
Soil microbes plays an important role in mediating the interaction between native and invasive plants as well as spread of the latter (Fahey and Florey 2022). For instance, the escape of invasive plant species from their co-evolved pathogens in non-native ranges provides them a competitive advantage over native plants (Mitchell and Power 2003; Allen et al. 2017), while some invasive plants are further endowed with microbial communities which directly inhibit growth of native plant species in their vicinity (Eppinga et al. 2006; Mangla et al. 2008; Flory and Clay 2013) or suppress the growth of microbes beneficial for the native plant communities (Bozzolo and Lipson 2013), suggesting that the microbial communities associated with exotic invasive plants play a significant role in shaping community structure of invaded ranges. Furthermore, soil mutualists such as rhizobia and mycorrhizal fungi can indirectly influence competitive interactions between native and invasive plants through differential effects on nutrient acquisition (Abbott et al. 2015; Marler et al. 1999), signifying that soil microbes can have substantial effects on plant community composition (Ehrenfeld et al. 2005; Mordecai 2011; Callaway and Rout 2010). Several studies have reported that invasive plants amend the endemic soil microbiome to facilitate their establishment in novel ranges (Si et al. 2013) and that plant–microbial interactions play an important role in mediating their establishment success in non-native range (Klironomos 2002; Van der Putten et al. 2007). However, there are limited studies on understanding the effects of specific microbial isolates associated with native and invasive plant species that impact their respective growth performances. Therefore, this study fills that gap and provides empirical evidence of the contrasting effects of specific bacterial isolates of the rhizospheres of native and invasive Prosopis congeners.
Prosopis genus comprises 44 species including some of the most aggressive invasive species in the world, like P. glandulosa, P. velutina, P. juliflora, and P. pallida (Burkart 1976; Pasiecznik et al. 2001). These invasive species have altered the global distribution patterns of other native plants, including its own non-invasive congeners like P. cineraria. Furthermore, P. juliflora is a polyploid across its invaded range (2n = 4x = 56), while its native congener, P. cineraria is a diploid (2n = 28) (Trenchard et al. 2008). Notably, the plant species with higher ploidy are shown to experience higher invasion success (Pandit et al. 2011; Te Beest et al. 2012) and often show better adaptability to fluctuating environments (Leitch and Leitch 2008; Richardson et al. 2000). Invasion success of exotic polyploids have been attributed to certain physiological characters such as enhanced ecological tolerance, higher growth and reproductive potential, efficient dispersal strategies, self-compatibility, and higher phenotypic plasticity (Baker 1965; Rejmanek and Richardson 1996; Pyšek and Richardson 2008). Furthermore, Thébault et al. (2010) compared the rhizosphere microbial activity between native and introduced cytotypes of Senecio inaequidens and found that a higher amount of microbial biomass carbon was associated with native and invasive tetraploids as compared to the native diploids. Similarly, in case of Centaurea stoebe, the soil bacterial diversity was higher in native tetraploids than native diploids and even higher in introduced tetraploids (Thébault et al. 2010), suggesting that ploidy impacts the microbial communities associated with a plant species which ultimately influences their establishment success in the introduced environment.
In an earlier study, involving native diploid and invasive polyploid Prosopis congeners, we established that selective enrichment of plant growth promoting communities from diverse phyla like Actinomycetota, Acidobacteria, Chloroflexi, etc., including higher abundance of pathways involved in antimicrobial synthesis and degradation, contributes to the invasion success of exotic polyploid Prosopis juliflora over its native diploid Prosopis cineraria (Kaushik et al. 2021). Higher abundance of antimicrobial pathways in P. juliflora rhizobiome was further corroborated by the presence of relatively higher proportion of Actinomycetota belonging to the genus Streptomyces using culture-based methods.
In this study, we investigated the role of soil microbes in mediating plant invasion by testing the effect of soil bacterial community on growth of native and invasive Prosopis congeners. We used microbial exclusion (soil sterilization) and reciprocal inoculation (inoculating rhizosphere bacteria of native species in the soils of invasive species and vice versa) experiments to assay the comparative growth performances of invasive and native Prosopis species. We hypothesized that invasive Prosopis juliflora benefits more from the mutualistic endemic soil microbes compared to its native congener, P. cineraria and that the microbial communities associated with the invasive P. juliflora limit the growth of native P. cineraria.
Methods
Rhizosphere isolate cultures
Rhizosphere soil samples of P. juliflora and P. cineraria were collected from Jodhpur, Rajasthan, India, as described in Kaushik et al. (2021). Soil sample (100 mg) was dissolved in 1 ml of double distilled water, serially diluted, and plated on mineral media containing pyruvate, malate, and succinate as the carbon sources (Biebl and Pfennig 1981; Lakshmi et al. 2011). The mineral medium contained: KH2PO4 (0.5 g l−1), MgSO4·7H2O (0.2 g l−1), NaCl (0.4 g l−1), NH4Cl (0.6 g l−1), CaCl2·2H2O (0.05 g l−1), sodium pyruvate (1.0 g l−1), malic acid (1.0 g l−1), succinic acid (1.0 g l−1), yeast extract (0.3 g l−1), ferric citrate (5 ml l−1 from a 0.1% w/v, stock) and trace element solution SL 7 (1 ml l−1). SL 7 contained: HCl (25% v/v; 1 ml), ZnCl2 (70 mg l−1), MnCl2·4H2O (100 mg l−1), H3BO3 (60 mg l−1), CoCl2·6H2O (200 mg l−1), CuCl2·H2O (20 mg l−1), NiCl2·6H2O (20 mg l−1), NaMoO4·2H2O (40 mg l−1) (Biebl and Pfennig 1981; Lakshmi et al. 2011). Plates were incubated at 30 °C for 3 days after which several bacterial colonies resembling Actinomycetota were sub-cultured and purified as single colonies. The purified colonies were then picked and put in 10 μl of double-distilled autoclaved water in a polymerase chain reaction (PCR) tube and centrifuged at 8000 rpm for 2 min. The dissolved colonies were amplified using colony polymerase chain reaction (PCR) and were sent for 16S sequencing for the identification of bacterial isolates. The sequences thus obtained were identified using EzBioCloud BLAST (Kim et al. 2012) to determine the closest bacterial species. Among the identified rhizobacterial isolates (Table 1), members belonging to the genus Streptomyces were the most common. Due to their preponderance in the rhizosphere of Prosopis congeners, Streptomyces species were chosen for investigating and understanding the effects of specific isolates on the plant growth performance of the alien invasive and native species of Prosopis. More specifically, members belonging to the genus Streptomyces are known to be efficient colonizers of the rhizosphere which generally act as plant growth promoters due to pathogen suppression and phytohormone production (Olanrewaju and Babalola 2019), but may rarely act as plant growth inhibitors due to antibiotic production against other plant growth promoting microbes (Murao and Hayashi 1983). Notably, the response of Streptomyces isolates associated with phylogenetically related native, diploid, and invasive, polyploid plants on their respective growth performances was hitherto unknown. For these garden experiments, we randomly selected one bacterial isolate each from the rhizospheres of invasive P. juliflora and native P. cineraria and are referred to as PJ1 and PC1, respectively. These isolates from P. juliflora and P. cineraria were identified as Streptomyces pratensis and S. coelescens, respectively (Table 1).
Rhizobacterial isolates PJ1 and PC1 were cultured using modified Biebl and Pfennig medium broth and allowed to grow for a week at 28–30 °C. The antibiotics streptomycin (0.4 g l−1), ampicillin (0.2 g l−1) and cycloheximide (0.025 g l−1) were added to the media to avoid contamination. The cultures were maintained until the optical density of the medium broth was 0.5 @O.D.600 (107–108 CFU/ml). After the optimum growth was achieved, the culture suspension was centrifuged at 6000 rpm for 10 min, washed and recentrifuged in double-distilled autoclaved water to get rid of the media salts. The cultures were washed twice using double-distilled water before being dissolved in 15–20 ml of double-distilled autoclaved water, to prepare the inoculum for garden experiments.
Experimental design
The garden experiments were conducted at the School of Life Sciences, University of Hyderabad, India, between January 2020 and April 2020. Seeds of Prosopis juliflora and P. cineraria were collected from the natural populations in Jodhpur, Rajasthan, India. Natural garden soil collected from the University of Hyderabad greenhouse facility was sterilized three times by autoclaving at 121 °C at 15 psi for 1 h for 3 consecutive days. The experiments were conducted in the greenhouse facility at the University of Hyderabad, India, with ambient temperature of 26 ± 2 °C under natural conditions. Before sowing, seeds of P. juliflora and P. cineraria were surface sterilized using 4% sodium hypochlorite (NaOCl) inside a laminar hood. The seeds were then rinsed with double-distilled autoclaved water and kept on moist filter paper inside the laminar hood until their radicles emerged. Four or more germinated seedlings of each species were transferred to a pre-sterilized pot. Four treatments (experiments) were carried out comprising seedlings of native and invasive Prosopis individuals. The following experimental combinations were investigated (Fig. 1): (i) seedlings of P. juliflora and P. cineraria grown in the natural garden soil; (ii) seedlings of P. juliflora and P. cineraria grown in the sterile garden soil; (iii) seedlings of P. juliflora grown in sterile soil and inoculated with its own rhizobacterial isolate (PJ1); (iv) seedlings of P. juliflora grown in sterile soil and inoculated with rhizobacterial isolate from P. cineraria (PC1), and (v) seedlings of P. cineraria grown in sterile soil inoculated with its own isolate (PC1); (vi) seedlings of P. cineraria grown in sterile soil inoculated with rhizobacterial isolate of P. juliflora (PJ1). Five or more replicate pots per treatment with four or more seedlings in each were raised and assayed for different plant growth parameters. However, in one or few replicates in some cases (e.g., P. cineraria seedlings grown in sterile soil inoculated with PJ1 isolate) though four or more seedlings were transferred but only one was established. Finally, a total of 15 seedlings per treatment were assessed for plant growth performance.
The seedlings from each treatment were grown for a 12-week duration and harvested for measurements related to plant growth performance. Plant growth parameters like root length, shoot length, root biomass (dry weight), shoot biomass (dry weight) and number of thorns were measured for each treatment. For dry weight estimation, the harvested seedlings were dried in an oven maintained at 65 °C for 24 h. All downstream statistical analysis was carried out using GraphPad Prism, wherein normal distribution and the homogeneity of variance were tested using the Shapiro–Wilk and D’Agostino and Pearson normality test. For statistical evaluation of differences between treatments, a one-way analysis of variance (ANOVA) followed by Tukey’s post hoc test (α = 0.05) was applied to understand the impact of sterilization and microbial inoculation on plant growth performance.
Results
Root length and root biomass of Prosopis juliflora
The seedlings of P. juliflora recorded a mean root length of 14.93 ± 0.45 cm when grown in the garden soil, but exhibited a significant reduction (11.33 ± 0.46 cm) when grown in the sterile soil (Figs. 2, 3a). The P. juliflora seedlings grown in the soil inoculated with the Streptomyces isolate from its own rhizosphere (PJ1) exhibited significantly enhanced mean root length (13.80 ± 0.48 cm) compared to the seedlings grown in the sterile soil (11.33 ± 0.46 cm; Figs. 2, 3a). However, there was no significant change in their mean root length when seedlings were grown in the soil inoculated with the Streptomyces rhizosphere isolate from the native P. cineraria (PC1) (11.91 ± 0.45; Figs. 2, 3a).
The mean root biomass of P. juliflora seedlings was the highest when grown in natural garden soil (141.3 ± 1.2 mg; Figs. 2, 3b). The seedlings exhibited significant reduction in mean root biomass when grown in the sterile soil (126.2 ± 1.5 mg). The seedlings of P. juliflora when grown in the soil inoculated with its own rhizosphere isolate (PJ1) showed enhanced mean root biomass (131.8 ± 1.1 mg) compared to the seedlings grown in the sterile soil (126.2 ± 1.5 mg; Figs. 2, 3b). However, no significant difference was observed in the mean root biomass of P. juliflora seedlings grown in the sterile soil (126.2 ± 1.5 mg) and those grown in the soil inoculated with rhizosphere isolate of the native P. cineraria, PC1 (126.7 ± 1.3 mg; Figs. 2, 3b).
Shoot length, shoot biomass and number of thorns of Prosopis juliflora
The mean shoot length of P. juliflora seedlings grown in the natural garden soil was significantly higher (8.71 ± 0.42 cm) compared to the seedlings grown in sterile soil (5.80 ± 0.27 cm; Figs. 2, 3c). However, P. juliflora seedlings grown in the soil inoculated with rhizobacterial isolate from P. juliflora (PJ1) recorded a higher shoot length (7.23 ± 0.26 cm) while the seedlings grown in the soil inoculated with the rhizobacterial isolate from native P. cineraria (PC1) recorded a reduced shoot length (6.82 ± 0.26 cm; Figs. 2, 3c). There was a significant increase in the shoot length of the P. juliflora seedlings when grown in soil inoculated with its own rhizobacterial isolate, PJ1 (7.23 ± 0.26 cm; Figs. 2, 3c) compared to the seedlings grown in sterile soil (5.80 ± 0.27 cm; Figs. 2, 3c).
The seedlings of P. juliflora grown in the natural garden soil yielded significantly higher mean shoot biomass (148.2 ± 1.1 mg) compared to the seedlings grown in the sterile soil (134.7 ± 1.6 mg; Figs. 2, 3d). P. juliflora seedlings yielded significantly higher mean shoot biomass when grown in the soil inoculated with its own rhizosphere bacterial isolate, PJ1 (140.9 ± 0.9 mg; Fig. 3d) compared to the mean shoot biomass of P. juliflora seedlings grown in the sterile soil (134.7 ± 1.6 mg; Figs. 2, 3d). However, there was no significant change in the mean shoot biomass of P. juliflora seedlings when grown in the soil inoculated with the rhizosphere bacterial isolates from native P. cineraria, PC1 (133.6 ± 1.3 mg; Figs. 2, 3d) compared to the seedlings grown in the sterile soil (134.7 ± 1.6 mg; Figs. 2, 3d).
Mean number of thorns was the highest in the seedlings of invasive P. juliflora grown in natural garden soil (15 ± 0.9) compared to significantly reduced mean number of thorns in P. juliflora seedlings grown in the sterile soil (11 ± 0.5; Figs. 2, 4). However, there was no significant difference in the mean number of thorns in the invasive P. juliflora seedlings when grown either in the sterilized soil (11 ± 0.5) or when grown in the soil inoculated with its own rhizosphere bacterial isolate PJ1 (11 ± 0.8) or when grown in the soil inoculated with rhizosphere bacterial isolates of P. cineraria PC1 (11 ± 0.7; Figs. 2, 4).
Root length and root biomass of native Prosopis cineraria
Seedlings of the native P. cineraria when grown in natural garden soil exhibited significantly lower mean root length (11.93 ± 0.35 cm) compared to the seedlings grown in the sterile soil (14.83 ± 0.62 cm; Figs. 2, 5a), but a marginal increase in root length was observed in the seedlings when grown in the soil inoculated with its own Streptomyces rhizosphere isolate, PC1 (14.95 ± 0.87 cm; Figs. 2, 5a). However, the root length of native P. cineraria seedlings grown in the sterile soil inoculated with the rhizobacterial isolate of invasive P. juliflora, PJ1 was significantly lower (9.68 ± 0.30 cm) compared to the seedlings grown in the natural garden soil (11.93 ± 0.35 cm), sterile soil (14.83 ± 0.62 cm) or the sterile soil inoculated with Streptomyces isolate, PC1 from native P. cineraria (14.95 ± 0.87 cm) (Figs. 2, 5a).
The mean root biomass of Prosopis cineraria seedlings grown in the garden soil (136.4 ± 1.0 mg, Fig. 5b) was significantly lower than those of its seedlings grown in sterile soil (141.5 ± 1.5 mg; Figs. 2, 5b) and a marginal increase was observed in the root biomass of P. cineraria seedlings grown in the soil inoculated with PC1 isolate (137.4 ± 1.2 mg; Figs. 2, 5b) compared to those grown in garden soil. The mean root biomass of native P. cineraria seedlings grown in sterile soil inoculated with rhizobacterial isolates of invasive P. juliflora was significantly lower (124.4 ± 1.2 mg; Figs. 2, 5b) compared to its seedlings grown in natural garden soil (136.4 ± 1.0 mg; Figs. 2, 5b), sterile soil (141.5 ± 1.5 mg; Figs. 2, 5b) or sterile soil inoculated with its own rhizobacterial isolate PC1 (137.4 ± 1.2 mg; Figs. 2, 5b).
Shoot length, shoot biomass and number of thorns of native Prosopis cineraria
The seedlings of native P. cineraria recorded a mean shoot length of 7.11 ± 0.22 cm when grown in the garden soil and there was a significant increase in their shoot length when these seedlings were grown in the sterilized soil (8.90 ± 0.47 cm; Figs. 2, 5c). However, a marginal increase was observed in the shoot length of seedlings grown in sterile soil inoculated with its own rhizobacterial isolate PC1 (8.10 ± 0.33; Figs. 2, 5c) compared to that of the seedlings grown in sterile soil (8.90 ± 0.47 cm). The mean shoot length of P. cineraria seedlings grown in sterile soil inoculated with rhizobacterial isolates of P. juliflora PJ1 was significantly lower (5.56 ± 0.40 cm) compared to the shoot length of the seedlings grown in garden soil (7.11 ± 0.22 cm), sterilized soil (8.90 ± 0.47 cm) or sterile soil inoculated with its own rhizobacterial isolate PC1 (8.10 ± 0.33 cm) (Figs. 2, 5c).
The mean shoot biomass of the P. cineraria seedlings grown in natural garden soil was significantly lower (145.8 ± 1.7 mg) than the seedlings grown in sterile soil (152.2 ± 1.2 mg; Figs. 2, 5d). However, there was no significant difference in the mean shoot biomass of the native P. cineraria seedlings grown in the sterile soil (152.2 ± 1.2 mg) and those grown in the soil inoculated with its own rhizobacterial isolate PC1 (146.8 ± 1.7 mg; Figs. 2, 5d). The mean shoot biomass of P. cineraria seedlings grown in the sterile soil inoculated with rhizosphere isolate of P. juliflora, PJ1 was significantly lower (130.6 ± 1.3 mg) compared to the seedlings grown in the garden soil (145.8 ± 1.7 mg), sterile soil (152.2 ± 1.2 mg) or sterile soil inoculated with PC1 isolate from native P. cineraria (146.8 ± 1.7 mg) (Figs. 2, 5d).
There was no significant difference in the mean number of thorns between the seedlings of P. cineraria grown either in sterilized soil (16 ± 0.7; Figs. 2, 4) or the soil inoculated with its own rhizosphere bacterial isolate PC1 (17 ± 0.9; Figs. 2, 4). However, the least number of thorns was observed in the P. cineraria seedlings grown in the soil inoculated with rhizosphere bacterial isolate of P. juliflora PJ1 (9 ± 0.8; Figs. 2, 4).
Discussion
Invasive plants are known to alter soil communities to gain competitive advantage over native species (Si et al. 2013). In this study, we tested the hypothesis that invasive Prosopis juliflora, a globally widespread tropical invasive, may benefit more from the associated mutualistic soil microbial community in its invaded range compared to its native congener, P. cineraria. In an earlier study, we had shown that P. juliflora recruits a unique set of rhizosphere bacterial communities that proffer it an adaptive advantage mediated by various metabolic pathways (Kaushik et al. 2021). In this study, we further demonstrate the competitive advantage of exotic P. juliflora over native P. cineraria by providing empirical evidence of the differential impacts of soil bacterial isolates on growth performance of exotic and native Prosopis congeners. Our results show that exclusion of soil microbes by soil sterilization produces contrasting effects on the two congeners, evaluated in terms of growth parameters such as root length and biomass, shoot length and biomass, and number of thorns (Figs. 2, 3, 4, 5).
Soil microbial exclusion reduced growth performance of invasive P. juliflora as indicated by reduced above and below-ground growth parameters (Figs. 2 and 3), suggesting positive feedback from the endemic soil communities on the growth performance of the exotic species. In contrast, exclusion of the soil biota resulted in enhanced growth performance (Figs. 2 and 5) of the native congener, indicating negative feedback from the native soil biota on growth parameters of the native P. cineraria. These results are consistent with earlier studies involving invasive cogongrass Imperata cylindrica and native Pinus palustris and Aristida stricta, in which the invader species were reported to show higher biomass in live soil than sterile soil, while the native species exhibited significantly enhanced biomass upon soil sterilization (Fahey and Florey 2022). Our results, therefore, provide further conclusive evidence of positive soil feedback in case of the exotic invasive species and negative feedback in case of the native plant species.
Our study also points out that the number of thorns in alien P. juliflora seedlings reduced significantly (Fig. 4) when grown in sterilized soil, indicating the role and importance of soil microbes in development of thorns, which comprise above-ground defense mechanism such as against herbivory in the invasive P. juliflora. However, there was no effect of soil sterilization on the number of thorns in case of native P. cineraria. Our results signify the importance of complete soil microbiome in mediating plant defense especially in case of the alien invasive plants such as P. juliflora further corroborating the role of soil microbes as mediators of plant defensive phenotype and above-ground interactions with herbivores (Schädler and Ballhorn 2016).
These studies also clearly demonstrate that the presence of native soil biota facilitated the growth performance of alien invasive P. juliflora in its non-native range, but negatively impacted the growth of native P. cineraria. These results point out that the native species tend to be restricted by the endemic soil microbes which have co-evolved alongside the host flora during evolutionary time (Lankau 2012). Conversely, the absence of restrictive microbial community in alien P. juliflora and facilitation of its growth performance provides further evidence to the enemy release hypothesis, which posits that the reduced loads of the natural enemies like pathogens, predators, or parasites in the non-native ranges aid plant invasion (Keane and Crawley 2002). Notably, the absence of inhibitory soil microbes in the non-native range results in an overall positive soil feedback for exotic alien plant species, while the presence of natural pathogens specific to the native plants co-evolved during evolutionary history results in a negative soil feedbacks for the native plants. These results further substantiate our earlier observations on the rhizosphere microbiome of the two congeners in which we showed that the alien invasive P. juliflora exhibited selective enrichment of growth-promoting phyla like Actinomycetota, Chloroflexi, Firmicutes and Acidobacteria and a lower abundance of phytopathogenic genera like Serratia compared to its native congener, P. cineraria (Kaushik et al. 2021).
The soil inoculation experiments involving seedlings of P. juliflora and P. cineraria and their respective Streptomyces isolates, PJ1 and PC1, respectively, also yielded contrasting results. The root length of P. juliflora seedlings grown in sterile soil was significantly lower compared to those grown in soils inoculated with PJ1 isolate, while there was no change in root length when seedlings were grown in the soil inoculated with PC1 isolate (Fig. 3). This result suggests that in absence of any soil microbes, invasive P. juliflora showed decreased growth performance than in the presence of its rhizobacterial isolate PJ1. However, in case of native Prosopis cineraria, only a marginal increase in root length was observed upon inoculation with its own PC1 isolate compared to the seedlings grown in sterile soil (Fig. 5). However, there was a significant decline in root length of the P. cineraria seedlings when grown in soils inoculated with PJ1 isolate (Fig. 5). This result indicates restrictive influence of PJ1 microbial isolate from P. juliflora on the growth performance of P. cineraria. In other words, the rhizobacteria recruited by P. juliflora are not only different from those of native P. cineraria but that the microbial community of P. juliflora negatively affects growth of native P. cineraria, thereby hampering its spread and growth performance.
Our results also show that there was a significant increase in root biomass of P. juliflora when its seedlings were grown in soil inoculated with its bacterial isolate PJ1, while no change was observed when its seedlings were grown in soil inoculated with PC1 bacterial isolate (Fig. 3). In contrast, only an insignificant increase in root biomass of native P. cineraria was observed when its seedlings were grown in soils inoculated with its own bacterial isolate PC1 (Fig. 5) compared to the seedlings grown in natural garden soil, while a significant decline in root biomass was observed when the native P. cineraria seedlings were grown in soils inoculated with PJ1 isolate of P. juliflora (Fig. 5). These results clearly point out to uniqueness and differential soil microbiome recruitment strategy of exotic invasive P. juliflora which offers it an adaptive advantage over P. cineraria. As such, our results are consistent with results of many earlier studies pointing to the role of invasive species in changing native soil microbial community in their non-native ranges to gain invasion success (Batten et al. 2006; Kourtev et al. 2002; Kaushik et al. 2021).
Our results on the comparative growth performance measured in terms of shoot length showed that P. juliflora seedlings exhibited a significant increase when grown in soils inoculated with its own rhizobacterial isolate PJ1 compared to when grown in sterile soil (Figs. 2 and 3). However, the seedlings of exotic P. juliflora exhibited no significant change in growth performance when grown in soils inoculated with rhizobacterial isolate of P. cineraria (PC1). The native P. cineraria seedlings exhibited a significant decline in their mean shoot length when the seedlings were grown in soils inoculated with PJ1 isolate, but only a marginal increase was observed when grown in soils with PC1 isolate (Fig. 5). Similarly, we found an increase in shoot biomass of P. juliflora seedlings when grown in soil inoculated with its own rhizobacterial isolate (PJ1) while no change was observed when its seedlings were grown in the soils inoculated with P. cineraria (PC1) isolate (Figs. 2 and 3). Likewise, for shoot biomass of the native P. cineraria seedlings, an insignificant increase was observed when its seedlings were grown in soils inoculated with PC1 isolate compared to the seedlings grown in natural garden soil, but a significant decline was observed in the seedlings when grown in soils inoculated with PJ1 isolate (Figs. 2 and 5). These results signify that exotic invasive P. juliflora experienced: (i) reduced growth performance in absence of soil microbes; (ii) better growth performance in presence of its unique soil bacterial community which it recruits differentially and does not share with its native congener, P. cineraria; and (iii) lack of increase in growth performance in the presence of non-specific soil microbes unique to its native congener P. cineraria. Similarly, the native P. cineraria experienced: (i) enhanced growth performance in absence of native soil microbes; (ii) enhanced growth performance in presence of its unique soil bacterial community which it does not share with invasive congener, P. juliflora; and (iii) reduced growth performance in the presence of non-specific soil microbes unique to its invasive congener P. juliflora. Such results corroborate our earlier findings of differential recruitment of soil microbial communities by native and invasive Prosopis congeners (Kaushik et al. 2021) and further our understanding of the divergent legacy effects of microbial species even from the same genus on the respective growth performance of alien invasive and native congeners, which was hitherto unknown.
Conclusion
Our research shows that native P. cineraria receives negative feedback from its soil microbial population, but invasive P. juliflora receives positive input from the non-native range soil microbial community. Our findings advance our knowledge of the divergent growth-promoting effects of differently recruited microbial species belonging to the same genus (Streptomyces) in the rhizospheres of foreign invasive and native plants, and they offer new experimental support for the enemy release theory. Based on these results, we conclude that soil microbes may indirectly affect competition among native and invasive plants through differential impacts on plant growth performance parameters which influence direct competitive interactions. These findings raise new questions about the possible genomic attributes of bacterial genera like Streptomyces associated with the invasive plants which could potentially have negative impacts on the growth of native plants. Further experiments are required to decipher the factors which determine the growth-promoting or inhibiting nature of microbial community associated with native and invasive plants.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Abbott KC, Karst J, Biederman LA, Borrett SR, Hastings A, Walsh V, Bever JD (2015) Spatial heterogeneity in soil microbes alters outcomes of plant competition. PLoS ONE 10(5):e0125788
Allen WJ, Meyerson LA, Cummings D, Anderson J, Bhattarai GP, Cronin JT (2017) Biogeography of a plant invasion: drivers of latitudinal variation in enemy release. Glob Ecol Biogeogr 26(4):435–446
Bai F, Chisholm R, Sang W, Dong M (2013) Spatial risk assessment of alien invasive plants in China. Environ Sci Technol 47(14):7624–7632
Baker HG (1965) Characteristics and modes of origin of weeds. In: Genetics of colonizing species. pp 147–172
Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8(2):217–230
Biebl H, Pfennig N (1981) Isolation of members of the family Rhodospirillaceae. In: The prokaryotes. Springer, Berlin. pp 267–273
Bozzolo FH, Lipson DA (2013) Differential responses of native and exotic coastal sage scrub plant species to N additions and the soil microbial community. Plant Soil 371(1):37–51
Burkart A (1976) A monograph of the genus Prosopis (Leguminosae subfam. Mimosoideae). J Arnold Arboretum 57:450–525
Callaway RM, Rout ME (2010). Soil biota and plant invasions: biogeographical effects on plant–microbe interactions. Fifty years of invasion ecology: The legacy of Charles Elton, pp 131–142
Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15(1):22–40
Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Resour 30:75–115
Eppinga MB, Rietkerk M, Dekker SC, De Ruiter PC, Van der Putten WH, Van der Putten WH (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114(1):168–176
Fahey C, Flory SL (2022) Soil microbes alter competition between native and invasive plants. J Ecol 110(2):404–414
Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101(3):607–613
Kaushik R, Pandit MK, Meyerson LA, Chaudhari DS, Sharma M, Dhotre D, Shouche YS (2021) Contrasting composition, diversity and predictive metabolic potential of the rhizobacterial microbiomes associated with native and invasive Prosopis congeners. Curr Microbiol 78(5):2051–2060
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17(4):164–170
Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park S-C, Jeon YS, Lee J-K, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417(6884):67–70
Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83(11):3152–3166
Lakshmi KVNS, Sasikala C, Takaichi S, Ramana CV (2011) Phaeospirillum oryzae sp. nov., a spheroplast-forming, phototrophic alphaproteobacterium from a paddy soil. Int J Syst Evol Microbiol 61(7):1656–1661
Lankau RA (2012) Coevolution between invasive and native plants driven by chemical competition and soil biota. Proc Natl Acad Sci 109(28):11240–11245
Leitch AR, Leitch IJ (2008) Genomic plasticity and the diversity of polyploid plants. Science 320(5875):481–483
Mangla S, Inderjit, Callaway RM (2008) Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J Ecol 96(1):58–67
Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80(4):1180–1186
Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421(6923):625–627
Mordecai EA (2011) Pathogen impacts on plant communities: unifying theory, concepts, and empirical work. Ecol Monogr 81(3):429–441
Murao S, Hayashi H (1983) Gougerotin, as a plant growth inhibitor, from Streptomyces sp. No. 179. Agric Biol Chem 47(5):1135–1136
Olanrewaju OS, Babalola OO (2019) Streptomyces: implications and interactions in plant growth promotion. Appl Microbiol Biotechnol 103(3):1179–1188
Pandit MK, Pocock MJ, Kunin WE (2011) Ploidy influences rarity and invasiveness in plants. J Ecol 99(5):1108–1115
Pasiecznik NM, Felker P, Harris PJ, Harsh L, Cruz G, Tewari JC, Cadoret K, Maldonado LJ (2001) The Prosopis juliflora–Prosopis pallida complex: a monograph (Vol. 172). Coventry: HDRA.
Pyšek P, Richardson DM (2008) Traits associated with invasiveness in alien plants: where do we stand? In: Biological invasions. Springer, Berlin. pp 97–125
Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77(6):1655–1661
Richardson DM, Pyšek P, Rejmanek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6(2):93–107
Schädler M, Ballhorn DJ (2016) Beneficial soil microbiota as mediators of the plant defensive phenotype and aboveground plant-herbivore interactions. In: Progress in Botany, Vol. 78. Springer, Cham. pp 305–343
Si C, Liu X, Wang C, Wang L, Dai Z, Qi S, Du D (2013) Different degrees of plant invasion significantly affect the richness of the soil fungal community. PLoS ONE 8(12):e85490
Te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubešová M, Pyšek P (2012) The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot 109(1):19–45
Thébault A, Frey B, Mitchell EA, Buttler A (2010) Species-specific effects of polyploidisation and plant traits of Centaurea maculosa and Senecio inaequidens on rhizosphere microorganisms. Oecologia 163(4):1011–1020
Traveset A, Richardson DM (2020) Plant invasions: the role of biotic interactions—an overview. Plant invasions: the role of biotic interactions. CAB International, Wallingford, pp 1–25
Trenchard LJ, Harris PJ, Smith SJ, Pasiecznik NM (2008) A review of ploidy in the genus Prosopis (Leguminosae). Bot J Linn Soc 156(3):425–438
Van der Putten WH, Kowalchuk GA, Brinkman EP, Doodeman GTA, Van der Kaaij RM, Kamp AFD, Menting FBJ, Veenendaal EM (2007) Soil feedback of exotic savanna grass relates to pathogen absence and mycorrhizal selectivity. Ecology 88(4):978–988
Van Kleunen M, Dawson W, Essl F, Pergl J, Winter M, Weber E, Kreft H, Weigelt P, Kartesz J, Nishino M, Antonova LA, Barcelona JF, Cabezas FJ, Cárdenas D, Cárdenas-Toro J, Castaño N, Chacón E, Chatelain C, Ebel AL, Figueiredo E, Fuentes N, Groom QJ, Henderson L, Inderjit, Kupriyanov A, Masciadri S, Meerman J, Morozova O, Moser D, Nickrent DL, Patzelt A, Pelser PB, Baptiste MP, Poopath M, Schulze M, Seebens H, Thomas J, Shu W, Velayos M, Wieringa JJ, Pyšek P (2015) Global exchange and accumulation of non-native plants. Nature 525(7567):100–103
Acknowledgements
MS thanks CSIR and RK thanks the DBT, New Delhi, for the award for research fellowships. MKP thanks Institution of Eminence, University of Delhi, for Faculty Research Grant. We thank the staff and the laboratory facilities provided by Centre for Interdisciplinary Studies of Mountain & Hill Environment, University of Delhi.
Funding
This work was supported by Faculty Research Grant of the Institution of Eminence, University of Delhi provided to MKP. This work received grant specifically from Department of Biotechnology (DBT/2015/UOD/358), Government of India, provided to RK. Financial support received from Council for Scientific and Industrial Research (CSIR) (09/045(1601)/2018/EMR-I) provided to MS is acknowledged. Infrastructure facilities funded by DST-FIST, UGC-SAP (DRS) and TEQIP and AICTE-MODROBS are acknowledged. The financial assistance of IoE FRP Grant to MKP is gratefully acknowledged.
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Kaushik, R., Sharma, M., Ramana, C.V. et al. Contrasting plant growth performance of invasive polyploid and native diploid Prosopis is mediated by the soil bacterial community. Ecol Process 12, 12 (2023). https://doi.org/10.1186/s13717-023-00425-0
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DOI: https://doi.org/10.1186/s13717-023-00425-0