Environmental Science and Pollution Research

, Volume 25, Issue 26, pp 26550–26561 | Cite as

Bio-cord plays a similar role as submerged macrophytes in harboring bacterial assemblages in an eco-ditch

  • Lei Zhou
  • Chengrong Bai
  • Jian Cai
  • Yang Hu
  • Keqiang Shao
  • Guang Gao
  • Erik Jeppesen
  • Xiangming TangEmail author
Research Article


Artificial carriers are widely used to enhance the formation of biofilm and improve pollutants’ removal efficiency in agricultural wastewater treatment ditches (eco-ditches), yet comprehensive insight into their bacterial community is scarce. In this study, bacterial diversities in four different habitats—the water column, surface sediments, submerged macrophytes (Myriophyllum verticillatum L.), and the artificial carriers (bio-cord)—were compared in a Chinese eco-ditch. Comparable richness and evenness of bacterial communities were observed on M. verticillatum and bio-cord, both being higher than for free-living bacteria in the water column but lower than for bacteria in the surface sediment. The highest similarity of bacterial community composition and structure also occurred between M. verticillatum and the bio-cord, dominated by α- and γ-proteobacteria, Verrucomicrobia, and Bacteroidetes. Firmicutes and Planctomycetes, respectively, were the exclusive abundant phyla in M. verticillatum and the bio-cord, probably indicating the unique interaction between M. verticillatum and their epiphytic bacteria. Some abundant genera, such as Roseomonas, Pseudomonas, and Rhodopirellula, which were exclusively observed in M. verticillatum or the bio-cord, have been reported to have the same capacity to remove nitrogen and organic matter in wastewater treatment systems. In conclusion, in the studied eco-ditch, the bio-cord was found to play a similar role as submerged macrophytes in harboring bacterial assemblages, and we therefore propose that bio-cord may be a good alternative or supplement to enhance wastewater treatment in agricultural ditches.


Ecological ditch system Artificial carrier Myriophyllum verticillatum L. Biofilm bacterial community 



This work was supported by National Natural Science Foundation of China (41471040, 41501101, 41571462, and 41621002), Key Research Program of Frontier Sciences, CAS (QYZDJ-SSW-DQC008), and the National Water Pollution Control and Management of Science and Technology Major Projects (grant no. 2017ZX07203-004). Erik Jeppesen was supported by the MARS project (Managing Aquatic ecosystems and water Resources under multiple Stress) funded under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), Contract No. 603378 ( We would like to express our deep thanks to Anne Mette Poulsen from Aarhus University for editorial assistance. We are grateful to the staff at the Institute of Lake Bosten of the Environmental Protection Bureau of Bayingolin Mongolia Autonomous Prefecture for their help with sample collection and water chemical analyses. The authors are grateful to the anonymous reviewers for their useful comments on this manuscript.

Supplementary material

11356_2018_2697_MOESM1_ESM.pdf (285 kb)
ESM 1 (PDF 285 kb)


  1. Acinas SG, Antón J, Rodríguezvalera F (1999) Diversity of free-living and attached bacteria in offshore western Mediterranean waters as depicted by analysis of genes encoding 16S rRNA. Appl Environ Microbiol 65:514–522Google Scholar
  2. Andersson S, Kuttuva Rajarao G, Land CJ, Dalhammar G (2008) Biofilm formation and interactions of bacterial strains found in wastewater treatment systems. FEMS Microbiol Lett 283:83–90CrossRefGoogle Scholar
  3. Araya R, Tani K, Takagi T, Yamaguchi N, Nasu M (2003) Bacterial activity and community composition in stream water and biofilm from an urban river determined by fluorescent in situ hybridization and DGGE analysis. FEMS Microbiol Ecol 43:111–119CrossRefGoogle Scholar
  4. Ateia M (2016) In-situ biological water treatment technologies for environmental remediation: a review. J Bioremed Biodeg 07:348CrossRefGoogle Scholar
  5. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011a) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci 108:14288–14293CrossRefGoogle Scholar
  6. Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S (2011b) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5:590–600CrossRefGoogle Scholar
  7. Cai X, Gao G, Tang X, Dong B, Dai J, Chen D, Song Y (2013) The response of epiphytic microbes to habitat and growth status of Potamogeton malaianus Miq. in Lake Taihu. J Basic Microbiol 53:828–837Google Scholar
  8. Cai X, Gao G, Yang J, Tang X, Dai J, Chen D, Song Y (2014) An ultrasonic method for separation of epiphytic microbes from freshwater submerged macrophytes. J Basic Microbiol 54:758–761CrossRefGoogle Scholar
  9. Cai J, Gao G, Shao K, Bai C (2017) Restoration of agriculture non-point source pollution and arid-semiarid areas by biological rope technology in situ: taking agricultural wastewater in Lake Bosten catchment as example. Environ Eng 35:20–25 (In Chinese)Google Scholar
  10. Campbell BJ, Engel AS, Porter ML, Takai K (2006) The versatile ε-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468CrossRefGoogle Scholar
  11. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624CrossRefGoogle Scholar
  12. Cattaneo A, Kalff J (1978) Seasonal changes in the epiphyte community of natural and artificial macrophytes in Lake Memphremagog (Que. & Vt.). Hydrobiologia 60:135–144CrossRefGoogle Scholar
  13. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270Google Scholar
  14. Chen CL, Maki JS, Dan R, Teo LM (2013) Early marine bacterial biofilm on a copper-based antifouling paint. Int Biodeterior Biodegrad 83:71–76CrossRefGoogle Scholar
  15. Chen L, Liu F, Wang Y, Li X, Zhang S, Li Y, Wu J (2015) Nitrogen removal in an ecological ditch receiving agricultural drainage in subtropical Central China. Ecol Eng 82:487–492CrossRefGoogle Scholar
  16. Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog 92:205–219CrossRefGoogle Scholar
  17. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulamsyedmohideen AS, Mcgarrell DM, Marsh T, Garrity GM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145CrossRefGoogle Scholar
  18. Cottrell MT, Waidner LA, Yu L, Kirchman DL (2005) Bacterial diversity of metagenomic and PCR libraries from the Delaware River. Environ Microbiol 7:1883–1895CrossRefGoogle Scholar
  19. Dhote S, Dixit S (2009) Water quality improvement through macrophytes—a review. Environ Monit Assess 152:149–153CrossRefGoogle Scholar
  20. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefGoogle Scholar
  21. Edgar RC, Haas BJ, Clemente JC, Christopher Q, Rob K (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefGoogle Scholar
  22. Fadrosh DW, Bing M, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J (2014) An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2:6CrossRefGoogle Scholar
  23. Faith DP (2006) The role of the phylogenetic diversity measure, PD, in bio-informatics: getting the definition right. Evol Bioinformatics Online 2:277–283Google Scholar
  24. Feng L, Chen K, Han D, Zhao J, Lu Y, Yang G, Mu J, Zhao X (2016) Comparison of nitrogen removal and microbial properties in solid-phase denitrification systems for water purification with various pretreated lignocellulosic carriers. Bioresour Technol 224–236Google Scholar
  25. Feng LJ, Mu J, Sun JY, Kong Y, Wang J, Lv ZH, Zhu L, Xu XY, Yang GF (2017) Kinetic characteristics and bacterial structures in biofilm reactors with pre-cultured biofilm for source water pretreatment. Int Biodeterior Biodegrad 121:26–34CrossRefGoogle Scholar
  26. Guan W, Yin M, He T, Xie S (2015) Influence of substrate type on microbial community structure in vertical-flow constructed wetland treating polluted river water. Environ Sci Pollut Res Int 22:16202–16209CrossRefGoogle Scholar
  27. Gulay A, Musovic S, Albrechtsen HJ, Al-Soud WA, Sorensen SJ, Smets BF (2016) Ecological patterns, diversity and core taxa of microbial communities in groundwater-fed rapid gravity filters. ISME J 10:1–14CrossRefGoogle Scholar
  28. Haichar FZ, 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 2:1221–1230CrossRefGoogle Scholar
  29. Hao B, Wu H, Cao Y, Xing W, Jeppesen E, Li W (2017) Comparison of periphyton communities on natural and artificial macrophytes with contrasting morphological structures. Freshw Biol 62:1783–1793CrossRefGoogle Scholar
  30. He T, Guan W, Luan Z, Xie S (2015) Spatiotemporal variation of bacterial and archaeal communities in a pilot-scale constructed wetland for surface water treatment. Appl Microbiol Biotechnol 100:1479–1488CrossRefGoogle Scholar
  31. Hempel M, Blume M, Blindow I, Gross EM (2008) Epiphytic bacterial community composition on two common submerged macrophytes in brackish water and freshwater. BMC Microbiol 8:58CrossRefGoogle Scholar
  32. Hempel M, Grossart HP, Gross EM (2009) Community composition of bacterial biofilms on two submerged macrophytes and an artificial substrate in a pre-alpine lake. Aquat Microb Ecol 58:79–94CrossRefGoogle Scholar
  33. Holmfeldt K, Dziallas C, Titelman J, Pohlmann K, Grossart HP, Riemann L (2009) Diversity and abundance of freshwater Actinobacteria along environmental gradients in the brackish northern Baltic Sea. Environ Microbiol 11:2042–2054CrossRefGoogle Scholar
  34. Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl Environ Microbiol 72:3832–3845CrossRefGoogle Scholar
  35. Jiang XT, Peng X, Deng GH, Sheng HF, Wang Y, Zhou HW, Tam NF (2013) Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb Ecol 66:96–104CrossRefGoogle Scholar
  36. Jones PR, Cottrell MT, Kirchman DL, Dexter SC (2007) Bacterial community structure of biofilms on artificial surfaces in an estuary. Microb Ecol 53:153–162CrossRefGoogle Scholar
  37. Kumwimba MN, Zhu B (2017) Effectiveness of vegetated drainage ditches for domestic sewage effluent mitigation. Bull Environ Contam Toxicol 98:682–689CrossRefGoogle Scholar
  38. Lee JW, Nam JH, Kim YH, Lee KH, Lee DH (2008) Bacterial communities in the initial stage of marine biofilm formation on artificial surfaces. J Microbiol 46:174–182CrossRefGoogle Scholar
  39. Leisner JJ, Laursen BG, Prevost H, Drider D, Dalgaard P (2007) Carnobacterium: positive and negative effects in the environment and in foods. FEMS Microbiol Rev 31:592–613CrossRefGoogle Scholar
  40. Lopez-Garcia P, Ghai R, Rodŕíguez-Valera F, McMahon KD, Toyama D, Rinke R, Cristina Souza de Oliveira T, Wagner Garcia J, Pellon de Miranda F, Henrique-Silva F (2011) Metagenomics of the water column in the pristine upper course of the Amazon river. PLoS ONE 6:e23785CrossRefGoogle Scholar
  41. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235CrossRefGoogle Scholar
  42. Lyautey E, Jackson CR, Cayrou J, Rols JL, Garabetian F (2005) Bacterial community succession in natural river biofilm assemblages. Microb Ecol 50:589–601CrossRefGoogle Scholar
  43. Ma Q, Qu YY, Zhang XW, Shen WL, Liu ZY, Wang JW, Zhang ZJ, Zhou JT (2015) Identification of the microbial community composition and structure of coal-mine wastewater treatment plants. Microbiol Res 175:1–5CrossRefGoogle Scholar
  44. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963CrossRefGoogle Scholar
  45. Mi Y, He C, Bian H, Cai Y, Sheng L, Ma L (2015) Ecological engineering restoration of a non-point source polluted river in northern China. Ecol Eng 76:142–150CrossRefGoogle Scholar
  46. Parfenova VV, Gladkikh AS, Belykh OI (2013) Comparative analysis of biodiversity in the planktonic and biofilm bacterial communities in Lake Baikal. Microbiology 82:91–101CrossRefGoogle Scholar
  47. Peng Y, Li J, Lu J, Xiao L, Yang L (2017) Characteristics of microbial community involved in early biofilms formation under the influence of wastewater treatment plant effluent. J Environ SciGoogle Scholar
  48. Real R, Vargas JM (1996) The probabilistic basis of Jaccard’s index of similarity. Syst Biol 45:380–385CrossRefGoogle Scholar
  49. Salles JF, Roux XL (2009) Community niche predicts the functioning of denitrifying bacterial assemblages. Ecology 90:3324–3332CrossRefGoogle Scholar
  50. Schloss PD (2008) Evaluating different approaches that test whether microbial communities have the same structure. ISME J 2:265–275CrossRefGoogle Scholar
  51. 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: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  52. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60CrossRefGoogle Scholar
  53. Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14:389–397CrossRefGoogle Scholar
  54. Tang X, Chao J, Gong Y, Wang Y, Wilhelm SW, Gao G (2017) Spatiotemporal dynamics of bacterial community composition in large shallow eutrophic Lake Taihu: high overlap between free-living and particle-attached assemblages. Limnol Oceanogr 62:1366–1382CrossRefGoogle Scholar
  55. Torsvik V, Ovreas L, Thingstad TF (2002) Prokaryotic diversity—magnitude, dynamics, and controlling factors. Science 296:1064–1066CrossRefGoogle Scholar
  56. Townsend SA, Gell PA (2005) The role of substrate type on benthic diatom assemblages in the Daly and Roper rivers of the Australian wet/dry tropics. Hydrobiologia 548:101–115CrossRefGoogle Scholar
  57. Tujula NA, Crocetti GR, Burke C, Thomas T, Holmstrom C, Kjelleberg S (2010) Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME J 4:301–311CrossRefGoogle Scholar
  58. Voget S, Klippel B, Daniel R, Antranikian G (2011) Complete genome sequence of Carnobacterium sp. 17-4. J Bacteriol 193:3403–3404CrossRefGoogle Scholar
  59. Wagner M, Loy A (2002) Bacterial community composition and function in sewage treatment systems. Curr Opin Biotechnol 13:218–227CrossRefGoogle Scholar
  60. Wang Y, Sheng HF, He Y, Wu JY, Jiang YX, Tam NF, Zhou HW (2012) Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Appl Environ Microbiol 78:8264–8271CrossRefGoogle Scholar
  61. Wetzel RG, Søndergaard M (1998) Role of submerged macrophytes for the microbial community and dynamics of dissolved organic carbon in aquatic ecosystems. Springer, New York, pp 133–148Google Scholar
  62. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer Publishing Company, Incorporated, 180–185 ppGoogle Scholar
  63. Wu Y, Hu Z, Yang L, Graham B, Kerr PG (2011) The removal of nutrients from non-point source wastewater by a hybrid bioreactor. Bioresour Technol 102:2419–2426CrossRefGoogle Scholar
  64. Wu R, Zhang X, Dai J, Gao G (2014a) Comparison of the abilities of three artificial substrates in purifying eutropic waters. J Lake Sci 26:682–690 (In Chinese)CrossRefGoogle Scholar
  65. Wu X, Wu H, Ye J (2014b) Purification effects of two eco-ditch systems on Chinese soft-shelled turtle greenhouse culture wastewater pollution. Environ Sci Pollut Res Int 21:5610–5618CrossRefGoogle Scholar
  66. Wu Y, Liu J, Shen R, Fu B (2017) Mitigation of nonpoint source pollution in rural areas: from control to synergies of multi ecosystem services. Sci Total Environ 607-608:1376–1380CrossRefGoogle Scholar
  67. Xiong Y, Peng S, Luo Y, Xu J, Yang S (2015) A paddy eco-ditch and wetland system to reduce non-point source pollution from rice-based production system while maintaining water use efficiency. Environ Sci Pollut Res Int 22:4406–4417CrossRefGoogle Scholar
  68. Yang H, Schmitt-Wagner D, Stingl U, Brune A (2005) Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis). Environ Microbiol 7:916–932CrossRefGoogle Scholar
  69. Ye L, Zhang T (2013) Bacterial communities in different sections of a municipal wastewater treatment plant revealed by 16S rDNA 454 pyrosequencing. Appl Microbiol Biotechnol 97:2681–2690CrossRefGoogle Scholar
  70. Ye W, Liu X, Lin S, Tan J, Pan J, Li D, Yang H (2009) The vertical distribution of bacterial and archaeal communities in the water and sediment of Lake Taihu. FEMS Microbiol Ecol 70:107–120CrossRefGoogle Scholar
  71. Yuan X, Qian X, Zhang R, Ye R, Hu W (2012) Performance and microbial community analysis of a novel bio-cord carrier during treatment of a polluted river. Bioresour Technol 117:33–39CrossRefGoogle Scholar
  72. Zhang T, Shao MF, Ye L (2012) 454 pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. ISME J 6:1137–1147CrossRefGoogle Scholar
  73. Zhang S, Pang S, Wang P, Wang C, Guo C, Addo FG, Li Y (2016) Responses of bacterial community structure and denitrifying bacteria in biofilm to submerged macrophytes and nitrate. Sci Rep 6:36178CrossRefGoogle Scholar
  74. Zhao J, Feng L, Dai J, Yang G, Mu J (2017) Characteristics of nitrogen removal and microbial community in biofilm system via combination of pretreated lignocellulosic carriers and various conventional fillers. Biodegradation 28:1–13CrossRefGoogle Scholar
  75. Zou L, Chen F, Wang X, Sun R (2013) High purification of micro-polluted water in compound artificial wetland with bio-cord and wetland plant. J Shanghai Univ (Nat Sci) 19:465–469 (In Chinese)Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Taihu Laboratory for Lake Ecosystem Research, State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and LimnologyChinese Academy of SciencesNanjingPeople’s Republic of China
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Department of Bioscience and Arctic Research CentreAarhus UniversitySilkeborgDenmark
  4. 4.Sino-Danish Centre for Education and ResearchBeijingChina

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