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Journal of Arid Land  2021, Vol. 13 Issue (8): 790-800    DOI: 10.1007/s40333-021-0016-2
Diversity of cultivable endophytic bacteria associated with halophytes in Xinjiang of China and their plant beneficial traits
LI Li1, GAO Lei1,2, LIU Yonghong1, FANG Baozhu1, HUANG Yin1, Osama A A MOHAMAD1, Dilfuza EGAMBERDIEVA3, LI Wenjun1,4,*(), MA Jinbiao1,*()
1 State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
2 University of Chinese Academy of Sciences, Beijing 100049, China
3 Faculty of Biology, National University of Uzbekistan, Tashkent 100174, Uzbekistan
4 State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, Guangzhou 510275, China
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Endophytic bacteria from halophytes have a wide range of application prospects in various fields, such as plant growth-promoting, biocontrol activity and stress resistance. The current study aimed to identify cultivable endophytic bacteria associated with halophytes grown in the salt-affected soil in Xinjiang Uygur Autonomous Region, China and to evaluate their plant beneficial traits and enzyme-producing activity. Endophytic bacteria were isolated from Reaumuria soongorica (PalL Maxim.), Artemisia carvifolia (Buch.-Ham. ex Roxb. Hort. Beng.), Peganum harmala L. and Suaeda dendroides (C. A. Mey. Moq.) by using the cultural-dependent method. Then we classified these bacteria based on the difference between their sequences of 16S rRNA (16S ribosomal RNA) gene. Results showed that the isolated bacteria from R. soongorica belonged to the genera Brucella, Bacillus and Variovorax. The bacteria from A. carvifolia belonged to the genera Micromonospora and Brucella. The bacteria from P. harmala belonged to the genera Paramesorhizobium, Bacillus and Peribacillus. The bacteria from S. dendroides belonged to the genus Bacillus. Notably, the genus Bacillus was detected in the three above plants, indicating that Bacillus is a common taxon of endophytic bacteria in halophytes. And, our results found that about 37.50% of the tested strains showed strong protease-producing activity, 6.25% of the tested strains showed strong cellulase-producing activity and 12.50% of the tested strains showed moderate lipase-producing activity. Besides, all isolated strains were positive for IAA (3-Indoleacetic acid) production, 31.25% of isolated strains exhibited a moderate phosphate solubilization activity and 50.00% of isolated strains exhibited a weak siderophore production activity. Our findings suggest that halophytes are valuable resources for identifying microbes with the ability to increase host plant growth and health in salt-affected soils.

Key wordsendophytes      environmental microbiology      halophytes      biodiversity      plant beneficial properties     
Received: 25 April 2021      Published: 10 August 2021
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LI Li, GAO Lei, LIU Yonghong, FANG Baozhu, HUANG Yin, Osama A A MOHAMAD, Dilfuza EGAMBERDIEVA, LI Wenjun, MA Jinbiao. Diversity of cultivable endophytic bacteria associated with halophytes in Xinjiang of China and their plant beneficial traits. Journal of Arid Land, 2021, 13(8): 790-800.

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Fig. 1 (a), percentage of isolated strains at the genus level; (b), Venn diagram of endophytic bacteria from four halophytes at the species level. P1, R. soongorica (Tamaricaceae); P2, A. carvifolia (Asteraceae); P3, P. harmala (Nitrariaceae); P4, S. dendroides (Amaranhaceae). The abbreviations are the same in the following figures and tables. The numbers in the Venn diagram represent the number of endophytic bacterial species.
Isolated strain Species with the highest similarity in the EzBioCloud database
Strain Size (bp) Accession number Top-hit taxon Identity (%) Accession number
P1.1 1489 MW228433 Bacillus halotolerans 99.45 LPVF01000003
P1.2 1488 MW228434 Bacillus atrophaeus 99.38 AB021181
P1.3 1417 MW228435 Brucella endophytica 98.35 KP721485
P1.4 1476 MW228436 Variovorax paradoxus 99.38 BCUT01000013
P1.5 1427 MW228437 Brucella endophytica 98.43 KP721485
P2.1 1450 MW228438 Micromonospora citrea 99.09 FMHZ01000002
P2.2 1417 MW228439 Brucella endophytica 98.71 KP721485
P2.3 1421 MW228440 Brucella endophytica 99.43 KP721485
P3.1 1488 MW228441 Bacillus filamentosus 100.00 KF265351
P3.2 1427 MW228442 Phyllobacterium phragmitis 98.36 PVBR01000053
P3.3 1424 MW228443 Phyllobacterium phragmitis 98.00 PVBR01000053
P3.4 1486 MW228444 Brevibacterium frigoritolerans 99.25 AM747813
P3.5 1426 MW228445 Phyllobacterium phragmitis 98.50 PVBR01000053
P4.1 1484 MW228446 Bacillus filamentosus 99.57 KF265351
P4.2 1483 MW228447 Bacillus atrophaeus 99.39 AB021181
P4.3 1485 MW228448 Bacillus atrophaeus 99.52 AB021181
Table 1 Sequence similarities of isolated endophytic bacterial 16S rRNA gene with sequences registered in the EzBioCloud database
Fig. 2 Neighbor-joining phylogenetic tree based on 16S rRNA gene sequences of endophytic bacteria
Isolated strain Enzyme-producing activity Plant growth-promoting traits
Proteaseb Cellulaseb Lipaseb IAAa Phosphate solubilizationb Siderophoreb
P1.1 +++ +++ + + + -
P1.2 +++ - ++ + + +
P1.3 - + - + - +
P1.4 - ++ - + ++ +
P1.5 - ++ - + - -
P2.1 ++ + - + - -
P2.2 ++ ++ - + + -
P2.3 ++ + - + ++ +
P3.1 - + - + ++ -
P3.2 ++ ++ - + ++ +
P3.3 +++ - - + + +
P3.4 +++ - - + + +
P3.5 - ++ - + - +
P4.1 - + - + - -
P4.2 +++ - - + ++ -
P4.3 +++ - ++ ++ + -
Table 2 Plant beneficial traits of endophytic bacterial strains associated with four halophytes
Fig. 3 Proportion of strains with different enzyme-producing activities (a-c) and plant growth-promoting traits (d-f)
[1]   Afzal I, Shinwari Z K, Sikandar S, et al. 2019. Plant beneficial endophytic bacteria: mechanisms, diversity, host range and genetic determinants. Microbiological Research, 221:36-49.
[2]   Amaresan N, Jayakumar V, Kumar K, et al. 2012. Isolation and characterization of plant growth promoting endophytic bacteria and their effect on tomato (Lycopersicon esculentum) and chilli (Capsicum annuum) seedling growth. Annals of Microbiology, 62(2):805-810.
[3]   Carter G T, Nietsche J A, Williams D R, et al. 1990. Citreamicins, novel antibiotics fromMicromonospora citrea: isolation, characterization, and structure determination. Journal of Antibiotics, 43(5):504-512.
[4]   Chen L, Dodd I C, Theobald J C, et al. 2013. The rhizobacteriumVariovorax paradoxus 5C-2, containing ACC deaminase, promotes growth and development ofArabidopsis thaliana via an ethylene-dependent pathway. Journal of Experimental Botany, 64(6):1565-1573.
[5]   Farahat M. 2020. Alleviation of salinity stress in wheat by ACC deaminase-producingBacillus aryabhattai EWR29 with multifarious plant growth-promoting attributes. Plant Archives, 20(1):417-429.
[6]   Fouda A, Eid A M, Elsaied A, et al. 2021. Plant growth-promoting endophytic bacterial community inhabiting the leaves ofPulicaria incisa (Lam.) DC inherent to arid regions. Plants, 10(1):76.
[7]   Gouda S, Das G, Sen S K, et al. 2016. Endophytes: a treasure house of bioactive compounds of medicinal importance. Frontiers in Microbiology, 7:1538.
[8]   Huang J F, Wang R H, Zhao Z Y, et al. 2006. Effects of climate change on soil salinization in Xinjiang oasis, China. In: Proceedings of the International Specialty Conference on Science and Technology for Desertification Control. Beijing, China, Agricultural University,306-313.
[9]   Hu M F, Tian C Y, Zhao Z Y, et al. 2012. Salinization causes and research progress of technologies improving saline-alkali soil in Xinjiang. Journal of Northwest A & F University, 40(10):111-117. (in Chinese)
[10]   Jiang H, Egamberdie V D, Panosyan H H, et al. 2020. Onshore soil microbes and endophytes respond differently to geochemical and mineralogical changes in the Aral Sea. Science of the Total Environment, 765:142675.
[11]   Jiménez-Gómez A, García-Estévez I, Escribano-Bailón M T, et al. 2021. Bacterial fertilizers based onRhizobium laguerreae andBacillus halotolerans enhanceCichorium endivia L. phenolic compound and mineral contents and plant development. Foods, 10(2):424.
[12]   Khan M A, Ozturk M, Gul B, et al. 2016. Halophytes for Food Security in Dry Lands(1st ed.ed.). Oxford: Elsevier Science Publishing Co. Inc.,49-66.
[13]   Khan M A, Asaf S, Khan A L, et al. 2020. Plant growth-promoting endophytic bacteria augment growth and salinity tolerance in rice plants. Plant Biology, 22(5):850-862.
[14]   Khare E, Mishra J, Arora N K. 2018. Multifaceted interactions between endophytes and plant: developments and prospects. Frontiers in Microbiology, 9:2732.
[15]   Lei Y J, Xia Z F, Luo X X, et al. 2020. Actinokineospora pegani sp. nov., an endophytic actinomycete isolated from the surface-sterilized root ofPeganum harmala L. International Journal of Systematic and Evolutionary Microbiology, 70(7):4358-4363.
[16]   Li H, Wang X F, Gao Y Q. 2004. Analysis and assessment of land desertification in Xinjiang based on RS and GIS. Journal of Geographical Sciences, 14:159-116.
[17]   Li L, Li Y Q, Jiang Z, et al. 2016. Ochrobactrum endophyticum sp. nov., isolated from roots ofGlycyrrhiza uralensis. Archives of Microbiology, 198(2):171-179.
[18]   Liang L X, Sun Q W, Hui N, et al. 2019. Phyllobacterium phragmitis sp. nov., an endophytic bacterium isolated fromPhragmites australis rhizome in Kumtag Desert. Antonie van Leeuwenhoek, 112(5):661-668.
[19]   Liu Y H, Guo J W, Li L, et al. 2017. Endophytic bacteria associated with endangered plantFerula sinkiangensis K. M. Shen in an arid land: diversity and plant growth-promoting traits. Journal of Arid Land, 9(3):432-445.
[20]   Mesa J, Mateos-Naranjo E, Caviedes M A, et al. 2015. Endophytic cultivable bacteria of the metal bioaccumulatorSpartina maritima improve plant growth but not metal uptake in polluted marshes soils. Frontiers in Microbiology, 6:1450.
[21]   Mishra A, Gond S K, Kumar A, et al. 2012. Sourcing the fungal endophytes:a beneficial transaction of biodiversity, bioactive natural products, plant protection and nanotechnology. In: Satyanarayana T, Johri B, Anil Prakash. Microorganisms in Sustainable Agriculture and Biotechnology. Dordrecht: Springer,581-612.
[22]   Mohamad O A, Li L, Ma J B, et al. 2018. Evaluation of the antimicrobial activity of endophytic bacterial populations from Chinese traditional medicinal plantLicorice and characterization of the bioactive secondary metabolites produced by Bacillus atrophaeus against Verticillium dahliae. Frontiers in Microbiology, 9:924-924.
[23]   Nakbanpote W, Panitlurtumpai N, Sangdee A, et al. 2014. Salt-tolerant and plant growth-promoting bacteria isolated from Zn/Cd contaminated soil: identification and effect on rice under saline conditions. Journal of Plant Interactions, 9(1):379-387.
[24]   Rajivgandhi G, Thillaichidambaram M, Muthuchamy M, et al. 2018. Antibacterial and anticancer potential of marine endophytic actinomycetesStreptomyces coeruleorubidus Grg 4 (Ky457708) compound against colistin resistant uropathogens and A549 lung cancer cells. Microbial Pathogenesis, 125:325-335.
[25]   Ramachandran G, Rajivgandhi G, Maruthupandy M, et al. 2019. Extraction and partial purification of secondary metabolites from endophytic actinomycetes of marine green algaeCaulerpa racemosa against multi drug resistant uropathogens. Biocatalysis and Agricultural Biotechnology, 17:750-757.
[26]   Sgroy V, Cassán F, Masciarelli O, et al. 2009. Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyteProsopis strombulifera. Applied Microbiology and Biotechnology, 85(2):371-378.
[27]   Shamsutdinov N Z, Shamsutdinova E Z, Orlovsky N S, et al. 2017. Halophytes: Ecological features, global resources, and outlook for multipurpose use. Herald of the Russian Academy of Sciences, 87(1):1-11.
[28]   Simarmata R, Widowati T, Dewi T K, et al. 2020. Isolation, screening and identification of plant growth-promoting endophytic bacteria from Theobroma cacao. Journal of Biology & Biology Education, 12(2):155-156.
[29]   Sonalkar V V, Mawlankar R, Venkata Ramana V, et al. 2015. Bacillus filamentosus sp. nov., isolated from sediment sample. Antonie van Leeuwenhoek, 107(2):433-441.
[30]   Taulé C, Vaz-Jauri P, Battistoni F. 2021. Insights into the early stages of plant-endophytic bacteria interaction. World Journal of Microbiology and Biotechnology, 37(1):13.
[31]   Teng S S, Liu Y P, Zhao L. 2010. Isolation, identification and characterization of ACC deaminase-containing endophytic bacteria from halophyteSuaeda salsa. Acta Microbiologica Sinica, 50(11):1503-1509. (in Chinese)
[32]   Tosi M, Gaiero J, Linton N, et al. 2021. Bacterial endophytes:diversity, functional importance, and potential for manipulation. In: Gupta V V S R, Sharma A K. Rhizosphere Biology:Interactions between Microbes and Plants. Rhizosphere Biology. Singapore: Springer,1-49.
[33]   Unnisa S A, Rasool A, Mir M I, et al. 2021. Plant growth promoting and antifungal asset of Indigenous rhizobacteria secluded from saffron (Crocus sativus L.) rhizosphere. Microbial Pathogenesis, 150:104734.
[34]   Wang G J. 2017. Studies on the construction and nutritional relationship ofCycas panzhihuaensis L. Zhou et S. Y. Yang mycorrhiza system. MSc Thesis. Kunmin: Southwest Forestry University. (in Chinese)
[35]   Wani Z A, Ashraf N, Mohiuddin T, et al. 2015. Plant-endophyte symbiosis, an ecological perspective. Applied Microbiology and Biotechnology, 99(7):2955-2965.
[36]   Yahaghi Z, Shirvani M, Nourbakhsh F, et al. 2019. Uptake and effects of lead and zinc on alfalfa (Medicago sativa L.) seed germination and seedling growth: Role of plant growth promoting bacteria. South African Journal of Botany, 124:573-582.
[37]   Zhao S, Zhou N, Wang L, et al. 2013. Halophyte-endophyte coupling: a promising bioremediation system for oil-contaminated soil in Northwest China. Environmental Science & Technology 47(21):11938-11939.
[38]   Zhao S, Zhou N, Zhao Z Y, et al. 2016a. Estimation of endophytic bacterial diversity in root of halophytes in Northern Xinjiang by high throughput sequencing. Acta microbiologica Sinica, 56(10):1583-1594. (in Chinese)
[39]   Zhao S, Zhou N, Zhao Z Y, et al. 2016b. High-throughput sequencing analysis of the endophytic bacterial diversity and dynamics in roots of the halophyteSalicornia europaea. Current Microbiology, 72(5):557-562.
[40]   Zhao S, Zhou N, Zhao Z Y, et al. 2016c. Isolation of endophytic plant growth-promoting bacteria associated with the halophyteSalicornia europaea and evaluation of their promoting activity under salt stress. Current Microbiology, 73(4):574-581.
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