Different Height Forms of Spartina alterniflora Might Select Their Own Rhizospheric Bacterial Communities in Southern Coast of China

Abstract

In the southernmost part of coast of China, two height forms of Spartina alterniflora, tall and short, have invaded Leizhou Peninsula within the last decade. However, the effect of different height forms of Spartina alterniflora on plant–microbe interaction has not been clarified. Here, the community structures of rhizosphere bacteria and the abundance of N- and S-cycling functional genes associated with selected S. alterniflora were investigated in the field and a common garden. The community structure of tall-form S. alterniflora was distinct from short-form S. alterniflora at OTU level in the field, even after transplantation into a common garden. The abundance of bacterial amoA, nirS, and nosZ in tall S. alterniflora was significantly greater than those in short S. alterniflora in the field; however, this difference disappeared in a 1-year common garden experiment. These results suggested that compared with the tall-form S. alterniflora, the rhizosphere of short-form S. alterniflora harbored fewer nitrification–denitrification related microorganisms, which might benefit from conserving N in an N limited habitat. Together, our results suggested that tall- and short-form S. alterniflora can host their specific rhizosphere microbial communities and had different strategies of N usage via selecting the composition of rhizosphere bacterial assemblages, which in turn might determine the growth and invasiveness of S. alterniflora in its introduced range.

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References

  1. 1.

    Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev. 37:634–663. https://doi.org/10.1111/1574-6976.12028

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci. 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Haichar FE, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230. https://doi.org/10.1038/ismej.2008.80

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Bais HP, Walker TS, Schweizer HP, Vivanco JA (2002) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiol Biochem 40:983–995. https://doi.org/10.1016/s0981-9428(02)01460-2

    CAS  Article  Google Scholar 

  5. 5.

    Zhang S, Zhu W, Wang B, Tang J, Chen X (2011) Secondary metabolites from the invasive Solidago canadensis L. accumulation in soil and contribution to inhibition of soil pathogen Pythium ultimum. Appl. Soil Ecol. 48:280–286. https://doi.org/10.1016/j.apsoil.2011.04.011

    Article  Google Scholar 

  6. 6.

    Huang J, Xu X, Wang M, Nie M, Qiu S, Wang Q, Quan Z, Xiao M, Li B (2016) Responses of soil nitrogen fixation to Spartina alterniflora invasion and nitrogen addition in a Chinese salt marsh. Sci. Rep. 6. https://doi.org/10.1038/srep20384

  7. 7.

    Jia D, Qi F, Xu X, Feng J, Wu H, Guo J, Lu W, Peng R, Zhu X, Luo Y (2016) Co-regulations of Spartina alterniflora invasion and exogenous nitrogen loading on soil N2O efflux in subtropical mangrove mesocosms. PLoS One 11:e0146199. https://doi.org/10.1371/journal.pone.0146199

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    An S, Gu B, Zhou C, Wang Z, Deng Z, Zhi Y, Li H, Chen L, Yu D, Liu Y (2007) Spartina invasion in China: implications for invasive species management and future research. Weed Res. 47:183–191. https://doi.org/10.1111/j.1365-3180.2007.00559.x

    Article  Google Scholar 

  9. 9.

    Liu W, Maung-Douglass K, Strong DR, Pennings SC, Zhang Y (2016) Geographical variation in vegetative growth and sexual reproduction of the invasive Spartina alterniflora in China. J. Ecol. 104:173–181. https://doi.org/10.1111/1365-2745.12487

    CAS  Article  Google Scholar 

  10. 10.

    Strong DR, Ayres DR (2013) Ecological and evolutionary misadventures of Spartina. Annu Rev Ecol Evol Syst 44:389–410. https://doi.org/10.1146/annurev-ecolsys-110512-135803

  11. 11.

    Wan S, Qin P, Liu J, Zhou H (2009) The positive and negative effects of exotic Spartina alterniflora in China. Ecol. Eng. 35:444–452. https://doi.org/10.1016/j.ecoleng.2008.05.020

    Article  Google Scholar 

  12. 12.

    Zhang Y, Huang G, Wang W, Chen L, Lin G (2012) Interactions between mangroves and exotic Spartina in an anthropogenically disturbed estuary in southern China. Ecology 93:588–597. https://doi.org/10.1890/11-1302.1

    Article  PubMed  Google Scholar 

  13. 13.

    Gallagher JL, Somers GF, Grant DM, Seliskar DM (1988) Persistent differences in two forms of Spartina alterniflora: a common garden experiment. Ecology 69:1005–1008. https://doi.org/10.2307/1941255

    Article  Google Scholar 

  14. 14.

    Mendelssohn IA, McKee KL (1988) Spartina alterniflora die-back in Louisiana: time-course investigation of soil waterlogging effects. J. Ecol. 76:509–521. https://doi.org/10.2307/2260609

    Article  Google Scholar 

  15. 15.

    Degnan PH, Ochman H (2012) Illumina-based analysis of microbial community diversity. ISME J 6:183–194. https://doi.org/10.1038/ismej.2011.74

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Hu A, Yang X, Chen N, Hou L, Ma Y, Yu C-P (2014) Response of bacterial communities to environmental changes in a mesoscale subtropical watershed, Southeast China. Sci Total Environ 472:746–756. https://doi.org/10.1016/j.scitotenv.2013.11.097

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Gremion F, Chatzinotas A, Harms H (2003) Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. Environ Microbiol 5:896–907. https://doi.org/10.1046/j.1462-2920.2003.00484.x

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Dar SA, Yao L, van Dongen U, Kuenen JG, Muyzer G (2007) Analysis of diversity and activity of sulfate-reducing bacterial communities in sulfidogenic bioreactors using 16S rRNA and dsrB genes as molecular markers. Appl Environ Microbiol 73:594–604. https://doi.org/10.1128/AEM.01875-06

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci U S A 102:14683–14688. https://doi.org/10.1073/pnas.0506625102

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189. https://doi.org/10.1128/aem.00231-06

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Jemaneh Zeleke QS, Wang J-G, Huang M-Y, Xia F, Wu J-H, Quan Z-X (2013) Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine marsh sediments. Front. Microbiol. 4. doi: https://doi.org/10.3389/fmicb.00243

  22. 22.

    Magalhães CM, Machado A, Matos P, Bordalo AA (2011) Impact of copper on the diversity, abundance and transcription of nitrite and nitrous oxide reductase genes in an urban European estuary. FEMS Microbiol Ecol 77:274–284. https://doi.org/10.1111/j.1574-6941.2011.01107.x

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res. Microbiol. 152:95–103. https://doi.org/10.1016/S0923-2508(00)01172-4

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Rotthauwe J-H, Witzel K-P, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124. https://doi.org/10.1093/bioinformatics/btu494

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Uroz S, Buée M, Murat C, Frey-Klett P, Martin F (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ Microbiol Rep 2:281–288. https://doi.org/10.1111/j.1758-2229.2009.00117.x

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Weinert N, Piceno Y, Ding G-C, Meincke R, Heuer H, Berg G, Schloter M, Andersen G, Smalla K (2011) PhyloChip hybridization uncovered an enormous bacterial diversity in the rhizosphere of different potato cultivars: many common and few cultivar-dependent taxa. FEMS Microbiol. Ecol. 75:497–506. https://doi.org/10.1111/j.1574-6941.2010.01025.x

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Xia F, Zeleke J, Sheng Q, Wu J-H, Quan Z-X (2015) Communities of ammonia oxidizers at different stages of Spartina alterniflora invasion in salt marshes of Yangtze River estuary. J. Microbiol. 53:311–320. https://doi.org/10.1007/s12275-015-4660-0

    Article  PubMed  Google Scholar 

  31. 31.

    Zheng Y, Bu N-S, Long X-E, Sun J, He C-Q, Liu X-Y, Cui J, Liu D-X, Chen X-P (2017) Sulfate reducer and sulfur oxidizer respond differentially to the invasion of Spartina alterniflora in estuarine salt marsh of China. Ecol. Eng. 99:182–190. https://doi.org/10.1016/j.ecoleng.2016.11.031

    Article  Google Scholar 

  32. 32.

    DeAngelis KM, Ji P, Firestone MK, Lindow SE (2005) Two novel bacterial biosensors for detection of nitrate availability in the rhizosphere. Appl Environ Microbiol 71:8537–8547. https://doi.org/10.1128/AEM.71.12.8537-8547.2005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Koch B, Worm J, Jensen LE, Højberg O, Nybroe O (2001) Carbon limitation induces ςS-dependent gene expression in pseudomonas fluorescens in soil. Appl Environ Microbiol 67:3363–3370. https://doi.org/10.1128/AEM.67.8.3363-3370.2001

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Yang L, Chang H-T, Huang M-NL (2001) Nutrient removal in gravel-and soil-based wetland microcosms with and without vegetation. Ecol Eng 18:91–105. https://doi.org/10.1016/S0925-8574(01)00068-4

    Article  Google Scholar 

  35. 35.

    Stottmeister U, Wießner A, Kuschk P, Kappelmeyer U, Kästner M, Bederski O, Müller R, Moormann H (2003) Effects of plants and microorganisms in constructed wetlands for wastewater treatment. Biotechnol. Adv. 22:93–117. https://doi.org/10.1016/j.biotechadv.2003.08.010

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Muyzer G, Stams AJ (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454. https://doi.org/10.1038/nrmicro1892

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Klein M, Friedrich M, Roger AJ, Hugenholtz P, Fishbain S, Abicht H, Blackall LL, Stahl DA, Wagner M (2001) Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J. Bacteriol. 183:6028–6035. https://doi.org/10.1128/JB.183.20.6028-6035.2001

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Klepac-Ceraj V, Bahr M, Crump BC, Teske AP, Hobbie JE, Polz MF (2004) High overall diversity and dominance of microdiverse relationships in salt marsh sulphate-reducing bacteria. Environ Microbiol 6:686–698. https://doi.org/10.1111/j.1462-2920.2004.00600.x

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

We thank Professor John Hodgkiss of the City University of Hong Kong for his assistance with the English language.

Funding

This research was supported by the Fundamental Research Funds for the Central Universities (Grant No. 20720150097).

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Correspondence to Yihui Zhang or Yun Tian.

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Lin, L., Liu, W., Zhang, M. et al. Different Height Forms of Spartina alterniflora Might Select Their Own Rhizospheric Bacterial Communities in Southern Coast of China. Microb Ecol 77, 124–135 (2019). https://doi.org/10.1007/s00248-018-1208-y

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Keywords

  • Spartina alterniflora
  • Rhizosphere bacteria
  • Plant–microbe interaction
  • Nitrogen cycling