Skip to main content
Log in

Effects of Planted Versus Naturally Growing Vallisneria natans on the Sediment Microbial Community in West Lake, China

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Submerged macrophytes play an important role in aquatic ecosystems, which has led to an increase in studies on vegetation recovery in polluted lakes from which submerged macrophytes have disappeared. The comparison of microbial communities in sediment cloned with planted and naturally growing submerged macrophytes is an interesting but rarely studied topic. In this investigation, Maojiabu and Xilihu, two adjacent sublakes of West Lake (Hangzhou, China), were selected as aquatic areas with planted and naturally growing macrophytes, respectively. Sediment samples from sites with/without Vallisneria natans were collected from both sublakes. The results showed that sediment total nitrogen and organic matter were significantly lower in the plant-covered sites than that in the non-plant sites in Maojiabu. Additionally, the sediment microbial community characterized by 16S ribosomal RNA (rRNA) sequencing differed more significantly for Maojiabu than for Xilihu. The relative abundances of microbes involved in C, N, and S elemental cycling were significantly higher in the sediments with plants than in those without. Results from both fatty acid methyl ester analysis and 16S rRNA sequencing indicated that vegetation significantly influenced the sulfate-reducing bacteria (SRB). Thus, the gene copies and composition of SRB were explored further. The relative gene abundance of SRB was 66% higher with natural vegetation colonization but was not influenced by artificial colonization. An increase in dominant SRB members from the families Syntrophobacteraceae and Thermodesulfovibrionaceae contributed to the increase of total SRB. Thus, macrophyte planting influences sediment nutrient levels and microbial community more than natural growth does, whereas the latter is more beneficial to sediment SRB.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Rodrigo MA, Rojo C, Alonso-Guillen JL, Vera P (2013) Restoration of two small Mediterranean lagoons: the dynamics of submerged macrophytes and factors that affect the success of revegetation. Ecol. Eng. 54:1–15. doi:10.1016/j.ecoleng.2013.01.022

    Article  Google Scholar 

  2. Sondergaard M, Johansson LS, Lauridsen TL, Jorgensen TB, Liboriussen L, Jeppesen E (2010) Submerged macrophytes as indicators of the ecological quality of lakes. Freshw. Biol. 55(4):893–908. doi:10.1111/j.1365-2427.2009.02331.x

    Article  Google Scholar 

  3. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413(6856):591–596. doi:10.1038/35098000

    Article  CAS  PubMed  Google Scholar 

  4. Sand-Jensen K, Pedersen NL, Thorsgaard I, Moeslund B, Borum J, Brodersen KP (2008) 100 years of vegetation decline and recovery in Lake Fure, Denmark. J. Ecol. 96(2):260–271. doi:10.1111/j.1365-2745.2007.01339.x

    Article  Google Scholar 

  5. Hilt S, Van de Weyer K, Koehler A, Chorus I (2010) Submerged macrophyte responses to reduced phosphorus concentrations in two peri-urban lakes. Restor. Ecol. 18:452–461. doi:10.1111/j.1526-100X.2009.00577.x

    Article  Google Scholar 

  6. Korner S (2002) Loss of submerged macrophytes in shallow lakes in north-eastern Germany. Int. Rev. Hydrobiol. 87(4):375–384. doi:10.1002/1522-2632(200207)87:4<375::aid-iroh375>3.0.co;2-7

    Article  Google Scholar 

  7. Lauridsen TL, Jensen JP, Jeppesen E, Sondergaard M (2003) Response of submerged macrophytes in Danish lakes to nutrient loading reductions and biomanipulation. Hydrobiologia 506(1–3):641–649. doi:10.1023/b:hydr.0000008633.17385.70

    Article  Google Scholar 

  8. Hilt S, Gross EM, Hupfer M, Morscheid H, Mahlmann J, Melzer A, Poltz J, Sandrock S, Scharf EM, Schneider S, de Weyer KV (2006) Restoration of submerged vegetation in shallow eutrophic lakes—a guideline and state of the art in Germany. Limnologica 36(3):155–171. doi:10.1016/j.limno.2006.06.001

    Article  CAS  Google Scholar 

  9. Sondergaard M, Jeppesen E, Lauridsen TL, Skov C, Van Nes EH, Roijackers R, Lammens E, Portielje R (2007) Lake restoration: successes, failures and long-term effects. J. Appl. Ecol. 44(6):1095–1105. doi:10.1111/j.1365-2664.2007.01363.x

    Article  Google Scholar 

  10. Chen K-N, Bao C-H, Zhou W-P (2009) Ecological restoration in eutrophic Lake Wuli: a large enclosure experiment. Ecol. Eng. 35(11):1646–1655. doi:10.1016/j.ecoleng.2008.10.009

    Article  Google Scholar 

  11. Gulati RD, Pires LMD, Van Donk E (2008) Lake restoration studies: failures, bottlenecks and prospects of new ecotechnological measures. Limnologica 38(3–4):233–247. doi:10.1016/j.limno.2008.05.008

    Article  CAS  Google Scholar 

  12. Liao CZ, Luo YQ, Fang CM, Chen JK, Li B (2012) The effects of plantation practice on soil properties based on the comparison between natural and planted forests: a meta-analysis. Glob. Ecol. Biogeogr. 21(3):318–327. doi:10.1111/j.1466-8238.2011.00690.x

    Article  Google Scholar 

  13. Vitali F, Mastromei G, Senatore G, Caroppo C, Casalone E (2016) Long lasting effects of the conversion from natural forest to poplar plantation on soil microbial communities. Microbiol. Res. 182:89–98. doi:10.1016/j.micres.2015.10.002

    Article  PubMed  Google Scholar 

  14. Lin YT, Hu HW, Whitman WB, Coleman DC, Chiu CY (2014) Comparison of soil bacterial communities in a natural hardwood forest and coniferous plantations in perhumid subtropical low mountains. Bot. Stud. 55:9. doi:10.1186/s40529-014-0050-x

    Article  Google Scholar 

  15. Heilmayr R (2014) Conservation through intensification? The effects of plantations on natural forests. Ecol. Econ. 105:204–210. doi:10.1016/j.ecolecon.2014.06.008

    Article  Google Scholar 

  16. Espinar JL (2006) Sample size and the detection of a hump-shaped relationship between biomass and species richness in Mediterranean wetlands. J. Veg. Sci. 17(2):227–232. doi:10.1111/j.1654-1103.2006.tb02441.x

    Article  Google Scholar 

  17. Costantini ML, Rossi L, Fazi S, Rossi D (2009) Detritus accumulation and decomposition in a coastal lake (Acquatina-southern Italy). Aquat. Conserv. 19(5):566–574. doi:10.1002/aqc.1004

    Article  Google Scholar 

  18. Cornwell JC, Owens MS (2011) Quantifying sediment nitrogen releases associated with estuarine dredging. Aquat. Geochem. 17(4–5):499–517. doi:10.1007/s10498-011-9139-y

    Article  CAS  Google Scholar 

  19. Li H, Song CL, Cao XY, Zhou YY (2016) The phosphorus release pathways and their mechanisms driven by organic carbon and nitrogen in sediments of eutrophic shallow lakes. Sci. Total Environ. 572:280–288. doi:10.1016/j.scitotenv.2016.07.221

    Article  CAS  PubMed  Google Scholar 

  20. Obi CC, Adebusoye SA, Ugoji EO, Ilori MO, Amund OO, Hickey WJ (2016) Microbial communities in sediments of Lagos lagoon, Nigeria: elucidation of community structure and potential impacts of contamination by municipal and industrial wastes. Front. Microbiol. 7:16. doi:10.3389/fmicb.2016.01213

    Article  Google Scholar 

  21. Schutter ME, Dick RP (2000) Comparison of fatty acid methyl ester (FAME) methods for characterizing microbial communities. Soil Sci. Soc. Am. J. 64(5):1659–1668

    Article  CAS  Google Scholar 

  22. Geets J, Borrernans B, Diels L, Springael D, Vangronsveld J, van der Lelie D, Vanbroekhoven K (2006) DsrB gene-based DGGE for community and diversity surveys of sulfate-reducing bacteria. J. Microbiol. Methods 66(2):194–205. doi:10.1016/j.mimet.2005.11.002

    Article  CAS  PubMed  Google Scholar 

  23. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8(4):790–803. doi:10.1038/ismej.2013.196

    Article  CAS  PubMed  Google Scholar 

  24. Leon JD, Gonzalez MI, Gallardo JF (2011) Biogeochemical cycles in natural forest and conifer plantations in the high mountains of Colombia. Rev. Biol. Trop. 59(4):1883–1894

    PubMed  Google Scholar 

  25. Yang K, Zhu JJ, Zhang M, Yan QL, Sun OJ (2010) Soil microbial biomass carbon and nitrogen in forest ecosystems of Northeast China: a comparison between natural secondary forest and larch plantation. J. Plant Ecol. 3(3):175–182. doi:10.1093/jpe/rtq022

    Article  Google Scholar 

  26. da Silva DKA, Freitas ND, de Souza RG, da Silva FSB, de Araujo ASF, Maia LC (2012) Soil microbial biomass and activity under natural and regenerated forests and conventional sugarcane plantations in Brazil. Geoderma 189:257–261. doi:10.1016/j.geoderma.2012.06.014

    Article  Google Scholar 

  27. Song K, Harper WF, Hori T, Riya S, Hosomi M, Terada A (2015) Impact of carbon sources on nitrous oxide emission and microbial community structure in an anoxic/oxic activated sludge system. Clean Techn. Environ. Policy 17(8):2375–2385. doi:10.1007/s10098-015-0979-9

    Article  CAS  Google Scholar 

  28. Kindaichi T, Yuri S, Ozaki N, Ohashi A (2012) Ecophysiological role and function of uncultured Chloroflexi in an anammox reactor. Water Sci. Technol. 66(12):2556–2561. doi:10.2166/wst.2012.479

    Article  CAS  PubMed  Google Scholar 

  29. Simek K, Nedoma J, Znachor P, Kasalicky V, Jezbera J, Hornak K, Sed’a J (2014) A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring. Limnol. Oceanogr. 59(5):1477–1492. doi:10.4319/lo.2014.59.5.1477

    Article  CAS  Google Scholar 

  30. Wang Z, Yang YY, Sun WM, Xie SG, Liu Y (2014) Nonylphenol biodegradation in river sediment and associated shifts in community structures of bacteria and ammonia-oxidizing microorganisms. Ecotox Environ Safe 106:1–5. doi:10.1016/j.ecoenv.2014.04.019

    Article  CAS  Google Scholar 

  31. Liang SH, Liu JK, Lee KH, Kuo YC, Kao CM (2011) Use of specific gene analysis to assess the effectiveness of surfactant-enhanced trichloroethylene cometabolism. J. Hazard. Mater. 198:323–330. doi:10.1016/j.jhazmat.2011.10.050

    Article  CAS  PubMed  Google Scholar 

  32. Holmer M, Storkholm P (2001) Sulphate reduction and sulphur cycling in lake sediments: a review. Freshw. Biol. 46(4):431–451. doi:10.1046/j.1365-2427.2001.00687.x

    Article  CAS  Google Scholar 

  33. Zhang W, Zhang L (2016) Vertical and temporal distributions of sulfate-reducing bacteria in sediments of Lake Erhai, Yunnan Province, China. Earth and Environment (in Chinese) 44(2):177–184

    Google Scholar 

  34. Wang MY, Liang XB, Yuan XY, Zhang W, Zeng J (2008) Analyses of the vertical and temporal distribution of sulfate-reducing bacteria in Lake Aha (China). Environ. Geol. 54(1):1–6. doi:10.1007/s00254-007-0787-6

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  36. Acha D, Iniguez V, Roulet M, Guimaraes JRD, Luna R, Alanoca L, Sanchez S (2005) Sulfate-reducing bacteria in floating macrophyte rhizospheres from an Amazonian floodplain lake in Bolivia and their association with Hg methylation. Appl. Environ. Microbiol. 71(11):7531–7535. doi:10.1128/aem.71.11.7531-7535.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Marietou A (2016) Nitrate reduction in sulfate-reducing bacteria. FEMS Microbiol. Lett. 363(15). doi:10.1093/femsle/fnw155

  38. Blumenberg M, Hoppert M, Krueger M, Dreier A, Thiel V (2012) Novel findings on hopanoid occurrences among sulfate reducing bacteria: is there a direct link to nitrogen fixation? Org. Geochem. 49:1–5. doi:10.1016/j.orggeochem.2012.05.003

    Article  CAS  Google Scholar 

  39. Fernandez ML, Granados-Chinchilla F, Rodriguez C (2015) A single exposure of sediment sulphate-reducing bacteria to oxytetracycline concentrations relevant to aquaculture enduringly disturbed their activity, abundance and community structure. J. Appl. Microbiol. 119(2):354–364. doi:10.1111/jam.12846

    Article  CAS  PubMed  Google Scholar 

  40. Varon-Lopez M, Franco Dias AC, Fasanella CC, Durrer A, Melo IS, Kuramae EE, Andreote FD (2014) Sulphur-oxidizing and sulphate-reducing communities in Brazilian mangrove sediments. Environ. Microbiol. 16(3):845–855. doi:10.1111/1462-2920.12237

    Article  CAS  PubMed  Google Scholar 

  41. Zeleke J, Lu S-L, Wang J-G, Huang J-X, Li B, Ogram AV, Quan Z-X (2013) Methyl coenzyme M reductase a (mcrA) gene-based investigation of methanogens in the mudflat sediments of Yangtze River estuary, China. Microb. Ecol. 66(2):257–267. doi:10.1007/s00248-012-0155-2

    Article  CAS  PubMed  Google Scholar 

  42. Besaury L, Ouddane B, Pavissich JP, Dubrulle-Brunaud C, Gonzalez B, Quillet L (2012) Impact of copper on the abundance and diversity of sulfate-reducing prokaryotes in two chilean marine sediments. Mar. Pollut. Bull. 64(10):2135–2145. doi:10.1016/j.marpolbul.2012.07.042

    Article  CAS  PubMed  Google Scholar 

  43. He H, Zhen Y, Mi T, Xu B, Wang G, Zhang Y, Yu Z (2015) Community composition and distribution of sulfate- and sulfite-reducing prokaryotes in sediments from the Changjiang estuary and adjacent East China Sea. Coast Shelf Sci 165:75–85. doi:10.1016/j.ecss.2015.09.005

    Article  CAS  Google Scholar 

  44. Vladar P, Rusznyak A, Marialigeti K, Borsodi AK (2008) Diversity of sulfate-reducing bacteria inhabiting the rhizosphere of Phragmites australis in lake velencei (Hungary) revealed by a combined cultivation-based and molecular approach. Microb. Ecol. 56(1):64–75. doi:10.1007/s00248-007-9324-0

    Article  CAS  PubMed  Google Scholar 

  45. Cifuentes A, Anton J, de Wit R, Rodriguez-Valera F (2003) Diversity of Bacteria and Archaea in sulphate-reducing enrichment cultures inoculated from serial dilution of Zostera noltii rhizosphere samples. Environ. Microbiol. 5(9):754–764. doi:10.1046/j.1470-2920.2003.00470.x

    Article  CAS  PubMed  Google Scholar 

  46. Muyodi FJ, Rubindamayugi MST, Semesi AK (2004) Effect of water hyacinth on distribution of sulphate-reducing bacteria in sediments of Lake Victoria. Water SA 30(3):421–425

    Article  CAS  Google Scholar 

  47. Nie M, Wang M, Li B (2009) Effects of salt marsh invasion by Spartina alterniflora on sulfate-reducing bacteria in the Yangtze River estuary, China. Ecol. Eng. 35(12):1804–1808. doi:10.1016/j.ecoleng.2009.08.002

    Article  Google Scholar 

  48. Cypionka H (2000) Oxygen respiration by Desulfovibrio species. Annu. Rev. Microbiol. 54:827–848. doi:10.1146/annurev.micro.54.1.827

    Article  CAS  PubMed  Google Scholar 

  49. Plugge CM, Zhang W, Scholten JCM, Stams AJM (2011) Metabolic flexibility of sulfate-reducing bacteria. Front. Microbiol. 2. doi:10.3389/fmicb.2011.00081

  50. Ibelings BW, Portielje R, Lammens E, Noordhuis R, van den Berg MS, Joosse W, Meijer ML (2007) Resilience of alternative stable states during the recovery of shallow lakes from eutrophication: Lake Veluwe as a case study. Ecosystems 10(1):4–16. doi:10.1007/s10021-006-9009-4

    Article  CAS  Google Scholar 

  51. van Altena C, Bakker ES, Kuiper JJ, Mooij WM (2016) The impact of bird herbivory on macrophytes and the resilience of the clear-water state in shallow lakes: a model study. Hydrobiologia 777(1):197–207. doi:10.1007/s10750-016-2779-6

    Article  Google Scholar 

  52. Gunderson LH (2000) Ecological resilience—in theory and application. Ann Rev Ecol Syst 31:425–439. doi:10.1146/annurev.ecolsys.31.1.425

    Article  Google Scholar 

  53. Hou EQ, Wen DZ, Li JL, Zuo WD, Zhang LL, Kuang YW, Li J (2012) Soil acidity and exchangeable cations in remnant natural and plantation forests in the urbanised Pearl River Delta, China. Soil Res 50(3):207–215. doi:10.1071/sr11344

    Article  CAS  Google Scholar 

  54. Sharma G, Pandey RR, Singh MS (2011) Microfungi associated with surface soil and decaying leaf litter of Quercus serrata in a subtropical natural oak forest and managed plantation in Northeastern India. Afr. J. Microbiol. Res. 5(7):777–787. doi:10.5897/AJMR10.621

    Article  Google Scholar 

  55. Martinez-Jauregui M, Diaz M, de Ron DS, Solino M (2016) Plantation or natural recovery? Relative contribution of planted and natural pine forests to the maintenance of regional bird diversity along ecological gradients in Southern Europe. For. Ecol. Manag. 376:183–192. doi:10.1016/j.foreco.2016.06.021

    Article  Google Scholar 

Download references

Acknowledgements

We thank Zhigang Dai, Jian Sun, and Fenli Min for the sediment sample collection on the lake. This study was supported by the Major Science and Technology Program for Water Pollution Control and Treatment of China 12th Five-Year Plan (No. 2012ZX07101007-005) and the Key Research Program of the Chinese Academy of Sciences (No. KFZD-SW-302-02).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qiaohong Zhou.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Chuan Wang and Shuangyuan Liu are co-first authors of this paper.

Electronic Supplementary Material

ESM 1

(DOCX 353 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, C., Liu, S., Zhang, Y. et al. Effects of Planted Versus Naturally Growing Vallisneria natans on the Sediment Microbial Community in West Lake, China. Microb Ecol 74, 278–288 (2017). https://doi.org/10.1007/s00248-017-0951-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-0951-9

Keywords

Navigation