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Journal of Arid Land
Journal of Arid Land  2023, Vol. 15 Issue (11): 1405-1420    DOI: 10.1007/s40333-023-0071-y
Research article     
Plant growth-promoting properties and anti-fungal activity of endophytic bacterial strains isolated from Thymus altaicus and Salvia deserta in arid lands
ZHAO Mengqi1,2, SU Huan1,2, HUANG Yin2,3, Rashidin ABDUGHENI2, MA Jinbiao2, GAO Jiangtao4, GUO Fei1, LI Li2,*()
1College of Life Science and Technology, Xinjiang University, Urumqi 830046, China
2State Key Laboratory of Desert and Oasis Ecology, Key Laboratory of Ecological Safety and Sustainable Development 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
4Key Laboratory of Biopesticide and Chemical Biology of Ministry of Education, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou 350002, China
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Abstract  

Endophytes, as crucial components of plant microbial communities, significantly contribute to enhancing the absorption of nutrients such as nitrogen and phosphorus by their hosts, promote plant growth, and degrade pathogenic fungal mycelia. In this study, an experiment was conducted in August 2022 to explore the growth-promoting potential of endophytic bacterial strains isolated from two medical plant species, Thymus altaicus and Salvia deserta, using a series of screening media. Plant samples of Thymus altaicus and Salvia deserta were collected from Zhaosu County and Habahe County in Xinjiang Uygur Autonomous Region, China, in July 2021. Additionally, the inhibitory effects of endophytic bacterial strains on the four pathogenic fungi (Fusarium oxysporum, Fulvia fulva, Alternaria solani, and Valsa mali) were determined through the plate confrontation method. A total of 80 endophytic bacterial strains were isolated from Thymus altaicus, while a total of 60 endophytic bacterial strains were isolated from Salvia deserta. The endophytic bacterial strains from both Thymus altaicus and Salvia deserta exhibited plant growth-promoting properties. Specifically, the strains of Bacillus sp. TR002, Bacillus sp. TR005, Microbacterium sp. TSB5, and Rhodococcus sp. TR013 demonstrated strong cellulase-producing activity, siderophore-producing activity, phosphate solubilization activity, and nitrogen-fixing activity, respectively. Out of 140 endophytic bacterial strains isolated from Thymus altaicus and Salvia deserta, 104 strains displayed anti-fungal activity against Fulvia fulva, Alternaria solani, Fusarium oxysporum, and Valsa mali. Furthermore, the strains of Bacillus sp. TR005, Bacillus sp. TS003, and Bacillus sp. TSB7 exhibited robust inhibition rates against all the four pathogenic fungi. In conclusion, the endophytic bacterial strains from Thymus altaicus and Salvia deserta possess both plant growth-promoting and anti-fungal properties, making them promising candidates for future development as growth-promoting agents and biocontrol tools for plant diseases.

Key words： endophytic bacteria      Thymus altaicus      Salvia deserta      pathogenic fungi      plant growth-promoting properties      anti-fungal activity     
Received: 07 March 2023      Published: 30 November 2023
Corresponding Authors: * LI Li (E-mail: lili.bobo@outlook.com)
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ZHAO Mengqi
SU Huan
HUANG Yin
Rashidin ABDUGHENI
MA Jinbiao
GAO Jiangtao
GUO Fei
LI Li
Cite this article:

ZHAO Mengqi, SU Huan, HUANG Yin, Rashidin ABDUGHENI, MA Jinbiao, GAO Jiangtao, GUO Fei, LI Li. Plant growth-promoting properties and anti-fungal activity of endophytic bacterial strains isolated from Thymus altaicus and Salvia deserta in arid lands. Journal of Arid Land, 2023, 15(11): 1405-1420.

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http://jal.xjegi.com/10.1007/s40333-023-0071-y     OR     http://jal.xjegi.com/Y2023/V15/I11/1405

Phylum Order Family Genus Species Strain
Actinomycetota Micrococcales Micrococcaceae Micrococcus 2 3
Kocuria 1 1
Mycobacteriales Dietziaceae Dietzia 1 2
Corynebacteriaceae Corynebacterium 1 1
Actinobacteria Microbacteriales Microbacteriaceae Microbacterium 1 18
Mycobacteriales Nocardiaceae Rhodococcus 2 2
Micrococcales Micrococcaceae Arthrobacter 2 2
Pseudomonadota Enterobacterales Enterobacteriaceae Enterobacter 3 7
Klebsiella 1 9
Escherichia 1 1
Pseudomonadales Pseudomonadaceae Pseudomonas 2 3
Firmicutes Bacillales Bacillaceae Bacillus 9 91
Table 1 Distribution of endophytic bacterial strains isolated from Thymus altaicus and Salvia deserta
Fig. 1 Relative abundance of endophytic bacterial strains isolated from different tissues of Thymus altaicus and Salvia deserta at the genus level (a) and species level (b). L, leaf; R, root; S, stem.
Fig. 2 Venn distribution of endophytic species in Thymus altaicus and Salvia deserta. (a), distribution between Thymus altaicus and Salvia deserta; (b), distribution among different tissues of Thymus altaicus and Salvia deserta.
Medium no. Medium
name		 Medium component (g/L) Reference
1 PDA Potato: 200.0 g/L; glucose: 20.0 g/L; agar: 15.0 g/L. Liu et al. (2017)
2 ISP2 Glucose: 4.0 g/L; yeast extract: 4.0 g/L; malt extract: 10.0 g/L; agar: 15.0 g/L. Liu et al. (2017)
3 Milk medium D-mannitol: 10.0 g/L; yeast extract: 3.0 g/L; K2HPO4: 0.49 g/L; MgSO4·7H2O 0.2 g/L; skim milk: 50.0 g/L; agar: 15.0 g/L. Li et al. (2018)
4 CMC-Na medium CMC-Na: 20.0 g/L; Na2HPO4: 2.5 g/L; KH2PO4: 1.5 g/L; peptone: 2.5 g/L; agar: 15.0 g/L. Li et al. (2018)
5 Lipase medium Peptone: 10.0 g/L; NaCl: 5.0 g/L; CaCl2: 0.1 g/L; ferric citrate: 0.2 g/L; beef extract: 3.0 g/L; agar: 15.0 g/L. Li et al. (2018)
6 Dephosphori-zation medium Yeast extract: 0.5 g/L; glucose: 10.0 g/L; (NH4)2SO4: 0.5 g/L; MgSO4·7H2O: 0.1 g/L; KCl: 0.2 g/L; NaCl: 0.2 g/L; FeSO4·7H2O: 2.0 mg/L; MnSO4·H2O: 2.0 mg/L; Ca3(PO4)2: 5.0 g/L; bromophenol blue: 25.0 g/L; agar: 15.0 g/L. Liu et al. (2017)
7 Chitinase medium Chitin colloid: 4.5 g/L; anhydrous citric acid: 1.0 g/L; bromocresol purple: 150.0 mg/L; tween 20: 200.0 μL/L; MgSO4·7H2O: 0.3 g/L; (NH4)2SO4: 3.0 g/L; KH2PO4: 2.0 g/L; agar: 15.0 g/L. Agrawal and Kotasthane (2012)
8 CAS medium CAS: 0.0605 g/L; FeCl3·6H2O (10 mM HCL dissolved): 10.0 mL; HDTMA: 0.0728 g/L; K2HPO4: 0.3 g/L; NaCl: 0.5 g/L; PIPES: 30.4 g/L; NH4Cl: 1.0 g/L; Mannitol: 2.0 g/L; MgSO4·7H2O: 0.493 g/L; CaCl2: 0.011 g/L; MnSO4·H2O: 0.00117 g/L; H3BO3: 0.0014 g/L; CuSO4·5H2O: 0.04 mg/L; ZnSO4·7H2O: 0.0012 mg/L; Na2MoO4·2H2O: 0.001 g/L; Casamino acids (10%; weight/volume): 30.0 mL; Glucose: 2.0 g/L; Agar: 15.0 g/L. Liu et al. (2017)
9 Nitrogen fixation medium D-mannitol: 10.0 g/L; K2HPO4: 0.2 g/L; MgSO4·7H2O: 0.2 g/L; NaCl:
0.2 g/L; CaCO3: 5.0 g/L; CaSO4·2H2O: 0.2 g/L; Agar: 15.0 g/L.		 Liu et al. (2017)
Table 2 Composition of the media used in the current study
Activity Positive Negative
Strong Moderate Weak
Protease-producing 2.2≤E<2.8 1.6≤E<2.2 1.0<E<1.6 E≤1.0
Cellulase-producing 4.9≤E<7.1 2.8≤E<4.9 1.0<E<2.8 E≤1.0
Lipase-producing 3.1≤E<4.1 2.1≤E<3.1 1.0<E<2.1 E≤1.0
Phosphate solubilization 2.0≤E<2.5 1.5≤E<2.0 1.0<E<1.5 E≤1.0
Siderophore-producing 3.0≤E<4.0 2.0≤E<3.0 1.0<E<2.0 E≤1.0
Chitinase-producing E>1.0 E≤1.0
Nitrogen-fixing E>1.0 E≤1.0
Table 3 Criteria for determining different enzyme-producing activities of endophytic bacterial strains
Activity Positive Negative
Strong Moderate Weak Total Number PERC (%)
Number PERC (%) Number PERC (%) Number PERC
(%)		 Number PERC
(%)
Protease-producing 1 2.7 8 21.6 28 75.7 37 46.3 43 53.7
Cellulase-producing 14 26.4 22 41.5 17 32.1 53 66.3 27 33.7
Lipase-producing 2 5.3 10 26.3 26 68.4 38 47.5 42 52.5
Phosphate solubilization 3 18.8 6 37.5 7 43.7 16 20.0 64 80.0
Chitinase-producing - - - - - - 24 30.0 56 70.0
Siderophore-producing 7 16.3 17 39.5 19 44.2 43 53.8 37 46.2
Nitrogen-fixing - - - - - - 67 83.8 13 16.2
Table 4 Number and percentage of endophytic bacterial strains isolated from Thymus altaicus with different enzyme-producing activities reflecting plant growth-promoting properties
Activity Positive Negative
Strong Moderate Weak Total Number PERC (%)
Number PERC (%) Number PERC (%) Number PERC (%) Number PERC (%)
Protease-producing 3 8.6 2 5.7 30 85.7 35 58.3 25 41.7
Cellulase-producing 6 12.0 33 66.0 11 22.0 50 83.3 10 16.7
Lipase-producing 2 5.9 8 23.5 24 70.6 34 56.7 26 43.3
Phosphate solubilization 0 0.0 1 16.7 5 83.3 6 10.0 54 90.0
Chitinase-producing - - - - - - 8 13.3 52 86.7
Siderophore-producing 7 18.4 14 36.8 17 44.8 38 63.3 22 36.7
Nitrogen-fixing - - - - - - 45 75.0 15 25.0
Table 5 Number and percentage of endophytic bacterial strains isolated from Salvia deserta with different enzyme-producing activities reflecting plant growth-promoting properties
Pathogenic fungi Positive Negative
Strong Moderate Weak Total Number PERC (%)
Number PERC (%) Number PERC (%) Number PERC (%) Number PERC (%)
Fusarium oxysporum 17 50.0 13 38.2 4 11.8 34 42.5 46 57.5
Fulvia fulva 21 51.2 12 29.3 8 19.5 41 51.3 39 48.7
Alternaria solani 21 52.5 17 42.5 2 5.0 40 50.0 40 50.0
Valsa mali 11 26.2 21 50.0 10 23.8 42 52.5 38 47.5
Table 6 Number and percentage of endophytic bacterial strains isolated from Thymus altaicus showing anti-fungal activity against the four pathogenic fungi (Fusarium oxysporum, Fulvia fulva, Alternaria solani, and Valsa mali)
Pathogenic fungi Positive Negative
Strong Moderate Weak Total
Number PERC (%) Number PERC (%) Number PERC (%) Number PERC (%) Number PERC (%)
Fusarium oxysporum 14 50.0 14 50.0 0 0.0 28 46.7 32 53.3
Fulvia fulva 10 41.7 9 37.5 5 20.8 24 40.0 36 60.0
Alternaria solani 17 63.0 9 33.3 1 3.7 27 45.0 33 55.0
Valsa mali 3 10.0 13 43.3 14 46.7 30 50.0 30 50.0
Table 7 Number and percentage of endophytic bacterial strains isolated from Salvia deserta showing anti-fungal activity against the four pathogenic fungi (Fusarium oxysporum, Fulvia fulva, Alternaria solani, and Valsa mali)
Strain Inhibition rate (%)
Fulvia fulva Alternaria solani Fusarium oxysporum Valsa mali
Bacillus sp. TL001 54.6 53.2 65.5 68.0
Micrococcus sp. TL002 54.7 67.5 46.9 -
Enterobacter sp. TL003 - 65.0 - -
Bacillus sp. TL004 - 50.7 - 63.3
Bacillus sp. TL006 65.0 73.0 70.0 68.7
Microbacterium sp. TR001 - - - -
Bacillus sp. TR002 - - - 45.6
Microbacterium sp. TR003 - - - -
Microbacterium sp. TR004 - - - -
Bacillus sp. TR005 67.0 65.4 58.8 50.8
Rhodococcus sp. TR007 - 56.0 - -
Microbacterium sp. TR009 - - - -
Rhodococcus sp. TR013 - - - -
Microbacterium sp. TR015 - - - 32.7
Microbacterium sp. TR016 - - - 38.2
Bacillus sp. TS001 69.3 58.5 57.0 48.1
Bacillus sp. TS002 66.2 55.7 60.1 56.2
Bacillus sp. TS003 67.5 73.9 63.0 61.4
Enterobacter sp. TS004 61.0 65.0 60.3 -
Microbacterium sp. TS005 - - - -
Bacillus sp. TS006 70.3 59.0 53.3 68.7
Microbacterium sp. TS009 - - - -
Bacillus sp. TS011 71.3 48.9 48.1 65.0
Microbacterium sp. TS012 - - - -
Microbacterium sp. TS013 - - - -
Bacillus sp. TS014 - - - 61.2
Microbacterium sp. TS015 - - - -
Bacillus sp. TS016 - - - 54.6
Bacillus sp. TS018 - - - 52.1
Klebsiella sp. TS B3 - 51.5 40.6 -
Microbacterium sp. TS B5 - - - -
Klebsiella sp. TS B6 - - - -
Bacillus sp. TS B7 65.2 67.7 60.9 64.9
Enterobacter sp. TSB018 - - - -
Klebsiella sp. TSB019 - - - -
Klebsiella sp. TSB020 - - - -
Klebsiella sp. TSB022 - - 44.3 -
Enterobacter sp. TSB023 - - - 31.9
Escherichia sp. TSB024 63.0 - - -
Bacillus sp. TSB025 56.3 60.1 66.8 -
Enterobacter sp. TSB031 43.0 51.0 68.0 59.5
Klebsiella sp. TSB034 - - - -
Bacillus sp. TSB035 69.2 70.0 65.2 64.3
Bacillus sp. TSB036 59.0 70.0 61.9 65.7
Microbacterium sp. TSB037 53.1 - - -
Bacillus sp. TR B1 69.8 74.2 66.1 51.2
Bacillus sp. TR B2 65.2 67.1 58.2 35.8
Bacillus sp. TR B3 68.3 64.0 62.2 56.2
Klebsiella sp. TR B6 - - - -
Klebsiella sp. TR B7 40.5 48.2 - -
Bacillus sp. TR B8 - - - 45.6
Microbacterium sp. TR B10 51.1 - - 48.8
Microbacterium sp. TR B11 - - - 48.8
Microbacterium sp. TR B14 44.4 44.5 41.2 -
Bacillus sp. TRB016 51.7 - - 45.2
Bacillus sp. TRB020 62.3 58.0 55.1 71.7
Bacillus sp. TRB021 70.0 62.9 65.3 53.7
Pseudomonas sp. TRB022 - 45.7 31.3 -
Klebsiella sp. TRB023 57.2 53.4 55.9 53.4
Microbacterium sp. TRB025 - - - -
Bacillus sp. TRB027 66.8 67.9 47.5 -
Bacillus sp. TRB028 40.2 47.1 - -
Micrococcus sp. TL B1 55.3 46.5 - -
Bacillus sp. TL B2 56.5 53.8 57.6 47.9
Bacillus sp. TL B3 61.8 62.8 65.7 59.8
Bacillus sp. TL B4 43.8 - 47.1 -
Bacillus sp. TL B6 - - - 37.9
Bacillus sp. TL B7 - - - 43.5
Bacillus sp. TL B9 - - - 50.4
Bacillus sp. TL B10 - - - 31.9
Bacillus sp. TL B11 - - - -
Bacillus sp. TL B13 - - - 45.2
Bacillus sp. TL B14 41.3 - - 39.0
Bacillus sp. TL B15 70.4 71.6 62.2 -
Bacillus sp. TL B16 66.5 71.2 59.2 41.7
Bacillus sp. TLB011 39.3 42.9 - 40.5
Bacillus sp. TLB013 41.1 46.8 - -
Bacillus sp. TLB014 68.3 74.8 62.6 -
Bacillus sp. TLB015 55.2 77.0 62.4 52.5
Bacillus sp. TLB017 52.5 69.8 57.6 52.9
Bacillus sp. SR001 - - - 41.3
Bacillus sp. SR002 - - - -
Bacillus sp. SR003 - - - 40.3
Bacillus sp. SR004 - - - 41.0
Bacillus sp. SR006 55.3 53.4 60.3 38.2
Arthrobacter sp. SR009 - - - -
Pseudomonas sp. SR011 - - - -
Bacillus sp. SR012 59.4 69.6 61.9 -
Microbacterium sp. SR014 - - - -
Dietzia sp. SR015 - - - -
Enterobacter sp. SR017 - - - -
Bacillus sp. SR020 44.8 59.1 57.6 -
Pseudomonas sp. SR023 - - - -
Bacillus sp. SS003 45.2 63.6 58.3 56.9
Bacillus sp. SS005 61.6 65.2 59.2 -
Arthrobacter sp. SS006 61.7 66 58.5 58.5
Bacillus sp. SS007 - - - -
Kocuria sp. SS008 - - - 56.9
Bacillus sp. SL001 62.5 57.3 62.0 46.6
Bacillus sp. SL001a 56.4 54.4 62.6 43.6
Bacillus sp. SL001b 61.9 58.1 60.8 42.5
Bacillus sp. SL002 51.3 - - -
Bacillus sp. SL003 - - - -
Bacillus sp. SL004 - 39.0 - -
Bacillus sp. SL005 - - - 36.3
Bacillus sp. SL006 64.4 70.0 61.2 66.8
Bacillus sp. SL007 67.3 70.3 71.0 67.2
Bacillus sp. SL008 56.5 48.1 58.8 63.3
Bacillus sp. SL009 62.9 63.0 53.0 51.7
Bacillus sp. SL011 - - - 47.5
Micrococcus sp. SL012 - - - -
Bacillus sp. SR B1 - - - 45.9
Dietzia sp. SR B2 - 51.5 - -
Bacillus sp. SRB023 - - - 36.7
Bacillus sp. SRB025 - - - 40.6
Bacillus sp. SRB026 55.3 48.4 66.9 45.2
Enterobacter sp. SRB027 - - 55.5 -
Bacillus sp. SRB028 - - - -
Bacillus sp. SRB032 - - - -
Bacillus sp. SRB034 - 74.8 63.2 -
Bacillus sp. SS B1 - - - -
Bacillus sp. SS B3 30.7 - - 41.0
Bacillus sp. SS B4 30.7 70.9 63.0 51.6
Bacillus sp. SSB012 35.3 66.1 58.1 54.8
Bacillus sp. SSB013 - 61.6 67.2 -
Bacillus sp. SSB014 - - - -
Bacillus sp. SSB015 54.0 70.3 64.1 57.1
Bacillus sp. SSB016 55.3 62.2 53.0 44.0
Bacillus sp. SSB019 63.1 68.6 64.3 49.0
Bacillus sp. SSB020 - 47.6 53.6 32.0
Corynebacterium sp. SL B1 63.1 66.1 53.1 -
Bacillus sp. SL B2 66.2 66.4 63.8 47.0
Bacillus sp. SL B6 44.1 - - 37.8
Bacillus sp. SLB010 - - 59.2 -
Bacillus sp. SLB011 - - - -
Bacillus sp. SLB013 - - 58.5 -
Bacillus sp. SLB015 - 68.6 50.7 -
Bacillus sp. SLB016 - - - -
Bacillus sp. SLB017 - - - -
Bacillus sp. SLB018 - - - 33.6
Table S1 Inhibition rates of tested endophytic bacterial strains isolated from Thymus altaicus and Salvia deserta against the four pathogenic fungi (Fulvia fulva, Alternaria solani, Fusarium oxysporum, and Valsa mali)
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