Skip to main content
Log in

The diversity of comammox bacteria and the effect of sewage discharge on their abundance in eutrophic lake sediments

  • Sediments, Sec 2 • Physical and Biogeochemical Processes • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Complete ammonia oxidation (comammox) bacteria can independently oxidize ammonia to nitrate, and their discovery has changed the long-term understanding of nitrification. Comammox bacteria have been found in a variety of natural environments, but there is still a lack of understanding regarding their presence in eutrophic lakes. The main purpose of this study was to investigate the diversity and abundance of comammox bacteria in a eutrophic lake and the effects of sewage discharge on bacterial abundance.

Materials and methods

Samples were taken from five areas of Lake Tangxun, China, i.e., a water chestnut (Trapa natans) area, a lotus (Nelumbo) area, a bare sediment area, a food sewage disposal area, and a domestic sewage disposal area. The diversity of comammox bacteria and the abundance of ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB), comammox bacteria, and anaerobic ammonia-oxidizing (anammox) bacteria were measured.

Results and discussion

Comammox bacteria were widely found in Lake Tangxun and were closely related to Candidatus Nitrospira nitrosa and Candidatus Nitrospira inopinata. The abundance of the comammox amoA gene was lower in the two sewage discharge areas (1.3 × 107 copies g−1) than in the emergent plant areas (1.75 × 108 copies g−1) and the bare sediment area (1.0 × 108 copies g−1). The abundance of the comammox amoA gene at the five sampling areas was higher than that of the AOA amoA gene and AOB amoA gene, which indicated that comammox bacteria had a growth advantage in this eutrophic lake.

Conclusions

Comammox bacteria were found in eutrophic lake sediments, and these bacteria belonged to comammox clade A. The abundance of comammox bacteria in the two sewage discharge areas was the lowest, indicating that they could survive in eutrophic waters, but eutrophication inhibited their growth.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Camejo PY, Domingo JS, McMahon KD, Noguera DR (2017) Genome-enabled insights into the ecophysiology of the comammox bacterium Candidatus Nitrospira nitrosa. mSystems 2:16

    Google Scholar 

  • Chen YL, Xu ZW, Hu HW, Hu YJ, Hao ZP, Jiang Y, Chen BD (2013) Responses of ammonia-oxidizing bacteria and archaea to nitrogen fertilization and precipitation increment in a typical temperate steppe in Inner Mongolia. Appl Soil Ecol 68:36–45

    Google Scholar 

  • Christensen PB, Revsbech NP, Sandjensen K (1994) Microsensor analysis of oxygen in the rhizosphere of the aquatic macrophyte Littorella-Uniflora (L) ascherson. Plant Physiol 105:847–852

    CAS  Google Scholar 

  • Costa E, Pérez J, Kreft J-U (2006) Why is metabolic labour divided in nitrification? Trends Microbiol 14:213–219

    CAS  Google Scholar 

  • Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509

    CAS  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624

    CAS  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O'Callaghan M, Bowatte S, He JZ (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394

    CAS  Google Scholar 

  • Duan HR, Wang QL, Erler DV, Ye L, Yuan ZG (2018) Effects of free nitrous acid treatment conditions on the nitrite pathway performance in mainstream wastewater treatment. Sci Total Environ 644:360–370

    CAS  Google Scholar 

  • Fowler SJ, Palomo A, Dechesne A, Mines PD, Smets BF (2018) Comammox Nitrospira are abundant ammonia oxidizers in diverse groundwater-fed rapid sand filter communities. Environ Microbiol 20:1002–1015

    CAS  Google Scholar 

  • Gao JF, Fan XY, Pan KL, Li HY, Sun LX (2016) Diversity, abundance and activity of ammonia-oxidizing microorganisms in fine particulate matter. Sci Rep 6:38785

    CAS  Google Scholar 

  • Haichar FE, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80

    CAS  Google Scholar 

  • 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 Microb 75:3127–3136

    CAS  Google Scholar 

  • Hou J, Song CL, Cao XY, Zhou YY (2013) Shifts between ammonia-oxidizing bacteria and archaea in relation to nitrification potential across trophic gradients in two large Chinese lakes (Lake Taihu and Lake Chaohu). Water Res 47:2285–2296

    CAS  Google Scholar 

  • Ji GD, Wang RJ, Zhi W, Liu XX, Kong YP, Tan YF (2012) Distribution patterns of denitrification functional genes and microbial floras in multimedia constructed wetlands. Ecol Eng 44:179–188

    Google Scholar 

  • Jiang Q, Xia F, Zhu T, Wang D, Quan Z (2019) Distribution of comammox and canonical ammonia oxidizing bacteria in tidal flat sediments of the Yangtze River estuary at different depths over four seasons. J Appl Microbiol 127:533–543

    CAS  Google Scholar 

  • Keene-Beach N, Noguera DR (2019) Design and assessment of species-level qPCR primers targeting comammox. Front Microbiol 10:36

  • Kits KD, Sedlacek CJ, Lebedeva EV, Han P, Bulaev A, Pjevac P, Daebeler A, Romano S, Albertsen M, Stein LY, Daims H, Wagner M (2017) Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549:269–272

    CAS  Google Scholar 

  • Koch H, Kessel MAHJV, Sebastian L (2019) Complete nitrification: insights into the ecophysiology of comammox nitrospira. Appl Microbiol Biot 103:177–189

    CAS  Google Scholar 

  • Konneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Google Scholar 

  • Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, Jorgensen BB, Jetten MSM (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. P Natl Acad Sci USA 102:6478–6483

    CAS  Google Scholar 

  • Li P, Li SN, Zhang Y, Cheng HM, Zhou HL, Qiu LG, Diao XP (2018) Seasonal variation of anaerobic ammonium oxidizing bacterial community and abundance in tropical mangrove wetland sediments with depth. Appl Soil Ecol 130:149–158

    Google Scholar 

  • Liu B, Li YM, Zhang JP, Zhou XH, Wu CD (2014) Abundance and diversity of ammonia-oxidizing microorganisms in the sediments of Jinshan Lake. Curr Microbiol 69:751–757

    CAS  Google Scholar 

  • Meinhardt KA, Bertagnolli A, Pannu MW, Strand SE, Brown SL, Stahl DA (2015) Evaluation of revised polymerase chain reaction primers for more inclusive quantification of ammonia-oxidizing archaea and bacteria. Env Microbiol Rep 7:354–363

    CAS  Google Scholar 

  • Nikolausz M, Kappelmeyer U, Szekely A, Rusznyak A, Marialigeti K, Kastner M (2008) Diurnal redox fluctuation and microbial activity in the rhizosphere of wetland plants. Eur J Soil Biol 44:324–333

    CAS  Google Scholar 

  • Orellana LH, Chee-Sanford JC, Sanford RA, Loffler FE, Konstantinidis KT (2018) Year-round shotgun metagenomes reveal stable microbial communities in agricultural soils and novel ammonia oxidizers responding to fertilization. Appl Environ Microb 84:e01646–e01617

    Google Scholar 

  • Oshiki M, Satoh H, Okabe S (2016) Ecology and physiology of anaerobic ammonium oxidizing bacteria. Environ Microbiol 18:2784–2796

    CAS  Google Scholar 

  • Otte S, Schalk J, Kuenen JG, Jetten MSM (1999) Hydroxylamine oxidation and subsequent nitrous oxide production by the heterotrophic ammonia oxidizer Alcaligenes faecalis. Appl Microbiol Biot 51:255–261

    CAS  Google Scholar 

  • Palomo A, Pedersen AG, Fowler SJ, Dechesne A, Sicheritz-Ponten T, Smets BF (2018) Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira. ISME J 12:1779–1793

    Google Scholar 

  • Pan KL, Gao JF, Fan XY, Li DC, Dai HH (2018) The more important role of archaea than bacteria in nitrification of wastewater treatment plants in cold season despite their numerical relationships. Water Res 145:552–561

    CAS  Google Scholar 

  • Pinto AJ, Marcus DN, Ijaz UZ, Santos QMBD, Dick GJ, Raskin L (2016) Metagenomic evidence for the presence of comammox Nitrospira-like bacteria in a drinking water system. Msphere 1:e00054–e00015

    Google Scholar 

  • Pjevac P, Schauberger C, Poghosyan L, Herbold CW, van Kessel MAHJ, Daebeler A, Steinberger M, Jetten MSM, Lucker S, Wagner M, Daims H (2017) AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Front Microbiol 8:1508

    Google Scholar 

  • Roots P, Wang YB, Rosenthal AF, Griffin JS, Sabba F, Petrovich M, Yang FH, Kozak JA, Zhang H, Wells GF (2019) Comammox Nitrospira are the dominant ammonia oxidizers in a mainstream low dissolved oxygen nitrification reactor. Water Res 157:396–405

    CAS  Google Scholar 

  • Shi XZ, Hu HW, Wang JQ, He JZ, Zheng CY, Wan XH, Huang ZQ (2018) Niche separation of comammox Nitrospira and canonical ammonia oxidizers in an acidic subtropical forest soil under long-term nitrogen deposition. Soil Biol Biochem 126:114–122

    CAS  Google Scholar 

  • Tsiknia M, Tzanakakis VA, Paranychianakis NV (2013) Insights on the role of vegetation on nitrogen cycling in effluent irrigated lands. Appl Soil Ecol 64:104–111

    Google Scholar 

  • van Kessel MAHJ, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJM, Kartal B, Jetten MSM, Lucker S (2015) Complete nitrification by a single microorganism. Nature 528:555–559

    Google Scholar 

  • Wang YF, Gu JD (2013) Higher diversity of ammonia/ammonium-oxidizing prokaryotes in constructed freshwater wetland than natural coastal marine wetland. Appl Microbiol Biot 97:7015–7033

    CAS  Google Scholar 

  • Wang YL, Ma LP, Mao YP, Jiang XT, Xia Y, Yu K, Li B, Zhang T (2017) Comammox in drinking water systems. Water Res 116:332–341

    CAS  Google Scholar 

  • Wang MY, Huang GH, Zhao ZR, Dang CY, Liu W, Zheng MS (2018) Newly designed primer pair revealed dominant and diverse comammox amoA gene in full-scale wastewater treatment plants. Bioresour Technol 270:580–587

    CAS  Google Scholar 

  • Xia F, Wang JG, Zhu T, Zou B, Rhee SK, Quan ZX (2018) Ubiquity and diversity of complete ammonia oxidizers (Comammox). Appl Environ Microb 84:e01390–e01318

    CAS  Google Scholar 

  • Yan J, Haaijer SCM, den Camp HJMO, van Niftrik L, Stahl DA, Konneke M, Rush D, Damste JSS, Hu YY, Jetten MSM (2012) Mimicking the oxygen minimum zones: stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system. Environ Microbiol 14:3146–3158

    CAS  Google Scholar 

  • Yu CD, Hou LJ, Zheng YL, Liu M, Yin GY, Gao J, Liu C, Chang YK, Han P (2018) Evidence for complete nitrification in enrichment culture of tidal sediments and diversity analysis of clade a comammox Nitrospira in natural environments. Appl Microbiol Biot 102:9363–9377

    CAS  Google Scholar 

  • Zhang JP, Liu B, Zhou XH, Chu JY, Li YM, Wang MY (2015) Effects of emergent aquatic plants on abundance and community structure of ammonia-oxidising microorganisms. Ecol Eng 81:504–513

    Google Scholar 

  • Zhao DY, Luo J, Zeng J, Wang M, Yan WM, Huang R, Wu QL (2014) Effects of submerged macrophytes on the abundance and community composition of ammonia-oxidizing prokaryotes in a eutrophic lake. Environ Sci Pollut Res Int 21:389–398

    Google Scholar 

  • Zhao ZR, Huang GH, He SS, Zhou N, Wang MY, Dang CY, Wang JW, Zheng MS (2019) Abundance and community composition of comammox bacteria in different ecosystems by a universal primer set. Sci Total Environ 691:146–155

    CAS  Google Scholar 

  • Zheng MS, Wang MY, Zhao ZR, Zhou N, He SS, Liu SF, Wang JW, Wang XK (2019) Transcriptional activity and diversity of comammox bacteria as a previously overlooked ammonia oxidizing prokaryote in full-scale wastewater treatment plants. Sci Total Environ 656:717–722

    CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (41371452, 40901264).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jianwei Zhao.

Ethics declarations

The authors declare that no conflict of interest exists in the submission of this article and the article does not contain any studies with human participants or animals. The manuscript is approved by all authors for publication.

Additional information

Responsible editor: Terrence H. Bell

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 143 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Y., Liu, G., Hua, Y. et al. The diversity of comammox bacteria and the effect of sewage discharge on their abundance in eutrophic lake sediments. J Soils Sediments 20, 2495–2503 (2020). https://doi.org/10.1007/s11368-020-02618-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-020-02618-y

Keywords

Navigation