Advertisement

Journal of Soils and Sediments

, Volume 19, Issue 10, pp 3648–3656 | Cite as

Diversity of anammox bacteria and abundance of functional genes for nitrogen cycling in the rhizosphere of submerged macrophytes in a freshwater lake in summer

  • Jianwei Zhao
  • Yangfan Xu
  • Lei Peng
  • Guanglong Liu
  • Xiaoqiong Wan
  • Yumei HuaEmail author
  • Duanwei Zhu
  • David P. HamiltonEmail author
Sediments, Sec 4 • Sediment-Ecology Interactions • Research Article
  • 136 Downloads

Abstract

Purpose

Submerged plants make an important contribution to nitrogen cycling in lakes including in the rhizosphere microenvironment through microbial activities. The main objective of this study was to investigate the abundance of functional genes for nitrogen cycling and the ecological relationship between these genes in the rhizosphere sediment of a freshwater lake in summer.

Materials and methods

Sediment from the rhizosphere of four submerged macrophytes (Ceratophyllum demersum, Hydrilla verticillata, Potamogeton maackianus, and Vallisneria spiralis) was sampled in Lake Liangzi, China, in summer. The anammox bacteria community structure and abundance of five functional genes for nitrogen cycling, ammonia monooxygenase (amoA) of ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA), anammox 16S rRNA, and nitrite reductase genes (nirK and nirS) in the sampled sediment, were determined.

Results and discussion

A total of 100 anammox gene sequences were grouped into eight operational taxonomic units (OTUs) and genus Ca. Kuenenia was the dominant species in Lake Liangzi in summer. Quantitative polymerase chain reaction (qPCR) revealed that gene copies of AOA amoA (2.42 × 106 copies g−1) were more than one order of magnitude higher than those of AOB amoA (1.98 × 105 copies g−1). The nirS gene (4.13 × 108 copies g−1) was more abundant than the nirK gene (7.28 × 107 copies g−1). There was no significant difference in the abundance of the AOB amoA gene among the rhizosphere of the four macrophytes. Redundancy analysis (RDA) showed a positive correlation between the abundance of the anammox 16S rRNA gene, AOA amoA and AOB amoA, which suggested two of these microbes may have provided a substrate for anammox bacteria in summer.

Conclusions

The diversity of anammox in the rhizosphere of submerged macrophytes of the freshwater lake in summer was very low, but the plant species could affect the abundance of most nitrogen circulating bacteria, especially for anammox bacteria. Anammox 16S rRNA gene was positively correlated with four other functional genes, indicating that all four genes had significant effects on anammox bacteria.

Keywords

Ammonia-oxidizing archaea Ammonia-oxidizing bacteria Anammox bacteria Denitrifying bacteria Rhizosphere Submerged macrophytes 

Notes

Funding information

This research was funded by the National Natural Science Foundation of China (Program No. 41371452) and Major Science and Technology Programme for Water Pollution Control and Treatment of China (Program No. 2014ZX07203010).

Supplementary material

11368_2019_2340_MOESM1_ESM.docx (18 kb)
ESM 1 (DOCX 18 kb)

References

  1. Ahn YH, Hwang IS, Min KS (2004) Anammox and partial denitritation in anaerobic nitrogen removal from piggery waste. Water Sci Technol 49:145–153CrossRefGoogle Scholar
  2. Berg G, Opelt K, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K (2006) The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiol Ecol 56:250–261CrossRefGoogle Scholar
  3. Bialowiec A, Davies L, Albuquerque A, Randerson PF (2012) The influence of plants on nitrogen removal from landfill leachate in discontinuous batch shallow constructed wetland with recirculating subsurface horizontal flow. Ecol Eng 40:44–52CrossRefGoogle Scholar
  4. Chen XP, Zhu YG, Xia Y, Shen JP, He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ Microbiol 10:1978–1987CrossRefGoogle Scholar
  5. Chen Y, Wen Y, Zhou Q, Vymazal J (2014) Effects of plant biomass on denitrifying genes in subsurface-flow constructed wetlands. Bioresour Technol 157:341–345CrossRefGoogle Scholar
  6. Chu J, Zhang J, Zhou X, Liu B, Li Y (2015) A comparison of anammox bacterial abundance and community structures in three different emerged plants-related sediments. Curr Microbiol 71:421–427CrossRefGoogle Scholar
  7. Dandie CE, Wertz S, Leclair CL, Goyer C, Burton DL, Patten CL, Zebarth BJ, Trevors JT (2011) Abundance, diversity and functional gene expression of denitrifier communities in adjacent riparian and agricultural zones. FEMS Microbiol Ecol 77:69–82CrossRefGoogle Scholar
  8. Egli K, Fanger U, Alvarez PJ, Siegrist H, van der Meer JR, Zehnder AJ (2001) Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch Microbiol 175:198–207CrossRefGoogle Scholar
  9. Francis CA, Beman JM, Kuypers MM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 1:19–27CrossRefGoogle Scholar
  10. Geets J, de Cooman M, Wittebolle L, Heylen K, Vanparys B, De Vos P, Verstraete W, Boon N (2007) Real-time PCR assay for the simultaneous quantification of nitrifying and denitrifying bacteria in activated sludge. Appl Microbiol Biotechnol 75:211–221CrossRefGoogle Scholar
  11. Hamersley MR, Lavik G, Woebken D, Rattray JE, Lam P, Hopmans EC, Damste JSS, Kruger S, Graco M, Gutierrez D, Kuypers MMM (2007) Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr 52:923–933CrossRefGoogle Scholar
  12. Henry S, Baudoin E, Lopez-Gutierrez JC, Martin-Laurent F, Brauman A, Philippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods 59:327–335CrossRefGoogle Scholar
  13. Herrmann M, Saunders AM, Schramm A (2008) Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Appl Environ Microbiol 74:3279–3283CrossRefGoogle Scholar
  14. Herrmann M, Saunders AM, Schramm A (2009) Effect of lake trophic status and rooted macrophytes on community composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments. Appl Environ Microbiol 75:3127–3136CrossRefGoogle Scholar
  15. Hou J, Cao XY, Song CL, Zhou YY (2013) Predominance of ammonia-oxidizing archaea and nirK-gene-bearing denitrifiers among ammonia-oxidizing and denitrifying populations in sediments of a large urban eutrophic lake (Lake Donghu). Can J Microbiol 59:456–464CrossRefGoogle Scholar
  16. Hua YM, Peng L, Zhang SH, Heal KV, Zhao JW, Zhu DW (2017) Effects of plants and temperature on nitrogen removal and microbiology in pilot-scale horizontal subsurface flow constructed wetlands treating domestic wastewater. Ecol Eng 108:70–77CrossRefGoogle Scholar
  17. Huang YT, Chen SS, Lee PH, Bae J (2013) Microbial community and population dynamics of single-stage autotrophic nitrogen removal for dilute wastewater at the benchmark oxygen rate supply. Bioresour Technol 147:649–653CrossRefGoogle Scholar
  18. Jiang XL, Wu YJ, Liu GH, Liu WZ, Lu B (2017) The effects of climate, catchment land use and local factors on the abundance and community structure of sediment ammonia-oxidizing microorganisms in Yangtze lakes. AMB Express 7:2–13CrossRefGoogle Scholar
  19. Jin XC, Tu QY (1990) Survey specification for lake eutrophication. China Environ Sci Press, BeijingGoogle Scholar
  20. Juretschko S, Timmermann G, Schmid M, Schleifer KH, Pommerening-Roser A, Koops HP, Wagner M (1998) Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol 64:3042–3051Google Scholar
  21. Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546CrossRefGoogle Scholar
  22. Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Dimitri G, Amann R, Jetten MSM, Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci U S A 106:4752–4757CrossRefGoogle Scholar
  23. Li H, Yang XR, Weng BS, Su JQ, Nie SA, Gilbert JA, Zhu YG (2016) The phenological stage of rice growth determines anaerobic ammonium oxidation activity in rhizosphere soil. Soil Biol Biochem 100:59–65CrossRefGoogle Scholar
  24. Ligi T, Truu M, Truu J, Nolvak H, Kaasik A, Mitsch WJ, Mander U (2014) Effects of soil chemical characteristics and water regime on denitrification genes (nirS, nirK, and nosZ) abundances in a created riverine wetland complex. Ecol Eng 72:47–55CrossRefGoogle Scholar
  25. Liu XD, Tiquia SM, Holguin G, Wu LY, Nold SC, Devol AH, Luo K, Palumbo AV, Tiedje JM, Zhou JZ (2003) Molecular diversity of denitrifying genes in continental margin sediments within the oxygen-deficient zone off the Pacific coast of Mexico. Appl Environ Microbiol 69:3549–3560CrossRefGoogle Scholar
  26. Mulder A, Vandegraaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16:177–183CrossRefGoogle Scholar
  27. Neef A, Amann R, Schlesner H, Schleifer KH (1998) Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology 144:3257–3266CrossRefGoogle Scholar
  28. Nie SA, Li H, Yang XR, Zhang ZJ, Weng BS, Huang FY, Zhu GB, Zhu YG (2015) Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere. ISME J 9:2059–2067CrossRefGoogle Scholar
  29. Oshiki M, Shimokawa M, Fujii N, Satohl H, Okabe S (2011) Physiological characteristics of the anaerobic ammonium-oxidizing bacterium ‘Candidatus Brocadia sinica’. Microbiology 157:1706–1713CrossRefGoogle Scholar
  30. Oshiki M, Awata T, Kindaichi T, Satoh H, Okabe S (2013) Cultivation of planktonic anaerobic ammonium oxidation (anammox) bacteria using membrane bioreactor. Microbes Environ 28:436–443CrossRefGoogle Scholar
  31. Park H, Sundar S, Ma YW, Chandran K (2015) Differentiation in the microbial ecology and activity of suspended and attached bacteria in a nitritation-anammox process. Biotechnol Bioeng 112:272–279CrossRefGoogle Scholar
  32. Petersen DG, Blazewicz SJ, Firestone M, Herman DJ, Turetsky M, Waldrop M (2012) Abundance of microbial genes associated with nitrogen cycling as indices of biogeochemical process rates across a vegetation gradient in Alaska. Environ Microbiol 14:993–1008CrossRefGoogle Scholar
  33. Philippot L, Hallin S (2005) Finding the missing link between diversity and activity using denitrifying bacteria as a model functional community. Curr Opin Microbiol 8:234–239CrossRefGoogle Scholar
  34. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361CrossRefGoogle Scholar
  35. Racchetti E, Longhi D, Ribaudo C, Soana E, Bartoli M (2017) Nitrogen uptake and coupled nitrification-denitrification in riverine sediments with benthic microalgae and rooted macrophytes. Aquat Sci 79:487–505CrossRefGoogle Scholar
  36. Reverey F, Ganzert L, Lischeid G, Ulrich A, Premke K, Grossart HP (2018) Dry-wet cycles of kettle hole sediments leave a microbial and biogeochemical legacy. Sci Total Environ 627:985–996CrossRefGoogle Scholar
  37. Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger JW, Schleifer KH, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23:93–106CrossRefGoogle Scholar
  38. Schmid M, Walsh K, Webb R, Rijpstra WIC, van de Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J, Schouten S, Damste JSS, Harris J, Shaw P, Jetten M, Strous M (2003) Candidatus “Scalindua brodae”, sp nov., Candidatus “Scalindua wagneri”, sp nov., two new species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 26:529–538CrossRefGoogle Scholar
  39. Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh BE, op den Camp HJM, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MSM, Wagner M, le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794CrossRefGoogle Scholar
  40. Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364CrossRefGoogle Scholar
  41. Tsushima I, Kindaichi T, Okabe S (2007) Quantification of anaerobic ammonium-oxidizing bacteria in enrichment cultures by real-time PCR. Water Res 41:785–794CrossRefGoogle Scholar
  42. van der Star WRL, Abma WR, Blommers D, Mulder JW, Tokutomi T, Strous M, Picioreanu C, Van Loosdrecht MCM (2007) Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam. Water Res 41:4149–4163CrossRefGoogle Scholar
  43. van der Star WRL, Miclea AI, van Dongen UGJM, Muyzer G, Picioreanu C, van Loosdrecht MCM (2008) The membrane bioreactor: a novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng 101:286–294CrossRefGoogle Scholar
  44. Vila-Costa M, Pulido C, Chappuis E, Calvino A, Casamayor EO, Gacia E (2016) Macrophyte landscape modulates lake ecosystem-level nitrogen losses through tightly coupled plant-microbe interactions. Limnol Oceanogr 61:78–88CrossRefGoogle Scholar
  45. Vilas MP, Marti CL, Adams MP, Oldham CE, Hipsey MR (2017) Invasive macrophytes control the spatial and temporal patterns of temperature and dissolved oxygen in a shallow lake: a proposed feedback mechanism of macrophyte loss. Front Plant Sci 8:1–14CrossRefGoogle Scholar
  46. Waki M, Yasuda T, Suzuki K, Komada M, Abe K (2015) Distribution of anammox bacteria in a free-water-surface constructed wetland with wild rice (Zizania latifolia). Ecol Eng 81:165–172CrossRefGoogle Scholar
  47. Weng BS, Xie XY, Yang JJ, Liu JC, Lu HL, Yan CL (2013) Research on the nitrogen cycle in rhizosphere of Kandelia obovata under ammonium and nitrate addition. Mar Pollut Bull 76:227–240CrossRefGoogle Scholar
  48. Wu YC, Xiang Y, Wang JJ, Zhong JC, He JZ, Wu QLL (2010) Heterogeneity of archaeal and bacterial ammonia-oxidizing communities in Lake Taihu, China. Environ Microbiol Rep 2:569–576CrossRefGoogle Scholar
  49. Xu XY, Ran Y, Li Y, Zhang QC, Liu YP, Pan H, Guan XM, Li JY, Shi JC, Dong L, Li Z, Di HJ, Xu JM (2016) Warmer and drier conditions alter the nitrifier and denitrifier communities and reduce N2O emissions in fertilized vegetable soils. Agric Ecosyst Environ 231:133–142CrossRefGoogle Scholar
  50. Xue YY, Yu Z, Chen HH, Yang JR, Liu M, Liu LMA, Huang BQ, Yang J (2017) Cyanobacterial bloom significantly boosts hypolimnelic anammox bacterial abundance in a subtropical stratified reservoir. FEMS Microbiol Ecol 93:1–11CrossRefGoogle Scholar
  51. Yan LY, Zhang SH, Lin D, Guo C, Yan LL, Wang SP, He ZL (2018) Nitrogen loading affects microbes, nitrifiers and denitrifiers attached to submerged macrophyte in constructed wetlands. Sci Total Environ 622:121–126CrossRefGoogle Scholar
  52. Yin XJ, Liu GL, Peng L, Hua YM, Wan XQ, Zhou WB, Zhao JW, Zhu DW (2018) Microbial community of nitrogen cycle-related genes in aquatic plant rhizospheres of Lake Liangzi in winter. J Basic Microbiol 58:998–1006CrossRefGoogle Scholar
  53. Zhang HH, Huang TL, Chen SN, Yang X, Lv K, Sekar R (2015) Abundance and diversity of bacteria in oxygen minimum drinking water reservoir sediments studied by quantitative PCR and pyrosequencing. Microb Ecol 69:618–629CrossRefGoogle Scholar
  54. Zhang HH, Wang Y, Chen SN, Zhao ZF, Feng J, Zhang ZH, Lu KY, Jia JY (2018) Water bacterial and fungal community compositions associated with Urban Lakes, Xi’an, China. Int J Environ Res Public Health 15:469–487CrossRefGoogle Scholar
  55. Zhang HH, Feng J, Chen SN, Zhao ZF, Li B, Wang Y, Jia JY, Li SL, Wang Y, Yan MM, Lu KY, Hao HY (2019) Geographical patterns of nirS gene abundance and nirS-type denitrifying bacterial community associated with activated sludge from different wastewater treatment plants. Microb Ecol 77:304–316CrossRefGoogle Scholar
  56. Zhao DY, Liu P, Fang C, Sun YM, Zeng J, Wang JQ, Ma T, Xiao YH, Wu QLL (2013) Submerged macrophytes modify bacterial community composition in sediments in a large, shallow, freshwater lake. Can J Microbiol 59:237–244CrossRefGoogle Scholar
  57. Zhao JW, Yin XJ, Huang SS, Zhang Y, Zhu DW, Hua YM, Zhou WB, Liu GL (2017) Distribution and diversity of anammox bacteria in two eutrophic lakes in Wuhan City, China. Fundam Appl Limnol 190:183–187CrossRefGoogle Scholar
  58. Zheng YL, Hou LJ, Liu M, Yin GY, Gao J, Jiang XF, Lin XB, Li XF, Yu CD, Wang R (2016) Community composition and activity of anaerobic ammonium oxidation bacteria in the rhizosphere of salt-marsh grass Spartina alterniflora. Appl Microbiol Biotechnol 100:8203–8212CrossRefGoogle Scholar
  59. Zhou S, Borjigin S, Riya S, Terada A, Hosomi M (2014) The relationship between anammox and denitrification in the sediment of an inland river. Sci Total Environ 490:1029–1036CrossRefGoogle Scholar
  60. Zhou ZC, Wei QY, Yang YC, Li M, Gu JD (2018) Practical applications of PCR primers in detection of anammox bacteria effectively from different types of samples. Appl Microbiol Biotechnol 102:5859–5871CrossRefGoogle Scholar
  61. Zhu GB, Wang SY, Wang WD, Wang Y, Zhou LL, Jiang B, Op den Camp HJM, Risgaard-Petersen N, Schwark L, Peng YZ, Hefting MM, Jetten MSM, Yin CQ (2013) Hotspots of anaerobic ammonium oxidation at land-freshwater interfaces. Nat Geosci 6:103–107CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Jianwei Zhao
    • 1
  • Yangfan Xu
    • 1
  • Lei Peng
    • 1
  • Guanglong Liu
    • 1
  • Xiaoqiong Wan
    • 1
  • Yumei Hua
    • 1
    Email author
  • Duanwei Zhu
    • 1
  • David P. Hamilton
    • 2
    Email author
  1. 1.Laboratory of Eco-Environmental Engineering Research, College of Resources and EnvironmentHuazhong Agricultural UniversityWuhanChina
  2. 2.Australian Rivers InstituteGriffith UniversityBrisbaneAustralia

Personalised recommendations