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Macrophyte identity shapes water column and sediment bacterial community

  • Yanran DaiEmail author
  • Juan Wu
  • Fei Zhong
  • Naxin Cui
  • Lingwei Kong
  • Wei Liang
  • Shuiping ChengEmail author
Primary Research Paper
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Abstract

By assembling mesocosms and utilizing high-throughput sequencing, we aim to characterize the shifts of the bacterial community in freshwaters driven by two contrasting submerged macrophyte species, Ceratophyllum demersum L. and Vallisneria spiralis L. Although the microbe in both the water column and sediment were largely modulated by the macrophyte, the effect varied considerably depending on bacterial locations and macrophyte species. Actinobacteria was the most abundant taxa in the water column of all the three treatments, but its abundances were significantly higher in the two planted treatments. Moreover, Alphaproteobacteria showed high abundance only in the unplanted control. For bacterial taxa in the sediment, C. demersum significantly increased the relative abundance of Anaerolineae but reduced the relative abundance of Betaproteobacteria and Gammaproteobacteria, while V. spiralis increased the relative abundance of Deltaproteobacteria and Gammaproteobacteria. Additionally, in the C. demersum treatment, the water column bacterial community increased more dramatically in richness, alpha diversity, and the relative abundance of the dominant taxa than those in the V. spiralis treatment. Taken together, the findings from this study reveal that the two species of submerged macrophyte modified the bacterial community in waters, despite the obvious interspecific performance differences.

Keywords

Submerged macrophyte Microbe Mesocosms Illumina high-throughput sequencing 

Notes

Acknowledgements

This study was financed by the National Natural Science Foundation of China (51609238 and 51578395). We declare no conflicts of interest. We thank the editor and reviewers for their constructive comments that improved this paper.

References

  1. Ahn, C., P. M. Gillevet & M. Sikaroodi, 2007. Molecular characterization of microbial communities in treatment microcosm wetlands as influenced by macrophytes and phosphorus loading. Ecological Indicators 7: 852–863.CrossRefGoogle Scholar
  2. Amaral, V., D. Graeber, D. Calliari & C. Alonso, 2016. Strong linkages between DOM optical properties and main clades of aquatic bacteria. Limnology and Oceanography 61: 906–918.CrossRefGoogle Scholar
  3. Baart, I., C. Gschöpf, A. P. Blaschke, S. Preiner & T. Hein, 2010. Prediction of potential macrophyte development in response to restoration measures in an urban riverine wetland. Aquatic Botany 93: 153–162.CrossRefGoogle Scholar
  4. Boschker, H. T. S., J. F. C. De Brouwer & T. E. Cappenberg, 1999. The contribution of macrophyte-derived organic matter to microbial biomass in salt-marsh sediments: stable carbon isotope analysis of microbial biomarkers. Limnology and Oceanography 44: 309–319.CrossRefGoogle Scholar
  5. Boschker, H. T. S., A. Wielemaker, B. E. M. Schaub & M. Holmer, 2000. Limited coupling of macrophyte production and bacterial carbon cycling in the sediments of Zostera spp. meadows. Marine Ecology Progress Series 203: 181–189.CrossRefGoogle Scholar
  6. Brix, H. & H. H. Schierup, 1989. The use of aquatic macrophytes in water-pollution control. Ambio Stockholm 18: 100–107.Google Scholar
  7. Brum, P. R. & F. A. Esteves, 2001. Changes in abundance and biomass of the attached bacterial community throughOTU the decomposition of three species of aquatic macrophytes. In: Faria, B.M.; Farjalla, V.F. & Esteves, F.A. (eds). Aquatic Microbial Ecology in Brazil. Series Oecologia Brasiliensis, vol. IX. PPGE-UFRJ: 77-96.Google Scholar
  8. Bunse, C., M. Bertos-Fortis, I. Sassenhagen, S. Sildever, C. Sjöqvist, A. Godhe, S. Gross, A. Kremp, I. Lips, N. Lundholm & K. Rengefors, 2016. Spatio-temporal interdependence of bacteria and phytoplankton during a Baltic Sea spring bloom. Frontiers in Microbiology 7: 517.CrossRefGoogle Scholar
  9. Carpenter, S. R. & D. M. Lodge, 1986. Effects of submersed macrophytes on ecosystem processes. Aquatic Botany 26: 341–370.CrossRefGoogle Scholar
  10. Clarke, K. R. & R. N. Gorley, 2001. PRIMER v5: User Manual/Tutorial. PRIMER-E: PlymOTUh: UK.Google Scholar
  11. Dai, Y. R., C. R. Jia, W. Liang, S. H. Hu & Z. B. Wu, 2012. Effects of the submerged macrophyte Ceratophyllum demersum L. on restoration of a eutrophic waterbody and its optimal coverage. Ecological Engineering 40: 113–116.CrossRefGoogle Scholar
  12. Dai, Y. R., J. Wu, X. H. Ma, F. Zhong, N. X. Cui & S. P. Cheng, 2017. Increasing phytoplankton-available phosphorus and inhibition of macrophyte on phytoplankton bloom. Science of Total Environment 579: 871–880.CrossRefGoogle Scholar
  13. Fan, Z., R. M. Han, J. Ma & G. X. Wang, 2016. Submerged macrophytes shape the abundance and diversity of bacterial denitrifiers in bacterioplankton and epiphyton in the Shallow Fresh Lake Taihu, China. Environmental Science and Pollution Research 23: 14102–14114.CrossRefGoogle Scholar
  14. Declerck, S., J. Vandekerkhove, L. Johansson, K. Muylaert, J. M. Conde-Porcuna, K. Van Der Gucht, C. Pérez-Martíez, T. Lauridsen, K. Schwenk, G. Zwart, W. Rommens, J. López-Romos, E. Jeppesen, W. Vyverman, L. Brendonck & L. De Meester, 2005. Multi-group biodiversity in shallow lakes along gradients of phosphorus and water plant cover. Ecology 86: 1905–1915.CrossRefGoogle Scholar
  15. Gordon-Bradley, N., D. S. Lymperopoulou & H. N. Williams, 2014. Differences in bacterial community structure on Hydrilla verticillata and Vallisneria americana in a freshwater spring. Microbes and environments 29: 67–73.CrossRefGoogle Scholar
  16. Gordon-Bradley, N., N. Li & H. N. Williams, 2015. Bacterial community structure in freshwater springs infested with the invasive plant species Hydrilla verticillata. Hydrobiologia 742: 221–232.CrossRefGoogle Scholar
  17. Gross, E. M., D. Erhard & E. Iványi, 2003. Allelopathic activity of Ceratophyllum demersum L. and Najas marina ssp. intermedia (Wolfgang) Casper. Hydrobiologia 506: 583–589.CrossRefGoogle Scholar
  18. He, D., L. Ren & Q. L. Wu, 2014. Contrasting diversity of epibiotic bacteria and surrounding bacterioplankton of a common submerged macrophyte, Potamogeton crispus, in freshwater lakes. FEMS microbiology ecology 90: 551–562.CrossRefGoogle Scholar
  19. Hempel, M., H. P. Grossart & E. M. Gross, 2009. Community composition of bacterial biofilms on two submerged macrophytes and an artificial substrate in a pre-alpine lake. Aquatic Microbial Ecology 58: 79–94.CrossRefGoogle Scholar
  20. Herrmann, M., A. M. Saunders & A. Schramm, 2009. Effect of lake trophic status and rooted macrophytes on community composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments. Applied and Environmental Microbiology 75: 3127–3136.CrossRefGoogle Scholar
  21. Hilt, S., 2015. Regime shifts between macrophytes and phytoplankton – concepts beyond shallow lakes, unravelling stabilizing mechanisms and practical consequences. Limnetica 34: 467–480.Google Scholar
  22. Ju, F. & T. Zhang, 2015. 16S rRNA gene high-throughput sequencing data mining of microbial diversity and interactions. Applied Microbiology and Biotechnology 99: 4119–4129.CrossRefGoogle Scholar
  23. Kirchman, D. L., 2002. The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiology Ecology 39: 91–100.Google Scholar
  24. Kirschner, A. K. T. & B. Velimirov, 1997. A seasonal study of bacterial community succession in a temperate backwater system, indicated by variation in morphotype numbers, biomass, and secondary production. Microbial Ecology 34: 27–38.CrossRefGoogle Scholar
  25. Kurtz, J. C., D. F. Yates, J. M. Macauley, R. L. Quarles, F. J. Genthner, C. A. Chancy & R. Devereux, 2003. Effects of light reduction on growth of the submerged macrophyte Vallisneria americana and the community of root-associated heterotrophic bacteria. Journal of Experimental Marine Biology and Ecology 291: 199–218.CrossRefGoogle Scholar
  26. Levi, P. S., P. Starnawski, B. Poulsen, A. Baattrup-Pedersen, A. Schramm & T. Riis, 2017. Microbial community diversity and composition varies with habitat characteristics and biofilm function in macrophyte-rich streams. Oikos 126: 398–409.CrossRefGoogle Scholar
  27. Lewicka-Rataj, K., A. Świątecki & D. Górniak, 2018. The effect of Lobelia dortmanna L. on the structure and bacterial activity of the rhizosphere. Aquatic Botany 145: 10–20.CrossRefGoogle Scholar
  28. Marschner, P. & S. Timonen, 2005. Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Applied Soil Ecology 28: 23–36.CrossRefGoogle Scholar
  29. Metzker, M. L., 2010. Sequencing technologies - the next generation. Nature Reviews Genetics 11: 31–46.CrossRefGoogle Scholar
  30. Murphy, J. & J. P. Riley, 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27: 31–36.CrossRefGoogle Scholar
  31. Murray, R. E. & R. E. Hodson, 1986. Influence of macrophyte decomposition on growth rate and community structure of Okefenokee Swamp bacterioplankton. Applied and environmental microbiology 51: 293–301.Google Scholar
  32. National Bureau of Environment Protection Editorial Committee of Water and Wastewater Monitoring Analytical Methods, 2002. Water and wastewater monitoring analysis method, 4th ed. Chinese Environment Science Press, Beijing, China.Google Scholar
  33. Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, E. Szoecs & H. Wagner, 2013. Vegan: Community Ecology Package.Google Scholar
  34. Pang, S., S. Zhang, X. Lv, B. Han, K. Liu, C. Qiu, C. Wang, P. Wang, H. Toland & Z. He, 2016. Characterization of bacterial community in biofilm and sediments of wetlands dominated by aquatic macrophytes. Ecological Engineering 97: 242–250.CrossRefGoogle Scholar
  35. Peralta, R. M., C. Ahn & P. M. Gillevet, 2012. Characterization of soil bacterial community structure and physicochemical properties in created and natural wetlands. Science of Total Environment 443: 725–732.CrossRefGoogle Scholar
  36. Qiu, D. R., Z. B. Wu, B. Y. Liu, J. Q. Deng, G. P. Fu & F. He, 2001. The restoration of aquatic macrophytes for improving water quality in a hypertrophic shallow lake in Hubei Province, China. Ecological Engineering 18: 147–156.CrossRefGoogle Scholar
  37. R Development Core Team, 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  38. Redford, A. J., R. M. Bowers, R. Knight, Y. Linhart & N. Fierer, 2010. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environmental Microbiology 12: 2885–2893.CrossRefGoogle Scholar
  39. Ruban, V., J. F. Lópea-Sánchez, P. Pardo, G. Rauret, H. Muntau & P. Quevauviller, 1999. Selection and evaluation of sequential extraction procedures for the determination of phosphorus forms in lake sediment. Journal of Environmental Monitoring 1: 51–56.CrossRefGoogle Scholar
  40. Segata, N., J. Izard, L. Waldron, D. Gevers, L. Miropolsky, W. S. Garrett & C. Huttenhower, 2011. Metagenomic biomarker discovery and explanation. Genome Biology 12: R60.CrossRefGoogle Scholar
  41. Shao, K. Q., G. Gao, B. Q. Qin, X. M. Tang, Y. P. Wang, K. X. Chi & J. Y. Dai, 2011. Comparing sediment bacterial communities in the macrophyte-dominated and algae-dominated areas of eutrophic Lake Taihu, China. Candian Journal of Microbiology 57: 263–272.CrossRefGoogle Scholar
  42. Srivastava, J., A. Gupta & H. Chandra, 2008. Managing water quality with aquatic macrophytes. Reviews in Environmental Science Biotechnology 7: 255–266.CrossRefGoogle Scholar
  43. Stepanauskas, R., M. A. Moran, B. A. Bergamaschi & J. T. Hollibaugh, 2003. Covariance of bacterioplankton composition and environmental variables in a temperate delta system. Aquatic Microbial Ecology 31: 85–98.CrossRefGoogle Scholar
  44. Søndergaard, M., L. S. Johansson, T. L. Lauridsen, T. L. Jørgensen, L. Liboriussen & E. Jeppesen, 2010. Submerged macrophytes as indicators of the ecological quality of lakes. Freshwater Biology 55: 893–908.CrossRefGoogle Scholar
  45. Van der Gucht, K., T. Vandekerckhove, V. Nele, S. Cousin, K. Muylaet, K. Sabbe, M. Gillis, S. Declerk, L. De Meester & W. Vyverman, 2005. Characterization of bacterial communities in four freshwater lakes differing in nutrient load and food web structure. FEMS Microbiology Ecology 53: 205–220.CrossRefGoogle Scholar
  46. van Donk, E. & W. J. van de Bund, 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: 261–274.CrossRefGoogle Scholar
  47. Vermaire, J. C., Y. T. Prairie & I. Gregory-Eaves, 2011. The influence of submerged macrophytes on sedimentary diatom assemblages. Journal of Applied Phycology 47: 1230–1240.CrossRefGoogle Scholar
  48. Waters, M. N., C. L. Schelske & M. Brenner, 2015. Cyanobacterial dynamics in shallow Lake Apopka (Florida, U.S.A.) before and after the shift from a macrophyte-dominated to a phytoplankton-dominated state. Freshwater Biology 60: 1571–1580.CrossRefGoogle Scholar
  49. Wu, Q. L., G. Zwart, J. F. Wu, M. P. Kamst-van Agterveld, S. J. Liu & M. W. Hahn, 2007. Submersed macrophytes play a key role in structuring bacterioplankton community composition in the large, shallow, subtropical Taihu Lake, China. Environmental Microbiology 9: 2765–2774.CrossRefGoogle Scholar
  50. Xian, Q., H. Chen, H. Liu, H. Zou & D. Yin, 2006a. Isolation and Identification of Antialgal Compounds from the Leaves of Vallisneria spiralis L. by Activity-Guided Fractionation (5 pp). Environmental Science and Pollution Research 13: 233–237.CrossRefGoogle Scholar
  51. Xian, Q., H. Chen, H. Zou & D. Yin, 2006b. Allelopathic activity of volatile substance from submerged macrophytes on Microcystin aeruginosa. Acta Ecologica Sinica 26: 3549–3554.CrossRefGoogle Scholar
  52. Xie, W. Y., J. Q. Su & Y. G. Zhu, 2015. Phyllosphere bacterial community of floating macrophytes in paddy soil environments as revealed by Illumina High-Throughput sequencing. Applied and Environmental Microbiology 81: 522–532.CrossRefGoogle Scholar
  53. Zeng, J., Y. Q. Bian, P. Xing & Q. L. Wu, 2012. Macrophyte species drive the variation of bacterioplankton community composition in a shallow freshwater lake. Applied and Environmental Microbiology 78: 177–184.CrossRefGoogle Scholar
  54. Zhang, C. H., S. F. Li, L. Yang, P. Huang, W. J. Li, S. Y. Wang, G. P. Zhao, M. H. Zhang, X. Y. Pang, Z. Yan, Y. Liu & L. P. Zhao, 2013. Structural modulation of gut microbiota in life-long calorie-restricted mice. Nature Communication 4: 2163.CrossRefGoogle Scholar
  55. Zhao, D. Y., P. Liu, C. Fang, Y. M. Sun, J. Zeng, J. Q. Wang, T. Ma, Y. H. Xiao & Q. L. Wu, 2013. Submerged macrophytes modify bacterial community composition in sediments in a large, shallow, freshwater lake. Canadian Journal of Microbiology 59: 237–244.CrossRefGoogle Scholar
  56. Zhao, D., S. Wang, R. Huang, J. Zeng, F. Huang & Z. Yu, 2017. Diversity and composition of bacterial community in the rhizosphere sediments of submerged macrophytes revealed by 454 pyrosequencing. Annals of Microbiology 67: 313–319.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of HydrobiologyChinese Academy of SciencesWuhanChina
  2. 2.Key Laboratory of Yangtze River Water Environment, Ministry of EducationTongji UniversityShanghaiChina

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