Advertisement

3 Biotech

, 9:144 | Cite as

Diversity, community distribution and growth promotion activities of endophytes associated with halophyte Lycium ruthenicum Murr

  • Yong-Hong Liu
  • Yong-Yang Wei
  • Osama Abdalla Abdelshafy Mohamad
  • Nimaichand Salam
  • Yong-guang Zhang
  • Jian-Wei Guo
  • Li Li
  • Dilfuza Egamberdieva
  • Wen-Jun LiEmail author
Original Article

Abstract

The purpose of this study was to investigate the composition, diversity, distribution, and growth promotion activity of endophytic bacteria isolated from L. ruthenicum Murr. Consequently, a total of 109 endophytic bacteria affiliated to 3 phyla, 12 orders and 36 genera were isolated using nine different selective media, from which, Actinobacteria was the dominant taxon containing seven orders at the phylum level; Micrococcales showed the highest diversity containing 12 genera at the family level. Based on PAST and SPSS analysis, species diversity and abundance were mostly isolated from nutritious soil condition (22 genera) and root tissue (27 genera). Furthermore, growth phase showed significant effect on the endophytic bacteria community (28 genera at dormancy and 17 genera at fluorescence stage). With regard to ex situ plant growth-promoting activities, Streptomyces dominated and exhibited broad ability in terms of their potential to grow on nitrogen-free media, synthesize cellulase and lipase enzymes. Characterization of potential plant-beneficial traits indicate that endophytic bacteria exhibited a number of positive activities, including potential diazotrophy (n = 66), phosphate-solubilizing (n = 6), production of lipase (n = 21) and cellulose (n = 35). Two strains, representing Bacillus sp. EGI 63071 and EGI 63106, were found to be effective in promoting the growth of Triticum aestivum (wheat: Xindong No.18) seedling under salt stress conditions.

Keywords

Environmental microbiology Endophytes Diversity Halophyte Lycium ruthenicum Growth promotion 

Notes

Funding

This research was supported by Xinjiang Uygur Autonomous Region regional coordinated innovation project (Shanghai cooperation organization science and technology partnership program) (No. 2017E01031) and China Biodiversity Observation Networks (Sino BON). This research was supported by Chinese Academy of Sciences President’s International Fellowship Initiative (Grant No. 2018VBA002S) for Dilfuza Egamberdieva.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

13205_2019_1678_MOESM1_ESM.docx (31 kb)
Supplementary material 1 (DOCX 30 KB)

References

  1. Abeer H, Abd_Allah EF, Alqarawi AA et al (2016) The interaction between arbuscular mycorrhizal fungi and endophytic bacteria enhances plant growth of Acacia gerrardii under salt stress. Front Microbiol.  https://doi.org/10.3389/fmicb.2016.01089 Google Scholar
  2. Baath E, Anderson TH (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA–based techniques. Soil Biol Biochem 35:955–963Google Scholar
  3. Bordiec S, Paquis S, Lacroix H et al (2011) Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot 62(2):595–603Google Scholar
  4. Chater KF (1993) Genetics of differentiation in Streptomyces. Annu Rev Microbiol 47(1):685–713Google Scholar
  5. Chen HK, Pu LK, Cao JM (2008) Current research state and exploitation of lycium ruthenicum murr. Heilongjiang Agric Sci 5:155–157 (In Chinese)Google Scholar
  6. Cui D, Liu B (2010) The halophytes resource of Xinjiang and the suggestions about its exploitation and utilization. J Arid Land Resour Environ 24(7):171–175 (In Chinese)Google Scholar
  7. Damodharan K, Palaniyandi SA, Le B et al (2018) Streptomyces sp. strain SK68, isolated from peanut rhizosphere, promotes growth and alleviates salt stress in tomato (Solanum lycopersicum cv. Micro-Tom). J Microbiol (Seoul Korea) 56(10):753–759Google Scholar
  8. Egamberdieva D, Berg G, Lindström K et al (2013) Alleviation of salt stress of symbiotic Galega officinalis L. (goat’s rue) by co-inoculation of Rhizobium with root colonizing Pseudomonas. Plant Soil 369:453–465Google Scholar
  9. Egamberdieva D, Wirth SJ, Shurigin VV (2017) Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Front Microbiol 8:1887.  https://doi.org/10.3389/fmicb.2017.01887 Google Scholar
  10. Faeth SH, Hammon KE (1997) Fungal endophytes in oak trees: long-term patterns of abundance and as- sociations with leafminers. Ecology 78:810–819Google Scholar
  11. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631Google Scholar
  12. Gao Z, Zhang B, Liu H et al (2017) Identification of endophytic Bacillus velezensis ZSY-1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis cinerea. Biol Control 105:27–39.  https://doi.org/10.1016/j.biocontrol.2016.11.007 Google Scholar
  13. Germida JJ, Siciliano SD, Jrde F et al (1998) Diversity of root-associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum. aestivum L.). FEMS Microbiol Ecol 26(1):43–50Google Scholar
  14. Gundel PE, Maseda PH, Ghersa CM et al (2010) Effects of the Neotyphodium endophyte fungus on dormancy and germination rate of Lolium multiflorum seeds. Austral Ecol 31(6):767–775Google Scholar
  15. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: palaeontological statistics software package of education and data analysis. Palaeontol Electron 4:1–9Google Scholar
  16. Hao Y, Xie Y, Zhang W et al (2016) The research progress on desert Lycium ruthenicum. Pratacult Sci 33:1835–1845Google Scholar
  17. Horikoshi K (2008) Past, present and future of extremophiles. Extremophiles 12:1–2.  https://doi.org/10.1007/s00792-007-0127-5 Google Scholar
  18. Jasim B, Joseph AA, John CJ et al (2014) Isolation and characterization of plant growth promoting endophytic bacteria from the rhizome of Zingiber officinale. 3Biotech, 4(2):197–204Google Scholar
  19. Jia F, Tiyip T, Wu N et al (2017) Characteristics of soil seed banks at different geomorphic positions within the longitudinal sand dunes of the Gurbantunggut Desert, China. J Arid Land 9(3):355–367Google Scholar
  20. Jin H, Yang XY, Yan ZQ et al (2014) Characterization of rhizosphere and endophytic bacterial communities from leaves, stems and roots of medicinal Stellera chamaejasme L. Syst Appl Microbiol 37(5):376–385Google Scholar
  21. Kim M, Oh HS, Park SC et al (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351Google Scholar
  22. Ki̇zi̇lkaya R (2009) Nitrogen fixation capacity of Azotobacter spp. strains isolated from soils in different ecosystems and relationship between them and the microbiological properties of soils. J Environ Biol 30(1):73–82Google Scholar
  23. Kumar S, Stecher G, Tamura K (2016) Mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874Google Scholar
  24. Li L (2011) Diversity and phylogeny of rhizobia and endophytes isolated from Glycyrrhiza spp. nodules in Northwestern China. Dissertation, Northwest A & F UniversityGoogle Scholar
  25. Li WJ, Xu P, Schumann P et al (2007) Georgenia ruanii sp. nov., a novel Actinobacterium isolated from forest soil in Yunnan (China) and emended description of the genus Georgenia. Int J Syst Evol Microbiol 57:1424–1428Google Scholar
  26. Li C, Liu R, Wang S, et al (2018a) Growth and sustainability of Suaeda salsa in the Lop Nur, China. J Arid Land 10(3):1–12Google Scholar
  27. Li L, Mohamad OAA, Ma J et al (2018b) Synergistic plant–microbe interactions between endophytic bacterial communities and the medicinal plant Glycyrrhiza uralensis F. Antonie Van Leeuwenhoek 42(19):1–14Google Scholar
  28. Liotti RG, Mi DSF, Da SG et al (2018) Diversity of cultivable bacterial endophytes in paullinia cupana and their potential for plant growth promotion and phytopathogen control. Microbiol Res 207:8.  https://doi.org/10.1016/j.micres.2017.10.011 Google Scholar
  29. Liu YH, Guo JW, Salam N et al (2016) Culturable endophytic bacteria associated with medicinal plant Ferula songorica: molecular phylogeny, distribution and screening for industrially important traits. 3 Biotech 6(2):209.  https://doi.org/10.1007/s13205-016-0522-7 Google Scholar
  30. Liu YH, Guo JW, Li L et al (2017a) Endophytic bacteria associated with endangered plant Ferula sinkiangensis KM Shen in an arid land: diversity and plant growth-promoting traits. J Arid Land 9(3):432–445Google Scholar
  31. Liu X, Ma J, Ma ZW et al (2017b) Soil nutrient contents and stoichiometry as affected by land-use in an agro-pastoral region of northwest China. Catena 150:146–153Google Scholar
  32. Lodewyck C, Vangronsveld J, Porteous F et al (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21(6):583–606Google Scholar
  33. Long HH, Sonntag DG, Schmidt DD et al (2010) The structure of the culturable root bacterial endophyte community of Nicotiana attenuate is organized by soil composition and host plant ethylene production and perception. New Phytol 185(2):554–567Google Scholar
  34. Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci USA 104: 11436–11440Google Scholar
  35. Meunchang S, Panichsakpatana S, Weaver RW (2006) Tomato growth in soil amended with sugar mill by-products compost. Plant Soil 280(1–2):171–176Google Scholar
  36. Mohamad OAA, Li L, MaJ B et al (2018) Evaluation of the antimicrobial activity of endophytic bacterial populations from Chinese traditional medicinal plant licorice and characterization of the bioactive secondary metabolites produced by Bacillus atrophaeus against Verticillium dahliae. Front Microbiol.  https://doi.org/10.3389/fmicb.2018.00924 Google Scholar
  37. Nimaichand S, Devi AM, Li WJ (2016) Direct plant growth-promoting ability of Actinobacteria in grain legumes. In: Subramaniam G, Arumugam S, Rajendran V Plant growth promoting actinobacteria: a new avenue for enhancing the productivity and soil fertility of grain legumes. Springer, Singapore, pp 1–16Google Scholar
  38. Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17:362–370Google Scholar
  39. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425Google Scholar
  40. Santoyo G, Moreno-Hagelsieb G, del C Orozco-Mosqueda M, et al (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99Google Scholar
  41. Schulthess FM, Faeth SH (1998) Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycologia 90(4):569–578Google Scholar
  42. Singh M, Kumar A, Singh R et al (2017) Endophytic bacteria: a new source of bioactive compounds. 3 Biotech 7:315.  https://doi.org/10.1007/s13205-017-0942-z Google Scholar
  43. Wang HF (2015) Study on biodiversity of endophytic bacteria isolated from four Chenopodiaceae halophytes in Xinjiang and evaluation of their growth-promoting function and salt-tolerance ability. PhD Dissertation. Urumqi: Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences. (In Chinese) Google Scholar
  44. Wang W, Zhai Y, Cao L et al (2016) Illumina-based analysis of core actinobacteriome in roots, stems, and grains of rice. Microbiol Res 190:12–18Google Scholar
  45. Wicaksono WA, Jones EE, Monk J et al (2017) Using bacterial endophytes from a New Zealand native medicinal plant for control of grapevine trunk diseases. Biol Control 114:65–72Google Scholar
  46. Yoon SH, Ha SM, Kwon S et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67(5):1613–1618Google Scholar
  47. Zhang F, Zhai H, Li H et al (2016) Technology research of greenhouse seedling raising and afforestation in coastal saline-alkali soil of Lycium ruthenicum Murr. Chin Agric Sci Bull 32:14–17. (In Chinese)Google Scholar
  48. Zhang G, Chen S, Zhou W et al (2018) Rapid qualitative and quantitative analyses of eighteen phenolic compounds from Lycium ruthenicum, Murray by UPLC-Q-Orbitrap MS and their antioxidant activity. Food Chem 269:150–156Google Scholar
  49. Zhao S, Zhou N, Wang L et al (2013) Halophyte-endophyte coupling: a promising bioremediation system for oil-contaminated soil in Northwest China. Environ Sci Technol, 47(21):11938–11939Google Scholar
  50. Zheng J, Ding C, Wang L et al (2011) Anthocyanins composition and antioxidant activity of wild Lycium ruthenicum Murr. from Qinghai-Tibet plateau. Food Chem 126:859–865Google Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  • Yong-Hong Liu
    • 1
    • 4
  • Yong-Yang Wei
    • 1
  • Osama Abdalla Abdelshafy Mohamad
    • 1
    • 5
  • Nimaichand Salam
    • 2
  • Yong-guang Zhang
    • 1
  • Jian-Wei Guo
    • 1
    • 3
  • Li Li
    • 1
  • Dilfuza Egamberdieva
    • 1
    • 6
  • Wen-Jun Li
    • 1
    • 2
    Email author
  1. 1.Key Laboratory of Biogeography and Bioresource in Arid LandXinjiang Institute of Ecology and Geography, Chinese Academy of SciencesUrumqiPeople’s Republic of China
  2. 2.State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, School of Life SciencesSun Yat-Sen UniversityGuangzhouPeople’s Republic of China
  3. 3.Key Laboratory of Crops with High Quality and Efficient Cultivation and Security Control, Yunnan Higher Education InstitutionsHonghe UniversityMengziPeople’s Republic of China
  4. 4.University of Chinese Academy of SciencesBeijingPeople’s Republic of China
  5. 5.Department of Biological, Marine Sciences, and Environmental Agriculture, Institute for Post Graduate Environmental StudiesArish UniversityArishEgypt
  6. 6.Department of Biotechnology and Microbiology, Faculty of Biology and Soil ScienceNational University of UzbekistanTashkentUzbekistan

Personalised recommendations