Annals of Microbiology

, Volume 68, Issue 5, pp 273–286 | Cite as

Bacterial community structure associated with the rhizosphere soils and roots of Stellera chamaejasme L. along a Tibetan elevation gradient

  • Hui Jin
  • Xiaoyan Yang
  • Rentao Liu
  • Zhiqiang Yan
  • Xudong Li
  • Xiuzhuang Li
  • Anxiang Su
  • Yuhui Zhao
  • Bo Qin
Original Article
  • 25 Downloads

Abstract

The effect of altitude on the composition and diversity of microbial communities have attracted highly attention recently but is still poorly understood. We used 16S rRNA gene clone library analyses to characterize the bacterial communities from the rhizosphere and roots of Stellera chamaejasme in the Tibetan Plateau. Our results revealed that Actinobacteria and Proteobacteria were dominant bacteria in this medicinal plant in the rhizosphere and root communities. The Shannon diversity index showed that the bacterial diversity of rhizosphere follows a small saddle pattern, while the roots possesses of a hump-backed trend. Significant differences in the composition of bacterial communities between rhizosphere and roots were detected based on multiple comparisons analysis. The community of Actinobacteria was found to be significantly negative correlated with soil available P (p < 0.01), while the phylum of Proteobacteria showed a positive relationship with available P (p < 0.05). Moreover, redundancy analysis indicated that soil phosphorus, pH, latitude, elevation and potassium positively correlated with bacterial communities associated with rhizosphere soils. Taken together, we provide evidence that bacterial communities associated with S. chamaejasme exhibited some certain elevational pattern, and bacterial communities of rhizosphere soil were regulated by environmental characteristics along elevational gradients in this alpine ecosystem.

Keywords

Bacterial community Phylogenetic diversity Stellera chamaejasme L. Tibetan Plateau Elevation gradient 

Notes

Acknowledgements

The authors are grateful the Professor Frank Stermitz for assistance with language editing. This work was financially supported by the National Key Research and Development Program (2017YFD0200804), the National Natural Science Foundation of China (No. 31772668, 21775154, 31560037 and 31570354), the Open Project Program of Breeding Base for State Key Laboratory of Land Degradation and Ecological Restoration of North-western China/Key Laboratory for Restoration and Reconstruction of Degraded Ecosystem in North-western China of Ministry of Education (2017KF009), the Open Project Program for State Key Laboratory of Grassland Agro-ecosystem of Lanzhou University (SKLGAE201704), Basic Research Program of Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences (080423SYR1), the Youth Science Foundations of Gansu Province (1506RJYA294), and Around five top priorities program of “One-Three-Five” Strategic Planning of Lanzhou Institute of Chemical Physics, Chinese Academy of Sciences.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

13213_2018_1336_MOESM1_ESM.pdf (1.9 mb)
ESM 1 (PDF 1971 kb)

References

  1. Anderson I, Abt B, Lykidis A, Klenk HP, Kyrpides N, Ivanova N (2012) Genomics of aerobic cellulose utilization systems in actinobacteria. PLoS One 7:e39331CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anwar S, Ali B, Sajid I (2016) Screening of rhizospheric actinomycetes for various in-vitro and in-vivo plant growth promoting (PGP) traits and for agroactive compounds. Front Microbiol 7:1334CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8:e56329CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL (2008) Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci U S A 105(Supplement 1):11505–11511CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun YN, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:633–642CrossRefGoogle Scholar
  6. Colwell RK, Lees DC (2000) The mid-domain effect: geometric constraints on the geography of species richness. Trends Ecol Evol 15:70–76CrossRefPubMedGoogle Scholar
  7. Compant S, Mitter B, Colli-Mull JG, Gangl H, Sessitsch A (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197CrossRefPubMedGoogle Scholar
  8. Corneo PE, Pellegrini A, Cappellin L, Roncador M, Chierici M, Gessler C, Pertot I (2013) Microbial community structure in vineyard soils across altitudinal gradients and in different seasons. FEMS Microbiol Ecol 84:588–602CrossRefPubMedGoogle Scholar
  9. Costa R, Götz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56:236–249CrossRefPubMedGoogle Scholar
  10. Cui HY, Jin H, Liu Q, Yan ZQ, Ding L, Qin B (2014) Nematicidal metabolites from roots of Stellera chamaejasme against Bursaphelenchus xylophilus and Bursaphelenchus mucronatus. Pest Manag Sci 70:827–835CrossRefPubMedGoogle Scholar
  11. Cui HY, Yang XY, Lu DX, Jin H, Yan ZQ, Chen JX, Li XZ, Qin B (2015) Isolation and characterization of bacteria from the rhizosphere and bulk soil of Stellera chamaejasme L. Can J Microbiol 61:171–181CrossRefPubMedGoogle Scholar
  12. Djukic I, Zehetner F, Mentler A, Gerzabek MH (2010) Microbial community composition and activity in different alpine vegetation zones. Soil Biol Biochem 42:155–161CrossRefGoogle Scholar
  13. Faoro H, Alves AC, Souza EM, Rigo LU, Cruz LM, Al-Janabi SM, Monteiro RA, Baura VA, Pedrosa FO (2010) Influence of soil characteristics on the diversity of bacteria in the southern Brazilian Atlantic forest. Appl Environ Microbiol 76:4744–4749CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fierer N, McCain CM, Meir P, Zimmermann M, Rapp JM, Silman MR, Knight R (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92:797–804CrossRefPubMedGoogle Scholar
  15. França L, Sannino C, Turchetti B, Buzzini P, Margesin R (2016) Seasonal and altitudinal changes of culturable bacterial and yeast diversity in alpine forest soils. Extremophiles 20:855–873CrossRefPubMedPubMedCentralGoogle Scholar
  16. Galperin MY (2013) Genomic diversity of spore-forming Firmicutes. Microbiol Spectr 1: TBS-0015-2012Google Scholar
  17. Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA, Podar M, Karpinets T, Uberbacher E, Tuskan GA, Vilgalys R, Doktycz MJ, Schadt CW (2011) Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl Environ Microbiol 77:5934–5944CrossRefPubMedPubMedCentralGoogle Scholar
  18. Guo GX, Kong WD, Liu JB, Zhao JX, Du HD, Zhang XZ, Xia PH (2015a) Diversity and distribution of autotrophic microbial community along environmental gradients in grassland soils on the Tibetan plateau. Appl Microbiol Biotechnol 99:8765–8776CrossRefPubMedGoogle Scholar
  19. Guo HR, Cui HY, Jin H, Yan ZQ, Ding L, Qin B (2015b) Potential allelochemicals in root zone soils of Stellera chamaejasme L. and variations at different geographical growing sites. Plant Growth Regul 77:335–342CrossRefGoogle Scholar
  20. Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319CrossRefPubMedGoogle Scholar
  21. Jin H, Yang XY, Yan ZQ, Liu Q, Li XZ, Chen JX, Zhang DH, Zeng LM, Qin B (2014) Characterization of rhizospere and endophytic bacterial communities from leaves, stems and roots of medicinal Stellera chamaejasme L. Syst Appl Microbiol 37:376–385CrossRefPubMedGoogle Scholar
  22. Jin H, Yang XY, Lu DX, Li CJ, Yan ZQ, Li XZ, Zeng LM, Qin B (2015) Phylogenic diversity and tissue specificity of fungal endophytes associated with the pharmaceutical plant, Stellera chamaejasme L. revealed by a cultivation independent approach. Anton Leeuw Int J G 108:835–850CrossRefGoogle Scholar
  23. Kan FL, Chen ZY, Wang ET, Tian CF, Sui XH, Chen WX (2007) Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in Qinghai-Tibet plateau and in other zones of China. Arch Microbiol 188:103–115CrossRefPubMedGoogle Scholar
  24. Khan AL, Waqas M, Kang SM, Al-Harrasi A, Hussain J, Al-Rawahi A, Al-Khiziri S, Ullah I, Ali L, Jung HY, Lee IJ (2014) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52:689–695CrossRefPubMedGoogle Scholar
  25. Kourteva PS, Ehrenfelda JG, Häggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905CrossRefGoogle Scholar
  26. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  27. Li XZ, Rui JP, Mao YJ, Yannarell A, Mackie R (2014) Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biol Biochem 68:392–401CrossRefGoogle Scholar
  28. Li YC, Li Z, Li ZW, Jiang YH, Weng BQ, Lin WX (2016) Variations of rhizosphere bacterial communities in tea (Camellia sinensis L.) continuous cropping soil by high-throughput pyrosequencing approach. J Appl Microbiol 121:787–799CrossRefPubMedGoogle Scholar
  29. Lu RK (2000) Methods of soil and agro-chemistry. Chinese Agricultural Science and Technology Press, BeijingGoogle Scholar
  30. Lugtenberg B, Kamilova F (2009) Plant-growth promoting rhizobacteria. Annu Rev Microbiol 63:541–556CrossRefPubMedGoogle Scholar
  31. Männistö MK, Tiirola M, Häggblom MM (2007) Bacterial communities in Arctic fields of Finnish Lapland are stable but highly pH-dependent. FEMS Microbiol Ecol 59:452–465CrossRefPubMedGoogle Scholar
  32. Margesin R, Jud M, Tscherko D, Schinner F (2009) Microbial communities and activities in alpine and subalpine soils. FEMS Microbiol Ecol 67:208–218CrossRefPubMedGoogle Scholar
  33. Padda KP, Puri A, Chanway CP (2016) Effect of GFP tagging of Paenibacillus polymyxa P2b-2R on its ability to promote growth of canola and tomato seedlings. Biol Fertil Soils 52:377–387CrossRefGoogle Scholar
  34. Palaniyandi SA, Yang SH, Zhang L, Suh JW (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Appl Microbiol Biotechnol 97:9621–9636CrossRefPubMedGoogle Scholar
  35. Pragya R, Yasmin A, Anshula J (2012) An insight into agricultural properties of actinomycetes. Int J Res BioSci 1:7–12Google Scholar
  36. Qiu J (2008) China: the third pole. Nature 454:393–396CrossRefPubMedGoogle Scholar
  37. Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837CrossRefPubMedGoogle Scholar
  38. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments andapplications. FEMS Microbiol Lett 278:1–9CrossRefPubMedGoogle Scholar
  39. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  40. Shen SY, Fulthorpe R (2015) Seasonal variation of bacterial endophytes in urban trees. Front Microbiol 6:427PubMedPubMedCentralGoogle Scholar
  41. Shen CC, Xiong JB, Zhang HY, Feng YZ, Lin XG, Li XY, Liang WJ, Chu HY (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211CrossRefGoogle Scholar
  42. Shen CC, Ni YY, Liang WJ, Wang JJ, Chu HY (2015) Distinct soil bacterial communities along a small-scale elevational gradient in alpine tundra. Front Microbiol 6:582PubMedPubMedCentralGoogle Scholar
  43. Singh D, Takahashi K, Kim M, Chun J, Adams JM (2012) A hump-backed trend in bacterial diversity with elevation on Mount Fuji, Japan. Microb Ecol 63:429–437CrossRefPubMedGoogle Scholar
  44. Singh D, Lee-Cruz L, Kim WS, Kerfahi D, Chun JH, Adams JM (2014) Strong elevational trends in soil bacterial community composition on Mt. Halla, South Korea. Soil Biol Biochem 68:140–149CrossRefGoogle Scholar
  45. Sundqvist MK, Liu ZF, Giesler R, Wardle DA (2014) Plant and microbial responses to nitrogen and phosphorus addition across an elevational gradient in subarctic tundra. Ecology 95:1819–1835CrossRefPubMedGoogle Scholar
  46. Tamreihao K, Ningthoujam DS, Nimaichand S, Singh ES, Reena P, Singh SH, Nongthomba U (2016) Biocontrol and plant growth promoting activities of a Streptomyces corchorusii strain UCR3-16 and preparation of powder formulation for application as biofertilizer agents for rice plant. Microbiol Res 192:260–270CrossRefPubMedGoogle Scholar
  47. Teixeira LCRS, Peixoto RS, Cury JC, Sul WJ, Pellizari VH, Tiedje J, Rosado AS (2010) Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J 4:989–1001CrossRefPubMedGoogle Scholar
  48. Terrazas RA, Giles C, Paterson E, Robertson-Albertyn S, Cesco S, Mimmo T, Pii Y, Bulgarelli D (2016) Plant-microbiota interactions as a driver of the mineral turnover in the rhizosphere. Adv Appl Microbiol 95:1–67Google Scholar
  49. Ulrich K, Ulrich A, Ewald D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol Ecol 63:169–180CrossRefPubMedGoogle Scholar
  50. Wakelin S, Mander C, Gerard E, Jansa J, Erb A, Young S, Condron L, O'Callaghan M (2012) Response of soil microbial communities to contrasted histories of phosphorus fertilisation in pastures. Appl Soil Ecol 61:40–48CrossRefGoogle Scholar
  51. Wang JT, Cao P, Hu HW, Li J, Han LL, Zhang LM, Zheng YM, He JZ (2015) Altitudinal distribution patterns of soil bacterial and archaeal communities along Mt. Shegyla on the Tibetan Plateau. Microb Ecol 69:135–145CrossRefPubMedGoogle Scholar
  52. Wawrik B, Kerkhof L, Kukor J, Zylstra G (2005) Effect of different carbon sources on community composition of bacterial enrichments from soil. Appl Environ Microbiol 71:6776–6783CrossRefPubMedPubMedCentralGoogle Scholar
  53. Wu ZX, Hao ZP, Zeng Y, Guo LP, Huang LQ, Chen BD (2015) Molecular characterization of microbial communities in the rhizosphere soils and roots of diseased and healthy Panax notoginseng. Anton Leeuw Int J G 108:1059–1074CrossRefGoogle Scholar
  54. Yao YX, Tang HZ, Su F, Xu P (2015) Comparative genome analysis reveals the molecular basis of nicotine degradation and survival capacities of Arthrobacter. Sci Rep UK 5:8642CrossRefGoogle Scholar
  55. Yuan YL, Si GC, Wang J, Luo TX, Zhang GX (2014) Bacterial community in alpine grasslands along an altitudinal gradient on the Tibetan Plateau. FEMS Microbiol Ecol 87:121–132CrossRefPubMedGoogle Scholar
  56. Zhang LM, Wang M, Prosser JI, Zheng YM, He JZ (2009) Altitude ammonia-oxidizing bacteria and archaea in soils of Mount Everest. FEMS Microbiol Ecol 70:208–217CrossRefGoogle Scholar
  57. Zhang C, Zhou SS, Feng LY, Zhang DY, Lin NM, Zhang LH, Pan JP, Wang JB, Li J (2013) In vitro anti-cancer activity of chamaejasmenin B and neochamaejasmin C isolated from the root of Stellera chamaejasme L. Acta Pharmacol Sin 34:262–270CrossRefPubMedGoogle Scholar
  58. Zhang BG, Zhang W, Liu GX, Chen T, Zhang GS, Wu XK, Chen XM, Chang SJ (2015) Variations in culturable terrestrial bacterial communities and soil biochemical characteristics along an altitude gradient upstream of the Shule river, Qinghai-Tibetan Plateau. Nat Environ Pollut Technol 14:839–846Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature and the University of Milan 2018

Authors and Affiliations

  • Hui Jin
    • 1
    • 2
  • Xiaoyan Yang
    • 2
  • Rentao Liu
    • 1
  • Zhiqiang Yan
    • 2
  • Xudong Li
    • 3
  • Xiuzhuang Li
    • 2
  • Anxiang Su
    • 4
  • Yuhui Zhao
    • 5
  • Bo Qin
    • 2
  1. 1.State Key Laboratory of Land Degradation and Ecological Restoration of North-western China and Key Laboratory for Restoration and Reconstruction of Degraded Ecosystem in North-western China of Ministry of EducationYinchuanPeople’s Republic of China
  2. 2.CAS Key Laboratory of Chemistry of Northwestern Plant Resources and Key Laboratory for Natural Medicine of Gansu Province, Lanzhou Institute of Chemical PhysicsChinese Academy of Sciences (CAS)LanzhouPeople’s Republic of China
  3. 3.State Key Laboratory of Grassland Agro-ecosystem, College of Pastoral Agriculture Science and TechnologyLanzhou UniversityLanzhouPeople’s Republic of China
  4. 4.Institute for the Control of AgrochemicalsMinistry of Agriculture (ICAMA)BeijingPeople’s Republic of China
  5. 5.Institute of BiologyGansu Academy of SciencesLanzhouPeople’s Republic of China

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