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Journal of Arid Land >

2025 , Vol. 17 >Issue 5: 696 - 713

DOI: https://doi.org/10.1007/s40333-025-0015-9

  • HUANG Yin 1, 2, 3 ,
  • ZHANG Xiaoye 1, 4 ,
  • MA Jinbiao 1, 2 ,
  • JIAO Haocheng 1, 3 ,
  • Murad MUHAMMAD 1, 3 ,
  • Rashidin ABDUGHENI 1, 2 ,
  • Vyacheslav SHURIGIN 1, 2 ,
  • Dilfuza EGAMBERDIEVA 1, 5 ,
  • LI Li , 1, 2, *
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收稿日期: 2024-09-27

  修回日期: 2025-02-20

  录用日期: 2025-03-24

  网络出版日期: 2025-08-12

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Diversity and plant growth-promoting properties of culturable bacteria associated with three halophytes in an arid land, Northwest China

  • HUANG Yin 1, 2, 3 ,
  • ZHANG Xiaoye 1, 4 ,
  • MA Jinbiao 1, 2 ,
  • JIAO Haocheng 1, 3 ,
  • Murad MUHAMMAD 1, 3 ,
  • Rashidin ABDUGHENI 1, 2 ,
  • Vyacheslav SHURIGIN 1, 2 ,
  • Dilfuza EGAMBERDIEVA 1, 5 ,
  • LI Li , 1, 2, *
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  • 1State Key Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
  • 2Xinjiang Key Laboratory of Biodiversity Conservation and Application in Arid Lands, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
  • 3University of Chinese Academy of Sciences, Beijing 100049, China
  • 4College of Life Sciences, Shihezi University, Shihezi 832003, China
  • 5Medical School, Central Asian University, Tashkent 111221, Uzbekistan
*LI Li (E-mail: )

Received date: 2024-09-27

  Revised date: 2025-02-20

  Accepted date: 2025-03-24

  Online published: 2025-08-12

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HUANG Yin , ZHANG Xiaoye , MA Jinbiao , JIAO Haocheng , Murad MUHAMMAD , Rashidin ABDUGHENI , Vyacheslav SHURIGIN , Dilfuza EGAMBERDIEVA , LI Li . [J]. Journal of Arid Land, 2025 , 17(5) : 696 -713 . DOI: 10.1007/s40333-025-0015-9

Abstract

Salt-tolerant bacteria associated with halophytes enhance plant resistance and adaptation to environmental stress. The purpose of this study was to investigate the diversity and plant-beneficial traits of bacteria associated with three halophytes in an arid land, Northwest China. The bacterial strains were isolated from the roots, shoots, rhizosphere, and bulk soil of three halophytes, i.e., Salicornia europaea L., Kalidium foliatum (Pall.) Moq., and Suaeda aralocaspica (Bunge) Freitag & Schütze, collected from the saline soils near to the Wujiaqu City, Xinjiang, Northwest China. A total of 567 strains were isolated and identified from these three halophytes belonging to 4 phyla, 6 classes, 25 orders, 36 families, and 66 genera, including 147 potential novel species. A total of 213 strains exhibited one or more plant growth- promoting properties, while 20 strains demonstrated multiple in vitro plant growth-promoting activities, including phosphate solubilization, nitrogen fixation, siderophore production, and production of hydrolytic enzymes such as protease and cellulase. Our findings showed that halophytes in the arid land harbor diverse bacteria with the potential to enhance plant growth and adaptability under challenging environmental conditions.

Key words： halophytes; endophytic bacteria; rhizosphere bacteria; diversity; functional strains

1 Introduction

Soil salinization is a global issue, seriously affecting soil resources and destroying the self-regulatory capacity of existing ecosystems (Singh, 2022; Zhao et al., 2022). Halophytes, or extremely salt-resistant plants, can thrive in habitats with salinity of 200 mM NaCl or higher, such as saline semi-deserts, saline soils, salt marshes, and seacoasts (Flowers and Colmer, 2008; Camacho-Sanchez et al., 2022).
Microbe-facilitated remediation strategies utilizing halophytes-associated bacteria to remediate saline soils are one of the essential methods to combat salinity (Ebadi et al., 2018; Khoshkholgh Sima et al., 2019). Halophyte-associated bacteria have evolved distinctive biochemical, physiological, and adoption strategies that enable halophytes to thrive in salinity (Etesami and Beattie, 2018; Kearl et al., 2019; Razzaghi Komaresofla et al., 2019; Xiong et al., 2020; Christakis et al., 2021; Dif et al., 2021). Priestia megaterium BP-R2 is an endophytic bacterium that enhances plant growth and stress tolerance under saline and drought conditions (Hwang et al., 2022). Bacillus sp. MA17 showed plant growth-promoting (PGP) properties under salt stress and efficiently reduced disease incidence in wheat by 64.50% (Hadj Brahim et al., 2022). The endophytic bacterium Acinetobacter johnsonii PC3 from Prosopis cineraria L. showed the highest biocontrol effectiveness with 82.00% disease reduction against cucumber damping-off caused by Pythium aphanidermatum under saline conditions (50 mM NaCl) (Al-Rashdi et al., 2022). These bacteria showed not only some PGP properties but also antagonistic activity, and have enormous potential to produce novel and important useful natural products (Bibi et al., 2018; Gao et al., 2021), increasing interest in the exploitation and utilization of bacteria associated with halophyte remediation.
The composition of plant microbiomes is largely shaped by a variety of abiotic stresses and environmental factors, rather than being determined solely by the host plant species. In particular, salinity is emerging as a pivotal force in the differentiation of microbiomes between halophytes and non-halophytes (Abdelfadil et al., 2024). The rhizosphere and endophytic microbial communities of halophytes display distinct structural and diversity patterns (Yuan et al., 2016), and these halophytes have the potential to elucidate the salt tolerance of non-halophytes (Zhang et al., 2024). In this context, elucidating the role of microbial diversity and function in saline soils becomes imperative for devising effective strategies to mitigate the adverse effects of salinity. Therefore, we hypothesize that there are significant differences between bacteria obtained from different halophytes, the diversity of bacteria is influenced by plant species and ecological niches, and some bacteria possess PGP properties and salt tolerance, which can enhance the salt tolerance of non-host plants.
The aims of this study are: (1) to isolate and identify culturable bacteria associated with three halophytes—Salicornia europaea L., Kalidium foliatum (Pall.) Moq., and Suaeda aralocaspica (Bunge) Freitag & Schütze—growing in saline soils using a culture-dependent approach and 16S rRNA (ribonucleic acid) gene sequencing; (2) to analyze the bacterial diversity and distribution patterns; and (3) to assess the PGP properties and salt stress tolerance of the isolated bacteria. The study will provide a scientific understanding of bacteria associated with the three halophytes and their potential to improve the agricultural productivity of high-saline soil in the arid land.

2 Materials and methods

2.1 Sample collection

Three halophyte species, i.e., S. europaea, K. foliatum, and S. aralocaspica, were collected from the saline soils of the Wujiaqu City, Xinjiang, Northwest China (44°13′38′′N, 87°40′16′′E). The study area belongs to the mid-temperate continental climate. The annual average temperature is 6℃-7℃, and the annual average precipitation is 190 mm. The soil exhibits highly alkaline conditions, with pH values ranging from 8.59 to 9.15, and significant salinity levels, as indicated by electrical conductivity (EC) values ranging from 8.40 to 12.93 mS/cm. Three individuals of healthy and disease-free plant species were selected in three replicates and randomly collected from sampling sites. Sample were then packed in aseptic bags and stored at 4℃ until further processing. Each sample was distinctly labeled in Table 1.
Table 1 Sample information and abbreviation from the three halophytes
Sample Salicornia europaea L.
(P1)		 Kalidium foliatum (Pall.) Moq.
(P2)		 Suaeda aralocaspica (Bunge)
Freitag & Schütze (P3)
Root and shoot (PE) P1PE P2PE P3PE
Rhizosphere soil (RR) P1RR P2RR P3RR
Bulk soil (RS) P1RS P2RS P3RS

2.2 Sample sterilization and pretreatment

Running tap water was used to wash away dirt, mud, and silt from the root systems and surfaces. The plant samples were subjected to ultrasonication at 45 kHz for 15 min until the water became clear. Surface sterilization was conducted on the plant samples by immersion in 75.00% alcohol for 1 min, followed by 5.00% NaClO for 2 min, and then rinsed three times with sterile distilled water in a laminar airflow chamber (Liu et al., 2017). To assess the efficiency of surface sterilization, we spread 100 µL aliquots of the final rinse water from each plant sample on the two selective isolation media, i.e., M1 (yeast: 0.25 g/L, K2HPO4: 0.50 g/L, NaCl: 30.00 g/L, and agar: 20.00 g/L) and M2 (tryptone: 15.00 g/L, soya peptone: 5.00 g/L, NaCl: 30.00 g/L, and agar: 20.00 g/L) ) (Gao et al., 2021) and incubated at 30℃ for one week. Aseptic plant samples were dissected into 1-2 cm fragments using a sterile surgical blade and dried in a laminar flow chamber. Samples were then placed in the sterilized commercial blender (Joyoung, JYL-C012, Hangzhou, China) for grinding (Li et al., 2018; Musa et al., 2020) and then preserved at -20℃.

2.3 Isolation and identification of bacteria

Each sample of 2 g was completely ground using a sterile mortar and pestle. The samples were transferred to a 50 mL Erlenmeyer flask containing 18 mL of sterile double-distilled water and incubated for 30 min at 30℃ and 100 r/m using a shaking incubator (Shanghai Tensuc Lab Instruments Manufacturing Co., Ltd., Shanghai, China). Dilutions were prepared to final concentrations of 10-3 and 10-5, and 100 µL of each dilution was plated onto the two selective isolation media (three replicates) and incubated at 30℃ for 15 d. Colonies exhibiting distinct morphologies were picked and purified by streaking 4 times on marine agar (MA) 2216 (BD Difco Sparks, New York, USA). Isolates were routinely cultured on MA at 30℃, maintained as a 20.00% (w/v) glycerol suspension, and stored at -80℃.
Deoxyribonucleic acid (DNA) extraction was performed using the Chelex-100 method (Walsh et al., 1991). Colonies were treated with 50 μL of a 5.00% Chelex-100 solution and boiled for 15 min. The supernatant served as template DNA to amplify the 16S rRNA gene sequence via polymerase chain reaction (PCR) using universal primers 27F (5'-GAGTTTGATCCTGGCTCAG- 3') and 1492R (5'-GAAAGGAGGTGATCCAGCC-3') (Beijing Biomed Gene Technology Co., Ltd., Beijing, China) (Bredow et al., 2015). The PCR mixture (50 µL) contained 4 µL (20-30 ng) template DNA, 25 µL 2×Taq PCR Master Mix, 2 µL of each primer (10 µmol/L), and was supplemented with DNase/RNase-free deionized water to 50 µL. PCR amplification on a C1000 Touch™ Thermal Cycler (Bio-Rad Laboratories Inc., Hercules, USA) was performed under the following conditions: pre-denaturation at 94℃ for 6 min, followed by 35 cycles of denaturation for 30 s at 94℃, annealing for 30 s at 55℃, and extension for 90 s at 72℃, with a final extension step at 72℃ for 7 min. The products were subsequently purified and sequenced by Sangon Biotech (Shanghai) Co., Ltd., China. Alignment of the 16S rRNA gene sequences was performed using the EzBioCloud database via an online alignment search tool (16S-based species-level identification). A sequence similarity below 98.65% indicated a putative novel species (Kim et al., 2014). The 16S rRNA gene sequences of bacteria determined in this study were deposited in the GenBank database in National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/) under the accession numbers OP662619-OP663185.

2.4 In vitro screening for plant-beneficial traits of bacterial isolates

2.4.1 Phosphate solubilization

Phosphate solubilization was assessed by inoculating isolates onto solid Pikovskaya medium supplemented with Ca3(PO4)2 (5.000 g/L) and bromophenol blue (0.025 g/L) with some modifications (Paul and Sinha, 2017; Abdelshafy Mohamad et al., 2020). The Petri dishes were inspected after incubation for 7 d at 30℃. The formation of clear zones or the color change from blue to yellow around the colonies indicated the utilization of tricalcium phosphate.

2.4.2 Siderophores production

Siderophore production was determined using a chrome azurol S (CAS) medium (Li et al., 2018). After incubation of isolates for 7 d at 30℃, the change of color from an orange/purple or purple/red halo zone indicated the production of siderophores (Alexander and Zuberer, 1991).

2.4.3 Assays for proteolytic and cellulolytic activity

The protease activity of isolates was determined by inoculating isolates onto 5.00% (v/v) skim milk agar medium using the spot inoculation technique (Tiru et al., 2013; Abdelshafy Mohamad et al., 2020). After 7 d of incubation at 30℃, clear zones surrounding the colonies indicated positive results. The cellulose activity of isolates was tested by inoculating on carboxymethylcellulose (CMC)-Na medium (KH2PO4: 1.500 g/L, NaH2PO4: 2.500 g/L, peptone: 2.500 g/L, carboxymethylcellulose sodium: 20.000 g/L, agar: 20.000 g/L, and pH: 7.0-7.5). After incubation for 7 d at 30℃, staining the plates with 5 mL of 0.10% Congo red solution for 15 min, followed by destaining with 5 mL of 1 M NaCl (Teather and Wood, 1982). A transparent or bright halo around the colonies indicated a positive reaction.
The ability to solubilize phosphate and produce siderophores, protease, and cellulose (E) was calculated using the following formula (Gao et al., 2021):
E = d 1 d 2 ,
where d1 is the diameter of the clear zone (mm); and d2 is the diameter of the isolate (mm). All experiments on plant-beneficial traits were performed twice, with three replicates for each isolate.

2.4.4 Nitrogen fixation activity

Nitrogen fixation was assayed by inoculating isolates on Ashby and non fiber carbohydrate (NFC) medium (Sen and Sen, 1965; Li et al., 2018). After 7 d of incubation at 30℃, the growth of colonies on both indicated nitrogen fixation activity.

2.4.5 Salt-tolerance assay

Bacterial tolerance to different NaCl concentrations (5.00%, 10.00%, 15.00%, and 20.00%; w/v) was tested using the Reasoner's 2A agar (R2A) medium. After incubation for 7 d at 30℃, we identified salt-tolerant bacteria based on colony growth on the agar plates.

2.5 Statistical analysis

All data obtained were statistically analyzed and visualized using Microsoft Excel v.2019 and R v.4.0.3 softwares.

3 Results

3.1 Diversity of culturable bacteria associated with the three halophytes

A total of 567 strains belonging to 4 phyla, 6 classes, 25 orders, 36 families, and 66 genera were isolated and purified from the plant and soil samples (root and shoot, rhizosphere, and bulk soil) of the three halophytes. At the phylum level (Fig. 1a), Actinomycetota (50.62%) was the predominant phylum in the three halophytes, followed by Bacillota (24.87%), Pseudomonadota (23.99%), and Bacteroidota (0.53%). At the class level (Fig. 1b), Actinomycetia (50.62%) was the dominant group. Predominant genera included Streptomyces, Halomonas, and Bacillus, accounting for 15.70%, 12.35%, and 12.17%, respectively (Fig. 1c). Analysis of the top 20 dominant genera among culturable bacteria across different samples revealed a high relative abundance of Streptomyces in P2RR, P3RR, and P2RS, Halomonas in P2RS and P3RS, Bacillus in P1PE, P3PE and P1RS, Nocardiopsis in P1RR and Brevibacterium in P2PE (Fig. 2).
Fig. 1 Community composition of culturable bacteria from the three halophytes at phylum (a), class (b), and genus (c) (top 20 dominant genera) levels
Fig. 2 Community composition at the genus level (top 20 dominant genera) (a) and flower diagram (b) at the species level of culturable bacteria isolated from different samples of the three halophytes (P1, P2, and P3). PE, RR, and RS indicate samples form root and shoot, rhizosphere soil, and bulk soil, respecitively. The detailed sample information is shown in Table 1. The abbreviations are the same in the following tables and figures.
Culturable bacteria from the three halophytes exhibited different levels of diversity (Table 2). P3PE had the highest richness, and Shannon and Simpson diversity indices (Table 2), suggesting a greater diversity of culturable endophytic bacteria of S. aralocaspica. The richness and Shannon
diversity index of P2RR exceeded those of P1RR and P3RR, and the richness, Shannon, and Simpson diversity indices of P2RS were higher than those of P1RS and P3RS (Table 2), indicating greater diversity of culturable rhizosphere and bulk soil bacteria of K. foliatum. The flower diagram additionally highlighted the variability in culturable bacteria across different plants and soil samples, with only one common species, Bacillus swezeyi (Fig. 2b), and the unique species of different plant and soil samples were shown in Table S1.
Table 2 Taxa and diversity of culturable bacteria
Group Index P1PE P2PE P3PE P1RR P2RR P3RR P1RS P2RS P3RS
Taxa Phylum 3 3 3 3 3 4 3 4 3
Class 4 5 4 4 4 5 4 5 3
Order 6 11 16 11 15 13 9 12 11
Family 6 16 18 13 17 15 11 14 12
Genus 7 24 25 16 21 20 18 22 16
Isolates 23 67 101 53 77 80 48 60 58
Diversity Richness 13.00 36.00 47.00 28.00 42.00 37.00 27.00 35.00 27.00
Shannon 2.36 3.39 3.57 3.02 3.47 3.40 3.04 3.29 2.98
Simpson 0.88 0.96 0.96 0.93 0.96 0.96 0.94 0.95 0.93
Pielou 0.92 0.93 0.93 0.91 0.93 0.94 0.92 0.92 0.90
Identificating strains by 16S rRNA gene, 147 strains showed less than 98.65% gene similarity and belonged to 29 genera, accounting for 25.93% of the total isolated strains. At the genus level, Streptomyces (37.41%) was the predominant genera of the potential novel strains, followed by Alkalihalobacillus (13.61%) and Microbacterium (7.48%) (Fig. 3). This result indicated that there were abundant new actinomycete resources among halophyte-related bacteria in the arid land.
Fig. 3 Phylogenetic tree of potential novel bacterial strains. The effective sequence length was 538 bp. Bar, the number of substitutions per sample.
Comparing the potential new species isolated from the three halophyte-associated bacteria, we observed that the diversity of novel species isolated from P2 was higher than those from P1 and P3 (Fig. 4), suggesting more new microbial resources in K. foliatum. Furthermore, comparing the potential novel species isolated from different plant and soil samples of the three halophytes at the genus level, we found that the diversity of new species was higher in P1RR, P2RR, and P3RR (Fig. 4), indicating potential new taxa in the rhizosphere of the three halophytes were more abundant. Above all, the bacteria associated with halophytes in the arid land possessed abundant microbial resources that remained largely untapped for excavation and utilization.
Fig. 4 Diversity of potentially novel bacterial strains isolated at the genus level

3.2 In vitro screening of bacterial strains for plant-beneficial traits

In the present study, 213 strains were screened for beneficial traits in vitro (Table S2). The proportions of phosphate solubilization isolates from PE, RR, and RS were 40.28%, 53.16%, and 41.94%, respectively (Fig. 5). The strains producing siderophores had a proportion of 29.17%, 64.56%, and 61.29% for PE, RR, and RS, respectively (Fig. 5). The proportion of strains with phosphate solubilization and siderophore production was the highest in RR, suggesting that strains with these capabilities were more readily isolated from soil, particularly rhizosphere soil. The proportions of strains producing protease in PE, RR, and RS were 38.89%, 39.30%, and 29.03%, respectively (Fig. 5). The proportions of cellulase-producing strains were 25.00%, 31.65%, and 25.81% for PE, RR, and RS, respectively (Fig. 5). Highly active cellulase-producing strains were higher in RR (16.46%) than in PE (8.33%) and RS (8.06%) (Fig. 5). This result suggested the rhizosphere bacteria of halophytes had more abundant microbial resources that produce cellulase.
Fig. 5 Screening results in bacterial strains solubilizing phosphate, producing siderophores, protease, and cellulase. ''‒'' indicates negative solubilization ability (E=1); ''+'' indicates weak solubilization ability (1<E≤2); ''++'' indicates moderate solubilization ability (2<E≤3); and ''+++'' indicates strong solubilization ability (E>3). E is the ability to solubilize phosphate and produce siderophores, protease, and cellulose.
Strains exhibiting nitrogen fixation in PE (68.06%), RR (46.84%), and RS (46.84%) were grown on both Ashby and NFC medium (Fig. 6). The proportion of nitrogen-fixing bacteria in PE was higher than those in RR and RS, suggesting that a richer endophytic bacteria in halophytes for nitrogen fixation. All strains tested tolerated 5.00% NaCl concentration, over 80.00% tolerated 10.00% NaCl concentration, about 50.00% withstood 15.00% NaCl concentration, and a subset in PE (19.44%), RR (8.86%), and RS (12.90%) resisted 20.00% NaCl concentration (Fig. 6). These results demonstrated the high salt tolerance of bacteria associated with halophytes. Among the tested strains, 20 exhibited five types of plant-beneficial traits in vitro, including phosphate solubilization, nitrogen fixation, siderophore production, protease, and cellulase (Table S2).
Fig. 6 Ability of nitrogen fixation and salt tolerance in bacterial strains. ''‒'' indicates negative and ''+'' indicates positive for nitrogen fixation and salt tolerance ability.

4 Discussion

The culturable bacteria associated with the three halophytes showed different levels of diversity. Diversity in RR exceeded those of RS in P2 and P3, but was lower in P1. The diversity of rhizosphere bacteria may be related to host plants and environments (Tkacz et al., 2015; Qiu et al., 2022). Culture-dependent methods rely on laboratory cultivation to study known and cultivable microorganisms, while culture-independent methods use genetic sequencing to reveal the full diversity of microbial communities, including uncultivable species. Two methods showed different results regarding the predominant genera of endophytic and rhizospheric bacteria from the three halophytes (Gao et al., 2022). More abundant and shared operational taxonomic units (OTUs) were found using the culture-independent method (Gao et al., 2022). However, there was only one shared species, Bacillus swezeyi. Therefore, relying solely on the culture-dependent method limits the comprehensive analysis of bacterial diversity.
Our findings revealed that 50.62% of the bacteria belonged to Actinomycetota, while only 7 bacteria were Actinomycetota when employing the culture-independent method (Gao et al., 2022). This result further confirmed that these two media exhibited strong selectivity for actinomycetes. Additionally, Euryarchaeota was detected in the rhizosphere microbiome of halophytes, including the Halobacteria, known for their survival in extremely saline environments (Gontia-Mishra et al., 2017; Gao et al., 2022). Considering the isolation of halophilic archaea in future processes is also advisable. Therefore, a range of media that accurately represents the diversity of culturable bacteria should be utilized for isolation.
In this study, we isolated 147 potential new strains, of which 98 belonged to Actinomycetota. Streptomyces constituted 37.41%, making it the predominant genus. Our findings revealed the rich resources of new Actinomycetota associated with halophytes in the arid land. These potential novel species may harbor the capacity to generate novel antibiotics and bioactive compounds (van der Meij et al., 2017; Mast and Stegmann, 2019; Thompson and Gilmore, 2024). At the same time, they can promote plant growth through mechanisms such as nitrogen fixation and phosphate solubilization (Compant et al., 2010), offering new application prospects for the field of agricultural biotechnology. Actinomycetota associated with halophytes likely possess unique adaptive mechanisms that enable survival in extreme environments (Abdelshafy Mohamad et al., 2018), encompassing osmotic pressure regulation, enhancement of antioxidant systems, and specific metabolic pathways. The adaptive traits of these potential novel species could enhance plant survival in arid and saline environments, providing new insights for ecological restoration and soil amelioration.
PGP bacteria could improve the availability of soil nutrients and partially reduce the need for fertilizers for plants without affecting natural microbial community structure (Chaudhary et al., 2020). Phosphate solubilizing strains could promote plant growth and hold potential as microbial fertilizers (Zhang et al., 2019; Chen et al., 2021; Wang et al., 2022). Advenella kashmirensis subsp. methylica MD2(2) demonstrated a strong and stable ability to dissolve inorganic phosphorus up to 283.69 μg/mL (Zhang and Yao, 2020). A. kashmirensis BKM20 (B1) exhibited significant potential for promoting plant growth (Benidire et al., 2021). Additionally, A. kashmirensis subsp. methylica is characterized as a methylotroph (Poroshina et al., 2015), capable of utilizing one-carbon (C1) compounds as the sole source of carbon and energy, and plays a key role in the carbon cycle between methane and CO2 (Iguchi et al., 2015). In this study, A. kashmirensis subsp. methylica EGI P1K047 likewise exhibited strong activity (Table S2). Due to the unique ecological niche, A. kashmirensis subsp. methylica EGI P1K047 possesses considerable potential for further application and exploration.
The three halophytic endophytics contained a significantly higher proportion of nitrogen-fixing bacteria compared with rhizosphere and bulk soil bacteria. Consistent with previous findings, the abundance of diazotrophic endophytic bacteria in S. europaea (Hrynkiewicz et al., 2019) supported our results. Endophytes in halophytes exhibited generally higher nitrogen metabolism compared with rhizosphere bacteria (Gao et al., 2022), further suggesting a stronger nitrogen fixation ability. Furthermore, all tested strains demonstrated high salt tolerance, tolerating up to 20.00% NaCl concentration. A greater proportion of endophytic strains from the three halophytes tolerated 20.00% NaCl concentration compared with rhizosphere and bulk soil strains, suggesting higher salt tolerance in endophytes. These strains possess significant PGP potential under salt stress, notably within the Halomonas and Bacillus (Kearl et al., 2019). Above all, halophytes in arid lands were potential sources of salt-tolerant bacteria with PGP abilities.

5 Conclusions

A total of 567 bacteria strains belonging to the phyla Actinomycetota, Bacillota, Pseudomonadota, and Bacteroidota were isolated from different ecological niches of the three halophytes in the arid land, Northwest China. All tested strains showed one or more PGP traits and high salt tolerance, with about 20 strains demonstrating abilities in phosphate solubilization, nitrogen fixation, siderophore production, protease, and cellulase activities. These findings provide scientific insights into the diversity of bacteria associated with the three halophytes and their potential to improve vegetation in salt-affected land.

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This research was funded by the Key Research and Development Project of Xinjiang Uygur Autonomous Region (2024B02015-3) and the Regional Coordinated Innovation Project (Shanghai Cooperation Organization Science and Technology Partnership Program) of Xinjiang Uygur Autonomous Region (2025E01024).

Author contributions

Conceptualization: HUANG Yin, ZHANG Xiaoye, MA Jinbiao, JIAO Haoche; Formal analysis: Murad MUHAMMAD, Vyacheslav SHURIGIN, Dilfuza EGAMBERDIEVA; Writing - review and editing: LI Li; Visualization: Rashidin ABDUGHENI. All authors approved the manuscript.

Appendix

Table S1 Unique species of culturable bacteria in different sites
Sampling site Unique species of culturable bacteria
P1PE Alkalihalobacillus pseudofirmus, Bacillus atrophaeus, Corynebacterium mucifaciens, Kocuria polaris, Kushneria marisflavi, Streptomyces murinus, and Streptomyces xiangtanensis
P2PE Advenella kashmirensis subsp. methylica, Arthrobacter gandavensis, Brevibacterium anseongense, Brevibacterium antiquum, Brevibacterium epidermidis, Brevibacterium sediminis, Citricoccus alkalitolerans, Corynebacterium glyciniphilum, Frigoribacterium endophyticum, Gordonia neofelifaecis, Gordonia terrae, Gracilibacillus ureilyticus, Kushneria pakistanensis, Mammaliicoccus sciuri, Microbacterium hydrocarbonoxydans, Mycolicibacterium frederiksbergense, Oceanobacillus picturae, Pelagibacterium luteolum, Salinicola corii, and Streptomyces melanosporofaciens
P3PE Aeromicrobium halocynthiae, Corynebacterium afermentans subsp. lipophilum, Demequina activiva, Demequina aestuarii, Halomonas titanicae, Luteimonas huabeiensis, Lysobacter spongiicola, Microbacterium amylolyticum, Microbacterium pumilum, Nesterenkonia halobia, Nocardiopsis alba, Ornithinimicrobium pekingense, Priestia filamentosa, Promicromonospora xylanilytica, Pseudarthrobacter oxydans, Rhizobium marinum subsp. pelagicum, Staphylococcus cohnii, Staphylococcus saprophyticus subsp. bovis, Streptomyces albidoflavus, Streptomyces daqingensis, Streptomyces microflavus, Streptomyces pseudovenezuelae, and Streptomyces violascens
P1RR Halobacillus litoralis, Lipingzhangella halophila, Paracoccus marcusii, Planococcus plakortidis, and Streptomyces sodiiphilus
P2RR Georgenia yuyongxinii, Halomonas stenophila, Marinococcus salis, Prauserella aidingensis, Streptomyces anulatus, Streptomyces diacarni, Streptomyces indonesiensis, Streptomyces rimosus subsp. rimosus, and Zhihengliuella salsuginis
P3RR Anaerobacillus isosaccharinicus, Chelativorans xinjiangense, Halomonas olivaria, Microbacterium suaedae, Nocardiopsis chromatogenes, Planococcus salinarum, and Streptomyces monticola
P1RS Haloechinothrix halophila, Halomonas montanilacus, Halomonas sulfidaeris, Marinobacter lipolyticus, Nesterenkonia aurantiaca, Paenisporosarcina quisquiliarum, Planococcus antarcticus, Planomicrobium iranicum, Streptomyces albospinus, and Virgibacillus salarius
P2RS Arthrobacter ruber, Exiguobacterium mexicanum, Galbibacter mesophilus, Halomonas huangheensis, Isoptericola salitolerans, Myceligenerans xiligouense, Nocardioides marinus, Streptomyces aqsuensis, Streptomyces artemisiae, Streptomyces flocculus, and Streptomyces lopnurensis
P3RS Alcanivorax xenomutans, Halomonas elongata, Halomonas ventosae, Salininema proteolyticum, Streptomyces cellulosae, Streptomyces flavovirens, Streptomyces lusitanus, and Streptomyces panacagri
Table S2 Potential plant-beneficial traits of bacteria associated with the three halophytes
Strain Phosphorus Siderophore Hydrolytic enzyme Nitrogen fixation Salt-tolerant concentration
Protease Cellulase 5.00% 10.00% 15.00% 20.00%
EGI P1B004 + + ‒ ‒ + + + + +
EGI P1B007 + ‒ ‒ ‒ ‒ + + + +
EGI P1B018 ‒ + ‒ ‒ ‒ + + + ‒
EGI P1B021 ‒ ‒ ‒ ‒ + + ‒ ‒ ‒
EGI P1B030 + + ‒ ‒ + + ‒ ‒ ‒
EGI P1B031 ‒ ‒ ‒ ‒ ‒ + ‒ ‒ ‒
EGI P1B032 ‒ ‒ ‒ ‒ ‒ + + ‒ ‒
EGI P1B037 ‒ ‒ ‒ ‒ + + + + ‒
EGI P1B041 ‒ + ‒ ‒ ‒ + + + +
EGI P1B044 ‒ ‒ +++ +++ + + + + ‒
EGI P1B047 ‒ ‒ ‒ + ‒ + ‒ ‒ ‒
EGI P1B048 + ‒ ‒ ‒ + + + + ‒
EGI P1B049 ‒ ‒ + ‒ + + + + ‒
EGI P1B050 ‒ ‒ ‒ ‒ ‒ + ‒ ‒ ‒
EGI P1B053 ‒ ‒ ‒ ‒ ‒ + + + +
EGI P1B057 ++ ‒ + ++ + + + + ‒
EGI P1B059 + ‒ + ‒ ‒ + ‒ ‒ ‒
EGI P1B060 ‒ ‒ ‒ ‒ + + + ‒ ‒
EGI P1B065 ‒ ‒ + ‒ + + + + ‒
EGI P1B067 ‒ + ‒ ‒ ‒ + + + +
EGI P1B068 ‒ ‒ + ++ + + + ‒ ‒
EGI P1B072 ‒ + ‒ ‒ + + + + ‒
EGI P1B073 ‒ ‒ ‒ ‒ + + + + +
EGI P1B074 ‒ ‒ + ‒ ‒ + + ‒ ‒
EGI P1B076 ‒ ‒ ‒ ‒ ‒ + ‒ ‒ ‒
EGI P1B078 + + + ‒ + + + ‒ ‒
EGI P1B079 ‒ + ‒ ‒ + + + ‒ ‒
EGI P1B081 ++ + + + + + + + ‒
EGI P1B088 + + ++ +++ + + ‒ ‒ ‒
EGI P1B089 + + ++ +++ + + ‒ ‒ ‒
EGI P1B090 ‒ ‒ ‒ ‒ ‒ + + ‒ ‒
EGI P1B091 + ‒ + ++ + + + ‒ ‒
EGI P1B094 ‒ + ‒ ‒ ‒ + + + +
EGI P1B101 ‒ ‒ + ‒ ‒ + + + ‒
EGI P1K001 + ‒ ‒ ‒ + + + + +
EGI P1K005 ++ + ‒ ‒ + + + + +
EGI P1K006 + ‒ + ++ + + + + ‒
EGI P1K020 ‒ ‒ ‒ ‒ ‒ + + + ‒
EGI P1K021 ‒ ‒ ‒ +++ + + + ‒ ‒
EGI P1K024 ‒ ‒ ‒ ‒ ‒ + + + +
EGI P1K025 ‒ ‒ + ‒ + + + + ‒
EGI P1K026 ‒ ‒ + ‒ + + + + ‒
EGI P1K028 ‒ ‒ ‒ ‒ + + + + ‒
EGI P1K029 + ‒ ‒ ‒ ‒ + + ‒ ‒
EGI P1K030 ‒ ‒ ‒ ‒ + + + + ‒
EGI P1K031 ‒ ‒ ‒ ‒ ‒ + ‒ ‒ ‒
EGI P1K036 ‒ ‒ + ‒ + + + + ‒
EGI P1K037 + ‒ + ‒ + + + + ‒
EGI P1K039 ‒ ‒ ‒ + ‒ + + ‒ ‒
EGI P1K041 ‒ ‒ ‒ ‒ + + + + ‒
EGI P1K042 + ‒ + ‒ + + + + ‒
EGI P1K043 + ‒ + + ‒ + ‒ ‒ ‒
EGI P1K047 +++ + ‒ ‒ + + + ‒ ‒
EGI P1K050 ++ + ‒ ‒ + + + ‒ ‒
EGI P1K052 + + + + + + + + ‒
EGI P1K056 ‒ ‒ ‒ ‒ + + + ‒ ‒
EGI P1K057 + ‒ ++ ++ + + + ‒ ‒
EGI P1K058 ‒ + ‒ ‒ ‒ + + + +
EGI P1K061 ‒ + ‒ ‒ ‒ + + + +
EGI P1K065 + ‒ ‒ ‒ + + ‒ ‒ ‒
EGI P1K067 ‒ + ‒ ‒ + + ‒ ‒ ‒
EGI P1S002 + ‒ + +++ + + + + ‒
EGI P1S006 ‒ ‒ ‒ ‒ + + + + ‒
EGI P1S007 ‒ ‒ ‒ ‒ + + + + ‒
EGI P1S009 + ‒ + ++ + + ‒ ‒ ‒
EGI P1S012 ‒ ‒ ‒ ‒ + + + ‒ ‒
EGI P1S013 ++ ++ + ‒ + + + + ‒
EGI P1S017 + ‒ + +++ + + + ‒ ‒
EGI P1S018 + ‒ + ‒ + + + + +
EGI P1S019 + + + + + + + + ‒
EGI P1S022 ‒ ‒ ‒ ‒ + + + + +
EGI P1S023 ‒ ‒ ‒ ‒ + + + ‒ ‒
EGI P2B001 + + + ++ + + + + ‒
EGI P2B006 + + ‒ ‒ + + + + +
EGI P2B012 ‒ + ‒ ‒ ‒ + + + +
EGI P2B013 + + ‒ ‒ + + + + ‒
EGI P2B016 ‒ ‒ + ‒ + + + ‒ ‒
EGI P2B027 + + ‒ +++ + + + ‒ ‒
EGI P2B029 + + ‒ ‒ ‒ + + + ‒
EGI P2B034 ‒ ‒ ‒ ‒ ‒ + + ‒ ‒
EGI P2B035 ‒ ‒ + ‒ ‒ + ‒ ‒ ‒
EGI P2B038 + + + + + + + ‒ ‒
EGI P2B040 ‒ + ‒ ‒ ‒ + ‒ ‒ ‒
EGI P2B042 + + ‒ ‒ ‒ + + ‒ ‒
EGI P2B045 + + ‒ ‒ ‒ + + ‒ ‒
EGI P2B046 + ‒ ‒ + ‒ + + + +
EGI P2B047 + + +++ +++ + + + ‒ ‒
EGI P2B049 + ‒ + ++ + + + ‒ ‒
EGI P2B050 + + ‒ ‒ ‒ + + + ‒
EGI P2B054 ++ + + +++ + + + ‒ ‒
EGI P2B055 ‒ ‒ ++ ‒ + + + + ‒
EGI P2B056 + + + ++ ‒ + + + ‒
EGI P2B057 + ‒ ‒ ‒ ‒ + + + ‒
EGI P2B058 + + ‒ ‒ ‒ + + ‒ ‒
EGI P2B059 ‒ ‒ ‒ ‒ ‒ + + + ‒
EGI P2B075 + + ‒ ‒ ‒ + + + ‒
EGI P2B077 ‒ ‒ ‒ ‒ ‒ + + ‒ ‒
EGI P2B079 + ‒ ‒ ‒ + + + + +
EGI P2K001 + + + + + + + + ‒
EGI P2K007 + + ++ +++ + + ‒ ‒ ‒
EGI P2K008 ‒ ‒ ‒ ‒ + + + ‒ ‒
EGI P2K009 ‒ + + ‒ ‒ + + + ‒
EGI P2K011 + ‒ ‒ ‒ + + + ‒ ‒
EGI P2K012 + ‒ +++ + ‒ + + ‒ ‒
EGI P2K017 + + ‒ ‒ ‒ + + ‒ ‒
EGI P2K019 + ‒ + ‒ ‒ + + ‒ ‒
EGI P2K020 ‒ + + ‒ ‒ + + + ‒
EGI P2K022 ‒ ‒ ‒ ‒ ‒ + + + ‒
EGI P2K028 + ‒ + +++ + + + + ‒
EGI P2K030 + ‒ ‒ +++ ‒ + + ‒ ‒
EGI P2K031 + ‒ + ‒ + + + ‒ ‒
EGI P2K032 ++ + ‒ + + + + ‒ ‒
EGI P2K034 + + ‒ ‒ + + ‒ ‒ ‒
EGI P2K035 + ‒ + +++ + + + ‒ ‒
EGI P2K039 ‒ ‒ ‒ ‒ ‒ + + ‒ ‒
EGI P2K040 + ‒ + ‒ + + + ‒ ‒
EGI P2K041 ‒ ‒ + ‒ ‒ + + + ‒
EGI P2K043 ‒ + ‒ ‒ + + + + ‒
EGI P2K047 + + ++ ++ + + + ‒ ‒
EGI P2K050 ‒ + ‒ ‒ ‒ + + ‒ ‒
EGI P2K052 ‒ + ‒ ‒ + + + + ‒
EGI P2K053 + ‒ ‒ ‒ + + + ‒ ‒
EGI P2K054 + + ‒ ‒ ‒ + + ‒ ‒
EGI P2K055 ‒ + ‒ ‒ ‒ + + + ‒
EGI P2K059 + + ‒ +++ ‒ + + ‒ ‒
EGI P2K060 ‒ + + ‒ + + + ‒ ‒
EGI P2K061 ‒ + ‒ ‒ + + + ‒ ‒
EGI P2K064 ‒ + ‒ ‒ ‒ + + + +
EGI P2K068 ‒ + + ‒ + + + ‒ ‒
EGI P2K071 + ‒ ‒ ‒ ‒ + ‒ ‒ ‒
EGI P2K074 ‒ + ‒ + ‒ + + + ‒
EGI P2K075 ‒ ‒ ‒ ‒ + + + ‒ ‒
EGI P2K076 + + ‒ +++ ‒ + + + ‒
EGI P2S006 ‒ + ‒ ‒ ‒ + + + ‒
EGI P2S007 ‒ + ‒ ‒ ‒ + + + ‒
EGI P2S008 + + + +++ + + + + ‒
EGI P2S009 + + ‒ ++ + + + + ‒
EGI P2S010 ‒ ‒ + ‒ ‒ + + ‒ ‒
EGI P2S013 ‒ ‒ ‒ ‒ ‒ + + + ‒
EGI P2S019 ‒ + + ‒ + + ‒ ‒ ‒
EGI P2S020 ‒ + ‒ ‒ ‒ + + ‒ ‒
EGI P2S022 ‒ + ‒ +++ ‒ + ‒ ‒ ‒
EGI P2S024 + + ‒ +++ + + + + +
EGI P2S027 + + + ++ ‒ + + + ‒
EGI P2S034 ‒ + + +++ + + + + ‒
EGI P2S036 ‒ ++ ‒ ‒ + + ‒ ‒ ‒
EGI P2S040 ‒ ‒ ++ ‒ ‒ + + + +
EGI P2S043 ‒ + + ‒ + + + + ‒
EGI P2S045 ‒ + ‒ ‒ + + + + ‒
EGI P2S051 ‒ + ‒ ‒ ‒ + + + ‒
EGI P2S052 + + + ‒ ‒ + + ‒ ‒
EGI P3B002 ‒ + ‒ ‒ ‒ + + + ‒
EGI P3B004 + + + + + + + + ‒
EGI P3B010 ‒ + +++ ‒ + + + + ‒
EGI P3B011 ‒ + ‒ ‒ ‒ + + + ‒
EGI P3B014 ‒ ‒ +++ ‒ ‒ + + + ‒
EGI P3B023 ‒ ‒ ‒ +++ ‒ + + ‒ ‒
EGI P3B024 ‒ + ‒ ‒ ‒ + + ‒ ‒
EGI P3B025 + + + ++ + + + + ‒
EGI P3B026 + + ++ +++ + + ‒ ‒ ‒
EGI P3B033 + + ‒ ++ + + + ‒ ‒
EGI P3B035 + + ‒ ‒ ‒ + + + +
EGI P3B037 ‒ + ‒ ‒ + + + ‒ ‒
EGI P3B039 ‒ + ‒ ‒ ‒ + + + ‒
EGI P3B040 + ‒ ‒ ‒ + + + + +
EGI P3B044 ‒ ‒ ‒ ‒ + + + + ‒
EGI P3B047 + + ‒ ‒ + + + + ‒
EGI P3B048 + ‒ + ++ + + + + ‒
EGI P3B055 ‒ + ‒ ‒ ‒ + + + +
EGI P3B056 ‒ ‒ ‒ ‒ ‒ + + + +
EGI P3B057 ‒ + ‒ ‒ ‒ + ‒ ‒ ‒
EGI P3B058 + ‒ ‒ ‒ ‒ + + + +
EGI P3K001 + ++ + + + + + + ‒
EGI P3K005 ‒ ‒ ‒ +++ ‒ + ‒ ‒ ‒
EGI P3K007 + + ‒ ‒ + + + ‒ ‒
EGI P3K008 ‒ ‒ ‒ ‒ ‒ + + + +
EGI P3K009 ‒ ‒ ‒ +++ + + + ‒ ‒
EGI P3K010 + ‒ +++ ‒ ‒ + + ‒ ‒
EGI P3K011 ‒ ‒ + ‒ ‒ + + + ‒
EGI P3K014 ‒ ‒ ‒ + ‒ + + ‒ ‒
EGI P3K015 + ‒ ‒ ‒ ‒ + ‒ ‒ ‒
EGI P3K016 ‒ + ‒ ‒ ‒ + + + ‒
EGI P3K021 + + ‒ ‒ ‒ + + + ‒
EGI P3K023 + ++ + ‒ + + + + ‒
EGI P3K026 + + ‒ + + + + ‒ ‒
EGI P3K027 ‒ + ‒ ‒ ‒ + + + ‒
EGI P3K030 + + + + + + + ‒ ‒
EGI P3K034 ‒ ‒ ‒ ‒ + + + + ‒
EGI P3K035 + + ‒ ‒ ‒ + + + ‒
EGI P3K036 ‒ + ++ ‒ ‒ + + + ‒
EGI P3K041 + + ‒ +++ ‒ + ‒ ‒ ‒
EGI P3K045 + ‒ ‒ ‒ ‒ + + + +
EGI P3K046 ‒ + ‒ ‒ + + + + +
EGI P3K047 ‒ + ‒ ‒ + + + ‒ ‒
EGI P3K051 ‒ ‒ ‒ ‒ + + + ‒ ‒
EGI P3K056 + ‒ + + + + + + ‒
EGI P3K057 ‒ ‒ ‒ ‒ + + + + ‒
EGI P3K058 ‒ + ‒ ‒ + + + ‒ ‒
EGI P3K059 ‒ ‒ + ‒ ‒ + + + ‒
EGI P3S001 + + + + + + + + ‒
EGI P3S003 + ‒ + ‒ + + + + ‒
EGI P3S005 ‒ ‒ ‒ ‒ ‒ + + ‒ ‒
EGI P3S009 + + ‒ ‒ ‒ + + ‒ ‒
EGI P3S010 ‒ + ‒ ‒ ‒ + + + ‒
EGI P3S014 + ‒ ‒ ‒ ‒ + + + ‒
EGI P3S015 + + + + + + + + ‒
EGI P3S024 ‒ + ‒ ‒ ‒ + + ‒ ‒
EGI P3S026 ‒ + ‒ ‒ ‒ + + + ‒
EGI P3S031 ‒ + ‒ ‒ + + + ‒ ‒
EGI P3S037 ‒ + + ‒ ‒ + + + ‒
EGI P3S039 ‒ ‒ ‒ ‒ ‒ + + ‒ ‒
EGI P3S042 ‒ + ‒ ‒ ‒ + + ‒ ‒
EGI P3S046 ‒ + ‒ ‒ ‒ + + + ‒

Note: ‒, negative (E=1); +, weak (1<E≤2); ++, moderate (2<E≤3); +++, strong (E>3). The ability to nitrogen fixation and salt-tolerant was recorded as ''+'' if strain grows on the test media. E is the ability to solubilize phosphate and produce siderophores, protease, and cellulose.

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