Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (20): 4131-4143.doi: 10.3864/j.issn.0578-1752.2025.20.008

• SOIL MICROORGANISMS • Previous Articles     Next Articles

Isolation and Identification of Rhizosphere Growth-Promoting Bacteria of Myroides odoratimimus PJ-3 and Their Salt/ Alkali-Tolerance and Growth-Promoting Effects on Maize

WU DongMing1,2,3,4(), XU Jing1,5, YUAN JiaMei1,3, WANG KeXuan1,3, LI YuYi1,3, HE Ping1,3, ZHANG JianFeng1,3, SONG DaLi1,3, GAO Miao1,3(), ZHOU Wei1,3()   

  1. 1 State Key Laboratory of Efficient Utilization of Arid and Semi-Arid Arable Land in Northern China/Key Laboratory of Plant Nutrition and Fertilizer, Key Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs (Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences), Beijing 100081
    2 Institute of Environment and Plant Protection, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101
    3 National Center of Technology Innovation for Comprehensive Utilization of Saline-Alkali Land, Dongying 257347, Shandong
    4 Danzhou Scientific Observing and Experimental Station of Agro-Environment, Ministry of Agriculture and Rural Affairs National Agricultural Green Development Long-Term Fixed Observation Danzhou Experimental Station, Danzhou 571737, Hainan
    5 Administrative Committee of Jiangning Hushu Modern Agricultural Industrial Park of Jiangsu Province, Nanjing 211121
  • Received:2025-07-16 Accepted:2025-09-30 Online:2025-10-16 Published:2025-10-14
  • Contact: GAO Miao, ZHOU Wei

Abstract:

【Objective】Soil salinization is a significant limiting factor for global agricultural production and food security. Based on the mutualistic symbiotic relationships between rhizosphere beneficial bacteria (PGPR) and plants, this study aimed to screen out PGPR strains that possessed multiple functions, such as salt tolerance, alkali tolerance, and promoting growth, with the salt-stressed soil from maize rhizosphere. The study would provide raw materials and theoretical basis for the development of microbial agents for salt-alkali soil improvement and support the comprehensive management of salt-alkali land. 【Method】The PGPR strains were isolated by using the dilution plate coating method. The isolates were identified through morphological and microscopic observation, Biolog Gen III microplate analysis, and 16S rRNA gene sequencing. A microcosmic experiment was employed to assess the salt-alkali tolerance and plant growth promotion potential (PGP) of the PGPR strains. 【Result】23 PGPR isolates were screened and obtained, and the PJ-3 isolate exhibited the optimal salt-alkali tolerance and PGP potential. It was identified as Myroides odoratimimus with the attributes of Gram-negative. Specifically, the strain PJ-3 possessed a robust fructose-glycolytic pathway and lactic acid-pyruvate and phosphosugar transformation systems, enabling tolerance to extreme saline-alkaline conditions of up to 5% NaCl with a pH of 11. Pot experiments further demonstrated that under moderate saline-alkaline stress, the strain PJ-3 significantly increased maize germination rate of maize by 70% and promoted plant height, leaf length, leaf width, aboveground fresh weight, and belowground fresh weight by over 50%. Further analysis revealed that its superior tolerance and PGP mechanisms included the secretion of proteases, siderophores, and the plant hormone IAA (indole-3-acetic acid), activation of reactive oxygen species (ROS) scavenging by antioxidant enzymes SOD (superoxide dismutase) and CAT (catalase) in maize. Moreover, it could stimulate the conservative growth strategy in roots, with the enchantment in root surface area, root tip number, branching frequency and root vigor. As a result, these positive effects improved the improved chlorophyll a-dominated photosynthesis. 【Conclusion】Collectively, it was the first to report that Myroides odoratimimus PJ-3 possesses multiple novel functions, including remarkable salt tolerance, alkali tolerance, and the promotion of both aboveground and belowground development in maize. It demonstrated broad application potential for the integrated management of saline-alkaline lands and agricultural development.

Key words: myroides odoratimimus, saline-alkali stress, promoting potential, root development, antioxidant enzyme activity

Fig. 1

Morphological characteristics (A) and Gram staining condition (B) of strain PJ-3 on NA medium"

Table 1

Utilization characteristics of strain PJ-3 for different carbon and nitrogen sources"

碳源种类
Carbon type
利用特征
Utilization
碳源种类
Carbon type
利用特征
Utilization

碳源种类
Carbon type
利用特征
Utilization
葡聚糖 Dextran - D-山梨醇 D-sorbitol - 粘液酸 Mucic acid -
D-麦芽糖 D-maltose - D-甘露醇 D-mannitol - 奎尼酸 Quinateic acid -
D-海藻糖 D-trehalose - D-阿拉伯醇 D-arabitol - D-葡糖二酸 D-glucaric acid -
D-纤维二糖 D-cellobiose - myo-肌醇 Myo-inositol - 万古霉素 Vancomycin +
龙胆二糖 Gentiobiose - 丙三醇 Glycerol - 四唑紫 Tetrazolium violet +
蔗糖 Sucrose - D-葡萄糖-6-PO4 D-glucose-6-PO4 - 四唑蓝 Tetrazolium blue +
葡聚糖 Glucan - D-果糖-6-PO4 D-fructose-6-PO4 + p-Hydroxy-苯乙酸 p-Hydroxy-phenylacetic acid -
D-松二糖 D-turanose - D-天冬氨酸 D-aspartic acid - 丙酮酸盐 Pyruvate -
水苏糖 Stachyose - D-丝氨酸 D-serine - D-乳酸甲酯 D-lactic methyl eslactate -
D-蜜三糖 D-raffinose - 醋竹桃霉素 Troleandomycin - L-乳酸 Lactic acid -
α-D-乳糖 α-D-lactose - 利福霉素SV Rifamycin SV + 柠檬酸 Citric acid -
D-蜜二糖 D-melibiose W 二甲胺四环素 Minocycline - α-Keto-戊二酸 α-Keto-valeric +
β-Methyl-D葡萄糖苷
β-Methyl-D glucoside
- 明胶
Gelatin
+ D-羟基丁二酸
D-hydroxybutyric acid
-
D-水杨甙 D-salicin - Glycyl-L-脯氨酸 Glycyl-L-proline + L-羟基丁二酸 L-hydroxybutyric acid +
N-Acetyl-D葡萄糖胺
N-Acetyl-D-glucosamine
- L-丙氨酸
L-alanine
- Bromo-琥珀酸
Bromo-succinic acid
-
N-Acetyl-β-D甘露糖胺
N-Acetyl-β-D-mannosamine
- L-精氨酸
L-arginine
- 萘啶酮酸
Nalidixic acid
W
N-Acetyl-D半乳糖胺
N-Acetyl-D galactosamine
- L-天(门)冬氨酸
L-aspartic acid
+ 氯化锂
Lithium chloride
-
α-D-葡萄糖 α-D-glucose - L-谷氨酸 L-glutamic acid + 亚碲酸钾 Potassium tellurite -
D-甘露糖 D-mannose - L-组氨酸 L-histidine - 吐温40 Tween 40 -
D-果糖 D-fructose - L-焦谷氨酸 L-cysteine glutamate - γ-Amino-丁酸 γ-Amino-butyric acid -
D-半乳糖 D-galactose + L-丝氨酸 L-aspartic acid - α-Hydroxy-丁酸 α-Hydroxy-butyric acid -
3-Methyl 葡萄糖
3-Methyl glucose
- 洁霉素
Lincomycin
+ β-Hydroxy-D,L-丁酸
β-hydroxy-D,L-butyric acid
-
D-海藻糖 D-trehalose - 盐酸胍 Guanidinium chloride + α-Keto-丁酸 α-Keto-butyric acid -
L-海藻糖 L-trehalose W 硫酸四癸钠 Sodium tetradecyl sulfate - 乙酰乙酸 Acetoacetic acid -
L-鼠李糖 L-rhamnose W 果胶 Pectin - 丙酸 Propionic acid -
肌苷 Inosine - 半乳糖醛酸 D-galacturonic acid + 醋酸 Acetic acid -
1%乳酸钠 1% sodium lactate - L-半乳糖酸 L-galactonic acid + 甲酸 Formic acid -
梭链孢酸 Fusidic acid + D-葡(萄)糖酸 D-glucose acid - 氨曲南 Aztreonam +
D-丝氨酸 D-serine - 葡萄糖醛酸 D-glucuronic acid W 丁酸钠 Sodium butyrate +

Fig. 2

Phylogenetic tree of strain PJ-3 based on 16S rRNA gene sequence"

Fig. 3

Growth characteristics of strain PJ-3 under different salt stress (A) and alkali stress (B)"

Table 2

Promoting characteristics of strain PJ-3"

促生特征
Promoting characteristics
透明圈或含量
Transparent ring or content
蛋白酶Protease (D/d) 4.37±1.07
铁载体Ironophore (D/d) 2.22±0.19
IAA (μg·mL-1) 1.35±0.32

Fig. 4

The effects of strain PJ-3 on the germination rate (A), shoot length (B), and root length (C) of maize seeds ** means highly significant difference with P<0.01。下同 The same as below"

Fig. 5

The effect of strain PJ-3 on the growth of maize"

Fig. 6

The effect of strain PJ-3 on the photosynthesis of maize leaves"

Fig. 7

The influence of strain PJ-3 on the root development of maize"

Fig. 8

The influence of strain PJ-3 on the stress-resistant enzyme activities in maize roots"

[1]
DONG Y, CHEN R R, GRAHAM E B, YU B Q, BAO Y Y, LI X, YOU X W, FENG Y Z. Eco-evolutionary strategies for relieving carbon limitation under salt stress differ across microbial clades. Nature Communications, 2024, 15: 6013.

doi: 10.1038/s41467-024-50368-z pmid: 39019914
[2]
REZAPOUR S, NOURI A, ASADZADEH F, BARIN M, ERPUL G, JAGADAMMA S, QIN R J. Combining chemical and organic treatments enhances remediation performance and soil health in saline-sodic soils. Communications Earth & Environment, 2023, 4: 285.
[3]
HOPMANS J W, QURESHI A S, KISEKKA I, MUNNS R, GRATTAN S R, RENGASAMY P, BEN-GAL A, ASSOULINE S, JAVAUX M, MINHAS P S, et al. Chapter One-Critical knowledge gaps and research priorities in global soil salinity. Advances in Agronomy. Academic Press, 2021, 169: 1-191.
[4]
WANG Y Q, YANG Y Z, ZHAO D L, LI Z, SUI X N, ZHANG H, LIU J, LI Y Q, ZHANG C S, ZHENG Y F. Ensifer sp. GMS 14 enhances soybean salt tolerance for potential application in saline soil reclamation. Journal of Environmental Management, 2024, 349: 119488.
[5]
ZHANG G L, BAI J H, ZHAI Y J, JIA J, ZHAO Q Q, WANG W, HU X Y. Microbial diversity and functions in saline soils: A review from a biogeochemical perspective. Journal of Advanced Research, 2024, 59: 129-140.
[6]
LI Y B, GAO W L, WANG C X, GAO M. Distinct distribution patterns and functional potentials of rare and abundant microorganisms between plastisphere and soils. Science of the Total Environment, 2023, 873: 162413.
[7]
LI D P, QI Z H, GUO J Y, WANG T, LI X Y, HOU N. Study on the screening of high-efficiency salt and alkali-tolerant microbial agents and their roles and mechanisms in enhancing saline-alkaline soil remediation. Journal of Cleaner Production, 2025, 519: 145992.
[8]
LI H, LA S K, ZHANG X, GAO L H, TIAN Y Q. Salt-induced recruitment of specific root-associated bacterial consortium capable of enhancing plant adaptability to salt stress. The ISME Journal, 2021, 15(10): 2865-2882.
[9]
ZHENG Y F, CAO X W, ZHOU Y N, MA S Q, WANG Y Q, LI Z, ZHAO D L, YANG Y Z, ZHANG H, MENG C, et al. Purines enrich root-associated Pseudomonas and improve wild soybean growth under salt stress. Nature Communications, 2024, 15: 3520.
[10]
邵嘉朱, 吕雯, 廖鑫琳, 袁歆瑜, 宋振, 蒋冬花. 大豆根际促生菌的分离、鉴定及其耐盐促生作用. 中国农业科学, 2024, 57(21): 4248-4263. doi:10.3864/j.issn.0578-1752.2024.21.007.
SHAO J Z, W, LIAO X L, YUAN X Y, SONG Z, JIANG D H. Isolation and identification of soybean rhizosphere growth-promoting bacteria and their salt tolerance and growth-promoting effects. Scientia Agricultura Sinica, 2024, 57(21): 4248-4263. doi:10.3864/j.issn.0578-1752.2024.21.007. (in Chinese)
[11]
CHEN L, LIU Y P, WU G W, ZHANG N, SHEN Q R, ZHANG R F. Beneficial rhizobacterium Bacillus amyloliquefaciens SQR9 induces plant salt tolerance through spermidine production. Molecular Plant-Microbe Interactions, 2017, 30(5): 423-432.
[12]
MISHRA P, MISHRA J, ARORA N K. Plant growth promoting bacteria for combating salinity stress in plants-Recent developments and prospects: A review. Microbiological Research, 2021, 252: 126861.
[13]
CHEN L, ZHOU G X, FENG B, WANG C, LUO Y, LI F, SHEN C C, MA D H, ZHANG C Z, ZHANG J B. Saline-alkali land reclamation boosts topsoil carbon storage by preferentially accumulating plant-derived carbon. Science Bulletin, 2024, 69(18): 2948-2958.
[14]
姜焕焕, 王通, 陈娜, 禹山林, 迟晓元, 王冕, 祁佩时. 根际促生菌提高植物抗盐碱性的研究进展. 生物技术通报, 2019, 35(10): 189-197.

doi: 10.13560/j.cnki.biotech.bull.1985.2018-0860
JIANG H H, WANG T, CHEN N, YU S L, CHI X Y, WANG M, QI P S. Research progress in PGPR improving plant's resistance to salt and alkali. Biotechnology Bulletin, 2019, 35(10): 189-197. (in Chinese)
[15]
RAVINDRAN C, VARATHARAJAN G R, RAJU R, VASUDEVAN L, ANANTHA S R. Infection and pathogenecity of Myroides odoratimimus (NIOCR-12) isolated from the gut of grey mullet (Mugil cephalus (Linnaeus, 1758)). Microbial Pathogenesis, 2015, 88: 22-28.
[16]
范瑞娟, 刘雅琴, 张琇. 嗜盐碱高环PAHs降解菌的分离及其降解特性研究. 农业环境科学学报, 2019, 38(6): 1280-1287.
FAN R J, LIU Y Q, ZHANG X. Isolation and degradation characteristics of haloalkaliphilic high molecular-weight polycyclic aromatic hydrocarbon-degrading bacteria. Journal of Agro-Environment Science, 2019, 38(6): 1280-1287. (in Chinese)
[17]
东秀珠, 蔡妙英. 常见细菌系统鉴定手册. 北京: 科学出版社, 2001: 140-176.
DONG X Z, CAI M Y. Handbook of Identification of Common Bacterial Systems. Beijing: Science Press, 2001: 140-176. (in Chinese)
[18]
宁楚涵, 李文彬, 张晨, 刘润进. 定殖植物根内和根围放线菌的分离鉴定及其体外抑菌促生效应. 微生物学报, 2019, 59(10): 2024-2037.
NING C H, LI W B, ZHANG C, LIU R J. Isolation and identification of antagonizing and growthpromoting Actinobacteria colonized in plant roots and rhizosphere. Acta Microbiologica Sinica, 2019, 59(10): 2024-2037. (in Chinese)
[19]
SCHWYN B, NEILANDS J B. Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry, 1987, 160(1): 47-56.

doi: 10.1016/0003-2697(87)90612-9 pmid: 2952030
[20]
张秀娟, 安丽芸, 刘勇, 刘菊, 李君剑. 基于梯度稀释法分析细菌多样性对土壤碳代谢的影响. 生态学报, 2020, 40(3): 768-777.
ZHANG X J, AN L Y, LIU Y, LIU J, LI J J. Effects of soil bacterial diversity on soil carbon metabolism based on gradient dilution method. Acta Ecologica Sinica, 2020, 40(3): 768-777. (in Chinese)
[21]
张缘杨, 宋德伟, 田雷, 马强, 李杨, 任婷婷, 陈芊如, 刘洋, 刘鑫, 公衍军, 等. 壳寡糖对干旱胁迫下烟草种子萌发及幼苗生长的影响. 特产研究, 2025: 1-10. https://doi.org/10.16720/j.cnki.tcyj.2025.130.
ZHANG Y Y, SONG D W, TIAN L, MA Q, LI Y, REN T T, CHEN Q R, LIU Y, LIU X, GONG Y J, et al. The effect of chitosan- oligosaccharide on tobacco seed germination and seedling growth under drought conditions. Special Wild Economic Animal and Plant Research, 2025: 1-10. https://doi.org/10.16720/j.cnki.tcyj.2025.130. (in Chinese)
[22]
ZHAO J, LIU H J, LI T T, LI Y P, WANG M Q, CI H T, LU Y W, ZHU C H, GAN L J, CHEN S G, et al. N4-acetylcytidine mRNA modification regulates photosynthesis in plants. New Phytologist, 2025, 247(5): 2098-2117.
[23]
LI T, DENG X P, WANG J J, ZHAO H, WANG L, QIAN K. Biodegradation of 3, 4-dichloroaniline by a novel Myroides odoratimimus strain LWD09 with moderate salinity tolerance. Water, Air, & Soil Pollution, 2012, 223(6): 3271-3279.
[24]
喻江, 王新珍, 王淳, 曹英雪, 于镇华. 一株耐盐碱柠檬酸杆菌在促进植物生长中的应用及其耐盐碱基因挖掘. 微生物学通报, 2024, 51(3): 864-879.
YU J, WANG X Z, WANG C, CAO Y X, YU Z H. A saline-alkali tolerant strain of Citrobacter: Application in promoting plant growth and mining of saline-alkali tolerance genes. Microbiology China, 2024, 51(3): 864-879. (in Chinese)
[25]
相凯文, 李丹丹, 郭自春, 任宗玲, 田慎重, 高磊, 彭新华, 蔡燕飞. 一株高产吲哚乙酸促生菌的筛选鉴定、条件优化、应用效果及其代谢途径. 微生物学通报, 2025, 52(6): 2599-2612.
XIANG K W, LI D D, GUO Z C, REN Z L, TIAN S Z, GAO L, PENG X H, CAI Y F. A high indole-3-acetic acid-producing bacterial strain with plant growth-promoting effect: Screening, identification, culture condition optimization, application, and genome-wide analysis. Microbiology China, 2025, 52(6): 2599-2612. (in Chinese)
[26]
卜凡, 韩思宁, 朱仁贵, 苑瑜瑾, 于玮玮, 谷医林, 王远宏. 一株耐盐碱多黏类芽孢杆菌TaRb44的分离鉴定和耐盐促生作用评价. 微生物学报, 2025, 65(4): 1498-1511.
BU F, HAN S N, ZHU R G, YUAN Y J, YU W W, GU Y L, WANG Y H. Isolation, identification, and plant growth-promoting effect evaluation of a saline-alkali-tolerant rhizobacterium Paenibacillus polymyxa TaRb44. Acta Microbiologica Sinica, 2025, 65(4): 1498-1511. (in Chinese)
[27]
金佳悦, 范忠玲, 郭利利, 李坤, 毕少杰, 王彦杰. 一株耐盐碱细菌肺炎克雷伯氏菌(Klebsiella pneumoniae)NP36的分离鉴定及全基因组分析. 微生物学通报, 2025, 52(4): 1447-1461.
JIN J Y, FAN Z L, GUO L L, LI K, BI S J, WANG Y J. Isolation, identification, and whole-genome analysis of a bacterium Klebsiella pneumoniae NP36 with saline-alkali tolerance. Microbiology China, 2025, 52(4): 1447-1461. (in Chinese)
[28]
ZHANG L Y, YUAN L, WEN Y C, ZHANG M L, HUANG S Y, WANG S Y, ZHAO Y Z, HAO X X, LI L J, GAO Q, et al. Maize functional requirements drive the selection of rhizobacteria under long-term fertilization practices. The New Phytologist, 2024, 242(3): 1275-1288.
[29]
WANG M K, ZHANG P, LI H S, DENG G S, KONG D L, KONG S F, WANG J J. Molecular-level carbon traits of fine roots: Unveiling adaptation and decomposition under flooded conditions. Biogeosciences, 2024, 21(11): 2691-2704.
[30]
WANG M K, KONG D L, MO X H, WANG Y H, YANG Q P, KARDOL P, VALVERDE-BARRANTES O J, SIMPSON M J, ZENG H, REICH P B, et al. Molecular-level carbon traits underlie the multidimensional fine root economics space. Nature Plants, 2024, 10(6): 901-909.

doi: 10.1038/s41477-024-01700-4 pmid: 38740944
[31]
CHEN H, WU W Q, DU K, YANG J, KANG X Y. CCT 39 transcription factor promotes chlorophyll biosynthesis and photosynthesis in poplar. Plant, Cell & Environment, 2025, 48(5): 3136-3150.
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