Purpose: Salt stress reduces plant growth and is now becoming one of the most important factors restricting the agricultural productivity. Inoculation of plant growth-promoting rhizobacteria (PGPR) has been shown to confer plant tolerance against abiotic stress, but the detailed mechanisms of how this occurs remain unclear and the application effects in different reports are unstable. In order to obtain a favorite effect of PGPR inoculation and improve our knowledge about the related mechanism, we performed this study to analyze the mechanism of a PGPR consortium on improving the salt resistance of crops. Methods: A region-specific (Saline land around Bohai Sea in China) PGPR consortium was selected that contains three strains (Pseudomonas sp. P8, Peribacillus sp. P10, and Streptomyces sp. X52) isolated from rhizosphere of Sonchus brachyotus DC. grown in a saline soil. By inoculation tests, their plant growth-promoting (PGP) traits and ability to improve the salt resistance of maize were investigated and shifting in rhizosphere bacterial community of the inoculated plants was analyzed using the high-throughput sequencing technology. Results: The three selected strains were salt tolerant, presented several growth promoting properties, and inhibited several phytopathogenic fungi. The inoculation of this consortium promoted the growth of maize plant and enriched the beneficial bacteria in rhizosphere of maize in a saline soil, including the nitrogen fixing bacteria Azotobacter, Sinorhizobium, and Devosia, and the nitrification bacteria Candidatus Nitrososphaera, and Nitrosovibrio. Conclusions: The bacterial consortium P8/P10/X52 could improve plant growth in a saline soil by both their PGP traits and regulating the rhizosphere bacterial community. The findings provided novel information about how the PGPR helped the plants in the view of microbiome. Keywords: Consortium inoculant, Saline soil, Rhizobacteria, Plant promoting trait, Maize * Correspondence: email@example.com; firstname.lastname@example.org Institute of Agro-resources and Environment (Hebei Fertilizer Technology Innovation Center), Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang, Hebei, People’s Republic of China Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Peng et al. Annals of Microbiology (2021) 71:40 Page 2 of 12 Introduction system, physical adsorption improvement, brine dis- Soil salinity is a common problem and one of the main charge pipe, slag adsorption etc., but all of them are abiotic stress factors that inhibit plant growth and devel- fresh water consuming procedures that is not suitable opment (Egamberdieva et al. 2019). Salinization refers to for arid and semi-arid areas (Ilangumaran and Smith the concentration increase or accumulation of water- 2017). On the other hand, in order to improve the salt soluble salts in soil. Salt-affected soils are classified by tolerance of plants, mechanisms (including genes) of the −1 electrical conductivity (EC > 4 dS m , ~ 0.3%), the salt resistance in plants have been studied (Li et al. 2014; exchangeable sodium percent (ESP > 6%), or pH usually Ondrasek and Rengel 2021), including the use of plant over 8.5. The salts mainly caused by the flooding and growth-promoting rhizobacteria (PGPR), traditional seepage of seawater, rising of brackish groundwater in breeding and genetic engineering (Fita et al. 2015; Yang areas with low rainfall and high evaporation, or saline ir- et al. 2009). Traditional breeding and genetic engineer- rigation water and poor water management in agricul- ing usually need a long period for obtaining progress or tural areas (Ondrasek and Rengel 2021). As the most success, and PGPR can greatly improve the salt tolerance important type of soil degradation, soil salinization ser- (Chen et al. 2016), drought resistance and growth of iously affects crop production mainly by decreasing the crops with low cost and short time. PGPR have been osmotic potential of the soil that makes the plants diffi- used in promoting plant growth and disease prevention cult to absorb water, but also by the direct toxic of salts. that in turn could improve the productivity in saline With the human activity in arable land, such as excessive land (Palaniyandi et al. 2014). Therefore, the application and long term supply of chemical fertilizers, the degree of PGPR is one of the most promising alternatives for of secondary salinization of soil becomes more and more improving plant growth in saline soil (Numan et al. serious. Therefore, soil salinization forms a limitation to 2018; Yang et al. 2009). At present, the use of PGPR to fit the increased food demand companied with the improve salt stress in crop production is becoming more development of human society and the increase of and more common. Various salt-tolerant PGPR, population. including Azospirillum, Burkholderia, Rhizobium, In general, around 953 × 10 ha or 20% of the irrigated Pseudomonas, Acetobacter and Bacillus associated with areas of the world have been affected by salinization, different plants have been successfully applied or tested and the salinity problem is more common in semi-arid for improving plant growth under salt stress (Chatterjee regions, as reported in Brazil, India, and China, due to et al. 2017; Egamberdieva et al. 2015). Maize is one of the low rainfall against high evaporative rate (Fagundes the most important cereal crops that is mainly planted et al. 2020; Singh 2021). In China, there are about 36 × in irrigated agricultural areas in both arid and semi-arid 10 ha of land with saline soil, accounting for about 5% regions (Nuss and Tanumihardjo 2010). As a moderately of the total available land base of the country. Although salinity-sensitive plant species, few salinity-tolerant these regions presented low agricultural productivity, the maize cultivars have been commercialized, but PGPR saline soils forms an important potential resource for can improve maize salt tolerance (Chen et al. 2016). arable land. However, these bacteria have not been fully investigated, Attempts to improve the crop production in the saline especially in arid and semiarid regions, and their effects lands have been made in China since 1930s (Li et al. in application were not suitable and unstable in some 2014). The related studies have been focused on two as- cases, in addition to their limited application range (Wu pects: land management or technologies to promote the et al. 2012). Furthermore, few of the microbial strains soil desalination; and breeding crop cultivars resistant or presented wide and strong adaptability in the soil. adapted to the saline soils. Some of the methods are also Considering that the biogeographic patterns of the soil applied in other countries. Rice production in the Me- bacteria (Chu et al. 2020; Li et al. 2020) and plant associ- kong River Delta of Vietnam (MRD) is endangered by ated bacteria (Román-Ponce et al. 2016; Zhang et al. sea-level rise and an associated increase in the incidence 2011) are determined by the soil physiological and bio- of salinity intrusion. Diffusion of salt tolerant rice var- logical traits, we propose that region-specific PGPR ieties in the MRD has been performing to solve this might have a stable effect on improve the salt resistance problem (Paik et al. 2020). Some well-proven, widely of the local crops. In order to verify this hypothesis, we used and cost-effective traditional ameliorative strategies performed the present study by using a set of efficient (e.g., conservation agriculture, application of natural bacteria screening methods for searching salt-tolerance conditioners) helped the crops against salinity and other PGPR against Sonchus brachyotus DC. (common name constraints, especially in developing countries (Ondrasek Qumacai or Kujucai in China) from rhizosphere of and Rengel 2021). plants grown in a saline land in Haixing County, Hebei Some desalinization technologies have been developed Province of China. A consortium composed of three in previous studies, such as the drainage-based cropping strains was selected based upon their salt resistance and Peng et al. Annals of Microbiology (2021) 71:40 Page 3 of 12 PGP traits, and its effects on maize growth and consortium as PGPR inoculant. In addition, these iso- rhizosphere microbiota were investigated. The results lates with different colony morphologies without nutri- provided theoretical support for application of the PGPR tional competition were also considered as the selection consortium in improving the productivity in saline land criteria. and in sustainable agriculture. All the selected isolates were tested for their in vitro inhibition against the phytopathogenic fungi Pythium aphanidermatum MJ-1, Fusarium oxysporium f.sp. cucu- Materials and methods merinum HG-11, Curvularia lunata sp. WM-1, Cochlio- Bacterial isolation bolus heterostrophus sp. WM-2, and Phytophthora Rhizobacteria were isolated from Sonchus brachyotus capsici LJ-3 on King’B medium by plate confronta- rhizosphere soil collected in saline field in Haixing County, Cangzhou City, Hebei Province of China. A tion method and plate diffusion method according to rhizosphere soil suspension was obtained by shaking off the references (Fernandez-Garayzabal et al. 1992). Diam- and discarded the loosely soil then rinsing the roots with eter in mm of the fungal colonies in both the control adhered soil in phosphate-buffered for 10 min at 150 (without bacterial inoculant) and the test (co-incubated -6 rpm. The suspension was serially diluted to 10 , and ali- with bacteria) was measured after 7 days incubation at quots of 0.1 mL of the last three dilutions were spread 28 °C. The inhibition (%) was presented as 100× (radius of control colony –radius of colony in test)/radius of separately onto King’B medium (KMB, 6.5 g Pep- control colony. All the tests were performed in triplicate. tone, 0.5 g K HPO , 0.5 g MgSO 7H O, 3 mL Glycerol, 2 4 4• 2 18 g agar, add dH O to 1 L) and incubated at 30 °C for Bacterial identification 48 h. Single colonies with different morphology traits For identification of the selected isolates, bacterial (shape, color, size, luster, texture, light transparence, genomic DNA was extracted by the CTAB/NaCl method edge integrity) were picked up and re-streaked several times on the same medium to obtain the pure culture. (Andreou 2013) from 5 mL of culture in broth of The purified bacteria were maintained at slants of King’B medium incubated at 30 °C for 24 h with agita- tion, and the almost complete 16S rDNA was amplified KMB medium at 4 °C for short time storage (3–4 weeks) from the DNA extract by using PCR with the universal or in broth of the same medium supplied with 30% (w/ bacterial primers 27F and 1492R (Frank et al. 2008). The v) glycerol at − 80 °C for long-term storage. PCR product was sequenced commercially in Invitrogen (Shanghai) with the same primers and the acquired se- Selection of the PGPR and estimation of their PGP traits quences were analyzed with BLASTn to identify the iso- The salt resistance of the isolates was tested by grown lates at genus/species level. them on King’B medium supplied with 0%, 5%, and 10% (w/v) of NaCl. The growth promoting properties of Plant growth conditions and treatments the isolates were tested according the reported methods. The saline soil used for the pot experiment was obtained Briefly, the production of IAA (indole-3-acetic acid) was from 0 to 30 cm in depth at the Haixing Farm (38.04 N determined by the method of Khalid et al. 2004 and Bric 117.24 E) that located in the same region for the bacter- et al. 1991; the production of ACCD (1-aminocyclopro- ial isolation. The soil was air-dried and sieved to 2.5 mm pane-1-carboxylic acid deaminase) was determined by before filling in the pot. The basic physicochemical the method of Penrose and Glick 2003]; the production properties of the soil were pH 8.39, total salt 3.09%, or- −1 −1 of siderophores was estimated based on the work of ganic matter 4.45 g kg , total N (TN) 0.27 g kg , alkali- −1 Schwyn and Neilands 1987; phosphate solubilization po- hydrolyzable N 22.75 mg kg , total phosphorus (P) 0.69 −1 −1 tential was determined by the method of Vyas et al. gkg , available P (AP) 10.39 mg kg , total potassium −1 −1 2007; and nitrogen fixation capacity was investigated (K) 18.59 g kg and available K (AK) 101.75 mg kg . using the method of Dobereiner et al. 1976. All the tests The non-saline soil obtained from Experimental Farm were performed in triplicate by incubation at 30 °C for (38.05 N 114.44 E) in Shijiazhuang City, Hebei Province, 48–96 h. IAA production and ACCD activities were also was also used for a parallel experiment, which presented quantitatively determined with the methods described the basic physicochemical properties as following: pH −1 previously (Khalid et al. 2004; Penrose and Glick 2003). 7.27, total salt 0.09%, organic matter 18.18 g kg , total −1 −1 Based upon their salt tolerance and PGP traits, isolates N (TN) 1.07 g kg , alkalihydrolyzable N 68.60 mg kg , −1 with strong ACCD activity, high nitrogen fixation ability, total phosphorus (P) 0.90 g kg , available P (AP) 27.19 −1 −1 high phosphate solubilization, and high IAA and mg kg , total potassium (K) 19.46 g kg and available −1 siderophore production were selected to compose a K (AK) 150.00 mg kg . For the subsequent analysis, a Peng et al. Annals of Microbiology (2021) 71:40 Page 4 of 12 mixture of the two soils (1 g of the saline soil + 9 g of USA) according to the manufacturer’s instructions. The the non-saline soil) was prepared to get a soil with quality and quantity of the extracts were measured by 0.31% of total salt, which is the limit concentration for the Nano Drop™2000 spectrophotometer (Nano Drop surviving of maize in a preliminary test. Technologies, Wilmington, DE, USA). Primer set of To define whether the bacteria had an effect on the F515 (5′-GTGCCAGCMGCCGCGG-3′) and R907 (5′- growth of maize in saline condition, surface-sterilized and CCGTCAATTCMTTTRAGTTT-3′) was used to amp- synchronized seeds of cultivar Zhengdan 958 were incu- lify the V4-V5 hypervariable regions of bacterial 16S bated with bacterial suspension (10 CFU/mL) prepared rRNA gene by PCR (Zhou et al. 2011). PCR products by mixing the three selected isolates P8, P10, and X52 in were purified and sequenced on a single lane of Illumina the same ratio (1:1:1 in volume) or sterilized water solu- MiSeq platform at the Shanghai Personal biotechnology tion as a control for 12 h and then pregerminated on sand Co., Ltd (Personalbio, Shanghai, China). under 0.0% and 0.3% NaCl concentrations and on the Sequencing libraries were generated using the Illumina mixed soil containing 0.3% total salt. The germinated Nano DNA LT Library Prep KitTruSeq DNA PCR-Free seeds were sown in pots filled with the natural soil sam- Library Preparation Kit (Illumina, San Diego, USA) by ples (200 g soil in each 1 litter pot, one seed per pot). Pot- following the manufacturer’s recommendations. Library ted plants were placed in a growth chamber at 25 °C with quality was assessed on a Qubit@ 2.0 Fluorometer a 16/8 h light/dark cycle. Deionized water was supplied (Thermo Fisher Scientific, Waltham, USA) and an Agi- from the bottom of the pot. Finally, 25 days after sowing, lent Bioanalyzer 2100 system (Agilent Technologies, plant agronomic traits were determined, including shoot Santa Clara, USA). Finally, the library was sequenced on length, root length, shoot dry weight, and root dry weight. an Illumina MiSeq platform and 300 bp paired-end Each treatment has three replicates (n =3). reads were generated (Personalbio, Shanghai, China). Raw reads were filtered by QIIME (Quantitative Insights Rhizosphere bacterial community analysis by 16S rDNA Into Microbial Ecology) quality filters (Bokulich et al. gene sequencing 2013). The remaining reads from the original DNA frag- To investigate the effect of P8/P10/X52 consortium on ments were merged using the FLASH tool (Magoč and maize rhizosphere microbiota in saline soil, sterilized Salzberg 2011). Paired-end reads were assigned to each and synchronized seeds were inoculated by immerging sample according to unique barcodes with QIIME (Ed- the seeds with the consortium suspension (1:1:1, 10 gar 2010). OTUs (operational taxonomic units) with CFU/mL/strain) or with sterilized water solution as a identities of 97% were determined for the quality fil- control for 12 h and then pregerminated on the mixed trated reads using the Mothur software (http:// www. soil containing 0.31% of total salt. Pregerminated seeds mothur.org), from which the Shannon diversity index were sown in a stone pot with dimensions of 305 mm and Chao1 richness were estimated (White et al. 2009). (height) × 225 mm (open top) × 205 mm (flat bottom) The sequence with the highest relative abundance from which were filled with 7 kg of the mixed soil samples each OTU was selected as the representative sequence −1 supplied with inorganic fertilizers (kg ha ) in the ratio to search the similar sequences in the National Center of 150 N, 75 P O and 75 K O. Each treatment had 48 for Biotechnology Information (NCBI) nucleotide non- 2 5 2 replicate pots. The growth conditions were the same as redundant database. PLS-DA (Partial least squares dis- described above and supplied each pots in equal water- criminant analysis) was also introduced as a supervised ing every 15 days. The rhizosphere soil was sampled at model to reveal the microbiota variation among groups, the three-leaf stage (10 days after sowing), jointing stage using the “plsda” function in R package “mixOmics” (27 days after sowing), tasseling stage (52 days after sow- (Chen et al. 2011). Each group represents by one color ing), and maturity stage (100 days after sowing) in three and has three dots, which represent three repetitions replicates for analyzing the microbiota by the high and are marked with an ellipse. It would be better if the throughput DNA sequencing described subsequently. same color dots are closer, and the different color dots The rhizosphere soil samples were obtained according are farther. to previous research (Hu et al. 2020). In brief, they were Abundances of taxa at the genus levels were statisti- sampled by brushing off the soils attached to the root cally compared among samples or groups by Metastats surface with a soft toothbrush. Samples from the three (http://metastats.cbcb.umd.edu/) (White et al. 2009). plants (repeats) were compiled to form a composite The difference in quantity (relatively abundance) of the sample and were stored at – 80 °C until it was used for OTUs was tested by pairwise comparison. Each time DNA extraction. Metastats compares generated the corresponding P and The metagenomic DNA was extracted from 0.5 g Q values. The corrected P value is called Q value, and rhizosphere soil and purified by using PowerSoil DNA when P value < 0.05, the closer the Q value is to 0, the Isolation Kit (Mo Bio Laboratories Inc., Carlsbad, CA, lower the probability of false positive. Peng et al. Annals of Microbiology (2021) 71:40 Page 5 of 12 Results Molecular identification of the selected bacteria Selection of PGPR consortium The acquired 16S rDNA sequences of isolates P8, P10, Based on the PGP traits (Table 1), three isolates P8, P10, and X52 were approximately 1.5 kb in length, which and X52 were able to grow in the presence of 5% and have been deposited in GenBank database under the 10% (w/v) NaCl were selected for constructing the con- accession numbers MT879460, MT878549, and sortium. Isolate P8 showed the best N fixation ability MT878548, respectively. The BLAST search of these se- and the highest ACCD activity; P10 presented the best quences against the GenBank database demonstrated phosphate solubilization and N fixation ability, while that P8, P10 and X52 shared more than 99.7% of se- X52 produced the highest IAA production and consider- quence identity with reference strains for Pseudomonas able siderophore production (Table 1). The quantitative silesiensis, Peribacillus simplex, and Streptomyces micro- analyses of IAA and ACCD revealed that X52 produced flavus, respectively (Table 1). Therefore, the three −1 IAA as high as 70.58 μgmL , and P8 reached the isolates were identified as Pseudomonas sp. P8, Peribacil- −1 −1 ACCD activity of 8.01 mM mg h (Table 1). lus sp. P10, and Streptomyces sp. X52. Enhancing maize salt stress tolerance by inoculation of Inhibition to phytopathogenic fungi by P8, P10, and X52 P8/P10/X52 consortium The antimicrobial activities of the selected isolates were sum- As shown in Fig. 1, the maize seedlings grew similarly in marized in Table 1 (details available as Suppl. Table S1). All the sand substrate with 0 and 0.3% NaCl concentrations, the three isolates presented a certain degree of inhibition on and no significant difference was observed among differ- all the tested fungal strains, in which the isolate X52 had the ent treatments in all the four growth traits: shoot length, strongest inhibitory effects on four of the five pathogens (ex- root length, shoot dry weight, and root dry weight. So, cept F. oxysporium f. sp. cucumerinum HG-11), with the in- maize growth was not affected by the salinity of 0.3% of hibition rates from 43.00% for F. oxysporium f.sp. NaCl. However, the growth of maize seedlings was sig- cucumerinum HG-11 to 82.98% for B. maydis. For Fusarium, nificantly improved by inoculation of the mixture of P8, the highest inhibition (69.50%) was found in culture with iso- P10, and X52 in sand despite the tested level of NaCl, late P10. The broad antifungal spectrum presented in the on the 25th day after sowing, comparing with the con- three selected bacterial isolates, especially X52, evidenced trol group (P < 0.05) (Fig. 1). These results implied that them the potential for biological control application. the consortium could improve the maize growth under Table 1 Plant growth promoting traits and molecular identification of the selected strains in the consortium Tested trait Pseudomonas sp. P8 Peribacillus sp. P10 Streptomyces sp. X52 Morphological traits Round, yellow, opaque Smooth, bulging, slimy, white Dry, yellow, embed in the culture medium Phosphate solubilization 3 50 Nitrogen fixation 5 5 0 −1 b IAA production (μgmL ) 1 (21.87) 1 (11.25) 5 (70.58) −1 −1 ACCD activity (mM mg h ) 5 (8.01) 3 (7.27) 3 (4.58) Siderophore production 2 2 3 Growth at 5% (w/v) NaCl++ + 10% (w/v) NaCl++ + Growth Inhibition (IR%) to Pythium sp. 41.24 35.74 68.04 Fusarium sp. 23.00 69.50 43.00 Curvularia lunata 56.60 54.51 78.13 Bipolaria maydis 51.06 60.49 82.98 Phytophthora sp. 54.69 47.92 62.24 Most related species Pseudomonas silesiensis Peribacillus simplex Streptomyces microflavus Reference strain A3 NBRC 15720 126182 Accession no. of 16S rDNA NR156815 NR115603 JN180196 Identity of 16S rRNA gene 99.73% 99.87% 99.85% IR inhibition rates of mycelium growth, IR(%) (CR-TR/CR) × 100 The scores are estimated from the qualitative analysis, 0 = negative; 5 = the best Results of quantitative analysis Growth positive Peng et al. Annals of Microbiology (2021) 71:40 Page 6 of 12 Fig. 1 The effects of P8/P10/X52 consortium on maize growth in substrates supplied with 0.3% NaCl. In sand: a the shoot length of maize; b the root length of maize; c the shoot dry weight; d the root dry weight of maize. In soil: e the shoot length of maize; f the root length of maize; g the shoot dry weight; h the root dry weight of maize. CK, control. ** indicates the significant difference (p < 0.01) for treatments inoculated with P10/P8/X52 consortium compared with control (CK) low level of saline stress (0.3% NaCl). The effects of P8/ genes were obtained from the samples, with an average P10/X52 consortium on maize growth were also verified of 286,683 and 281,592 reads per sample of treatments in saline soil (0.3% NaCl) (Fig. 1), by analysis of the same and controls, respectively. These reads were rarefied to growth traits on the 25th day after sowing (P < 0.01) 6909 bacterial genes of each sample, corresponding to a (Fig. 1). These results suggest that P8/P10/X52 consor- total of 233,637 OTUs. The raw data have been depos- tium could promote the maize growth with or without ited in SRA database under the accession numbers slight salt stress. PRJNA562815. The OTU Shannon rarefaction curve (see Supplementary Fig. S1) tended to be flat and the Promotion of the beneficial bacteria in maize rhizosphere Simpson index (see Supplementary Table S2) for most by consortium inoculation of the samples were greater than 0.90 (ranging from 0.76 Compared with the treatment of P8/P10/X52 consor- to 0.99), suggesting that the sequencing depth of the tium, germination time of control seeds is 1 day later samples can reflect the species diversity in the samples. and the plants grew with more pests and diseases in the The analysis of OTUs revealed differences in microbial mixed 0.3% saline soil. The plant growth and root devel- community structure in rhizosphere of different growth opment in control were also the worst, and the lower stages and between control and P8/P10/X52 consortium leaves became yellowish at the tasseling period. Finally, inoculation (Fig. 2). The number of OTUs in the soil at the maize yield of the P8/P10/X52 inoculation treatment the time of planting was the least; as the maize grew, the increased by 16.52% (P <0.05) compared to that of the number of OTUs in the rhizosphere was increased; control. meanwhile, the bacterial abundance of treatment inocu- In the metagenomic analysis, a total of 626,785 high- lated with P8/P10/X52 consortium was lower than that quality reads for the V4–V5 region of the 16S rRNA of control. Peng et al. Annals of Microbiology (2021) 71:40 Page 7 of 12 Fig. 2 The number of OTUs of soil in maize rhizosphere in different periods. Note: O indicate that the soil at the time of planting; C1 indicate that the rhizosphere soil at the time of the three-leaf stage of control; C2 indicate that the rhizosphere soil at the time of the jointing stage of control; C3 indicate that the rhizosphere soil at the time of the tasseling stage of control; C4 indicate that the rhizosphere soil at the time of the maturity stage of control; T1 indicate that the rhizosphere soil at the time of the three-leaf stage of P8/P10/X52; T2 indicate that the rhizosphere soil at the time of the jointing stage of P8/P10/X52; T3 indicate that the rhizosphere soil at the time of the tasseling stage of P8/P10/X52; T4 indicate that the rhizosphere soil at the time of the maturity stage of P8/P10/X52 According to the PLS-DA (Fig. 3), the largest species inoculation of P8/P10/X52 consortium can enrich the diversity varied along the growth of maize plant. As rhizosphere microbiota and may promote the beneficial maize grew, the difference in diversity between the P8/ bacteria in the rhizosphere of maize grown in saline soil. P10/X52 inoculated treatments and the controls in- creased, and at the final maturity stage, the difference Discussion between the P8/P10/X52 treatments and the controls The use of PGPR in agriculture as a sustainable and eco- was the largest, suggesting that the microbial community friendly approach is a recommended strategy and an composition in rhizosphere of maize was always changed emerging trend in agriculture, including in saline soil related to the P8/P10/X52 inoculation. (Numan et al. 2018; Yang et al. 2009). In the previous The rhizosphere microbiota of maize varied among studies, salt-tolerant PGPR with various PGP traits have the four sampling stages, and the bacterial genera with been tested (Chatterjee et al. 2017; Egamberdieva et al. significantly abundance were different according to the 2015; Numan et al. 2018; Yang et al. 2009). However, treatments and the growth stages of maize (Table 2). most of the related studies used single strain as inocu- Some genera were more abundant in controls, but lant (Chatterjee et al. 2017; Egamberdieva et al. 2015), others were more abundant in P8/P10/X52 treatments, and the inoculation effects were unstable in some cases while several genera only existed in controls or in P8/ (Wu et al. 2012). For getting PGPR inoculant efficiently P10/X52 treatments. For instance, Exiguobacterium was improving the growth and yield of staple crops in saline only found in control at the three-leaf stage, and Cupria- land, we tried in the present study to use consortium of vidus only found in controls and Saccharopolyspora only PGPR as inoculant by combining strains with comple- recorded in P8/P10/X52 treatments at the jointing stage. mentary PGP traits and without nutrient competition, At the maturity stage, the significantly different genera and the results were encouraging. were the highest, and all of them presented higher abun- In the present study, a set of efficient bacteria screen- dances in P8/P10/X52 treatment. It's worth noting that ing methods was employed for searching salt-tolerance most of the genera with significant difference in abun- PGPR from the rhizosphere of herbal plant Sonchus bra- dance at the maturity stage were related to the biological chyotus grown in saline soil. Three strains of Pseudo- nitrogen fixation (such as Azotobacter, Sinorhizobium, monas sp. P8, Peribacillus sp. P10, and Streptomyces sp. and Devosia) and to nitrification (such as Candidatus X52 were selected based upon their salt tolerance and Nitrososphaera, Nitrosovibrio), which are beneficial for several growth promoting properties, as well as inhibit- restoring the soil ecology. These results suggest that ing several common pathogenic fungi (Table 1). The Peng et al. Annals of Microbiology (2021) 71:40 Page 8 of 12 Fig. 3 Characteristics of soil colony in rhizosphere of maize in different growth stages. Samples marked with three numbers: 101, 102,103 = repeats of soil at the time of planting; 111, 112, 113 = rhizosphere soil at the three-leaf stage of control; 121, 122, 123 = rhizosphere soil at the jointing stage of control; 131, 132, 133 = rhizosphere soil at the tasseling stage of control; 141, 142, 143 = rhizosphere soil at the maturity stage of control; 311, 312, 313 = rhizosphere soil at the three-leaf stage of inoculation (P8/P10/X52) treatment; 321, 322, 323 = rhizosphere soil at the jointing stage of inoculation treatment; 331, 332, 333 = rhizosphere soil at the tasseling stage of inoculation treatment; 341, 342, 343 = rhizosphere soil at the maturity stage of inoculation treatment inoculation of consortium composed of these three The mechanisms for the PGP effects of PGPR have strains could promote the seed germination and growth been reported and reviewed (Numan et al. 2018) previ- of maize plant in saline soil (Fig. 1). Previously, Pseudo- ously, which can be sorted into two aspects: (1) PGPR monas and Bacillus strains, as well as Azospirillum, Bur- stimulate the metabolic pathways of plants, such as kholderia, Rhizobium, Acetobacter, and Raoultella stimulating plant synthesis of growth hormones, trigger- planticola, have been used individually as PGPR to im- ing the antioxidant system and starting siderophore pro- prove growth of various plants grown in saline soils, like duction of plants, as well as augmenting nutritional red pepper and cotton plants, (Chatterjee et al. 2017; capacity of the plants. (2) The PGPR themselves produce Egamberdieva et al. 2015; Wu et al. 2012). Among the various phytohormones like auxins and cytokinins to im- three strains we selected, P10 belonged to the genus prove the growth of both roots and shoots, or improve Peribacillus that was proposed recently as a new genus nutrient supplement by phytopathogenic antagonism, separated from Bacillus (Patel and Gupta 2020), while mineral solubilization, and nitrogen-fixation. In the Streptomyces strains were also reported as PGP bacteria present study, the three selected strains presented some for different crops, like wheat grown in saline soil of the PGP traits (Table 1), which might be a part of (Akbari et al. 2020; Olanrewaju and Babalola 2019). So, their mechanism to help the maize plant in alleviating the isolation and identification of the three strains in the stresses of salinity as reported previously (Etesami and present study further revealed that Pseudomonas, Periba- Maheshwari 2018). Furthermore, these three strains cillus, and Streptomyces are common PGPR in saline were originately isolated from Sonchus brachyotus, but soils. Although the sequence identity (99.73% to 99.87%) the consortium formed by them showed significant PGP of 16S rRNA gene between these three strains and the effects on maize grown in the same soil; therefore, their closely related reference strain for defined species were host specificity is not strong, and they may also be used apparently greater than the suggested species threshold for other crops. (97%) (Gevers et al. 2005), we did not affiliate them into Except directly stimulating the plant growth, inocula- species, since the phylogeny of 16S rRNA gene is not tion of the consortium in our study also regulated the sensitive enough for species definition in many cases. microorganisms in the rhizosphere of maize: decreased Peng et al. Annals of Microbiology (2021) 71:40 Page 9 of 12 Table 2 The difference in quantity (relatively abundance) of the the amount of phytopathogenic bacteria and increase rhizosphere microbiota of maize at each stage the relative abundance of beneficial bacteria, especially the nitrogen-fixing bacteria and nitrifying bacteria (Table 2). These results added the third possible mechanism of PGPR: regulating the microbiota in rhizosphere and in turn promoting the growth of plants, in addition to the two aspects mentioned above (Numan et al. 2018). The variations in the rhizosphere microbiota of maize in re- spect to the consortium inoculation and the four growth stages (Table 2, Fig. 2) demonstrated that the rhizo- sphere microbiota was affected by the interactions be- tween the inoculated consortium and the plant biophysical status. This estimation was also supported by the results of PLS-DA (Fig. 3), in which a clear separ- ation in the rhizosphere microbiota of maize in different growth stages and treatments was observed. For in- stance, some of the microbiotas from samples of differ- ent treatments (with/without inoculation) and different growth stages showed close relationships, while those from the original soils and from the inoculation treat- ment in thematuritystage formed twogroupswith great difference. These findings were consistent with the previous observations on the plant associated bac- teria that their community composition was deter- mined by the interactions among soil properties, the plant species and the microbes (Román-Ponce et al. 2016; Zhang et al. 2011). In the present study, genus Exiguobacterium was only detected in control at the three-leaf stage. As salt- tolerance bacteria, Exiguobacterium usually presented in saline environments (Patel et al. 2018; Remonsellez et al. 2018; Zhang et al. 2019). Cupriavidus was only found in control and Saccharopolyspora was only detected in the consortium inoculated samples in the jointing stage. Cupriavidus usually exists in environments loaded with metal ion, and the bacteria in this genus have been screened from metal ion environments for bioremedi- ation of metal contamination (Huang et al. 2019; von Rozycki and Nies 2009). Therefore, both Exiguobacter- ium and Cupriavidus might be selected by maize for salt resistance in different growth stages, when the consor- tium inoculant was absent. The genus Saccharopolyspora contains potential producers of diverse natural products, including antibiotics (Sayed et al. 2020) and insecticide with an excellent environmental and mammalian profile (Tao et al. 2019). So, its augmentation by the consortium inoculation might be beneficial to maize for improving insect resistance, which may be the reason why the in- oculation treatment showed fewer pests and diseases (data not shown). At the maturity stage, the presence of more significantly enriched genera in P8/P10/X52 inocu- lated treatment (Table 2) might be related its greater The quantity is relatively abundance, red indicates that the genus quantity is higher in that group biomass accumulation (Fig. 1), which made the plant produce more root exudates to support greater abundant Peng et al. Annals of Microbiology (2021) 71:40 Page 10 of 12 and diverse rhizosphere microbes. For example, more of hydrogen; mm: Millimeter; ha: Hectare; min: Minute; rpm: Revolutions per minute; mL: Milliliter; KMB: King’B medium; IAA: Indole-3-acetic acid; ACCD: 1- root exudates (sugars, organic acids, amino acids etc.) aminocyclopropane-1-carboxylic acid deaminase; CFU: Colony forming unit; can offer greater carbon source to the biological N- rDNA: Ribosomal deoxyribonucleic acid; rRNA: Ribosomal ribonucleic acid; fixation and more ammonia to stimulate nitrification, QIIME: Quantitative insights into microbial ecology; NCBI: National Center for Biotechnology Information; SRA: Sequence read archive; OTUs: Operational which could be explain why the abundances of Azoto- taxonomic units; PLS-DA: Partial least squares discriminant analysis; bacter, Sinorhizobium, Devosia (N-fixers) and Candida- BLAST: Basic local alignment search tool; IR: Inhibition rates tus Nitrososphaera, Nitrosovibrio (nitrification bacteria) were increased in the inoculation treatment. Azotobacter Supplementary Information is usually applied for nitrogen fixation (Kennedy and The online version contains supplementary material available at https://doi. org/10.1186/s13213-021-01650-8. Toukdarian 1987), but also tolerant to abiotic stresses such as temperature, pH, and insecticides (Chennappa Additional file 1: Figure S1. The Length Distribution of sequences. et al. 2016). Root inoculation with Azotobacter chroococ- Figure S2. The OTU Shannon rarefaction curve. Figure S3. The OTU cum 76A could promote tomato plant growth, stress tol- chao1 rarefaction curve. Figure S4. The OTU observed species rarefaction curve. Supplementary Table S1. Details for antagonistic erance, and nutrient assimilation efficiency under ability of consortium strains to phytopathogenic fungi. Supplementary moderate and severe salinity (Van Oosten et al. 2018). Table S2. The Alpha diversity index of rhizosphere bacteria in the So, the change in rhizosphere microbiota by the consor- treatments. tium promoted the accumulation of beneficial bacteria in the rhizosphere of maize in saline soil. Therefore, the Acknowledgements This research was done as part of the Talents construction project of science consortium composed of Pseudomonas sp. P8, Peribacil- and technology innovation and the Doctoral Program, Hebei Academy of lus sp. P10, and Streptomyces sp. X52 is a promising in- Agriculture and Forestry Sciences. oculant, which has the potential to improve crop growth in saline soil. Meanwhile, such consortium as an inocu- Authors’ contributions Dong Hu, Zhanwu Wang, and Jieli Peng designed research and experiments. lant may have a more stable and effective impact than Jieli Peng wrote the main manuscript text. Jia Ma prepared part of Table 1 inoculants contained only one strain/species of micro- and Suppl. Table S1. Xiaoyan Wei prepared Fig. 1 and part of Table 1. organism, and it could be the future development direc- Cuimian Zhang, Nan Jia, and Xu Wang performed the plant pot experiment. En Tao Wang provided critical reading and revising suggestion. All authors tion of microbial inoculants. read, reviewed, and approved the manuscript. Although Pseudomonas sp. P8, Peribacillus sp. P10, and Streptomyces sp. X52 have beneficial effects in maize Funding This work was supported by funds from the Science &Technology Program growth and altered composition of rhizosphere bacterial of Hebei (19222902D) and the Project of Natural Science Foundation of community, the results of high-throughput sequencing Hebei Province (C2020301047). ETW was partially supported by the show that their number or abundance in the rhizosphere sabbatical project and SIP20200726 authorized by National Institute of Polytechnology of Mexico. of inoculated maize was not high. Therefore, they are likely to affect the growth of maize by stimulating and Availability of data and materials regulating certain genes of plants, as reported in other The raw data have been deposited in SRA database under the accession numbers PRJNA562815. studies (Pieterse et al. 2012; Yang et al. 2009), and medi- ating the rhizosphere microbiota (Table 2, Fig. 2)to Declarations affect the growth of maize. PGPRs initially recognized as agents to enhance defense capacity of above ground Ethics approval and consent to participate No applicable. parts, which was described as induced systemic resist- ance (ISR) with different pathways (Kawaharada et al. Consent for publication 2015; Pieterse et al. 2012; Zamioudis and Pieterse 2012). All the authors have approved the manuscript that is enclosed. In the future, we will study such regulation mechanism, Competing interests so as to find more efficient PGPR inoculants. The authors declare that they have no competing interests. Author details Conclusion Institute of Agro-resources and Environment (Hebei Fertilizer Technology P8/P10/X52 consortium can promote the growth of Innovation Center), Hebei Academy of Agriculture and Forestry Sciences, maize and promote the accumulation of beneficial bac- Shijiazhuang, Hebei, People’s Republic of China. Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico teria in the rhizosphere of maize in saline soil, which re- Nacional, C.P. 11340, Ciudad de México, México. vealed the possibility to use bacterial consortia as inoculants to enhance the crop production in saline Received: 17 June 2021 Accepted: 1 September 2021 soils. 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Annals of Microbiology – Springer Journals
Published: Dec 1, 2021
Keywords: Consortium inoculant; Saline soil; Rhizobacteria; Plant promoting trait; Maize