Skip to main content
Log in

Salinity-driven heterogeneity toward anammox distribution and growth kinetics

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Anaerobic ammonium oxidation (anammox) has been widely applied for biological nitrogen removal in freshwater systems, and there is a potential for its extension in saline water systems. In this study, the abundance and biodiversity of anammox bacteria were investigated in both saline and freshwater full-scale sewage treatment plants (STPs). The anammox bacteria were widely found in four tested STPs with abundance of 105–107 copies per mL of 16S rRNA gene. Phylogenetic results showed that Ca. Scalindua and Ca. Brocadia dominated in saline and freshwater STPs, respectively. Ca. Kuenenia dominated in one of freshwater STPs. However, redundancy discriminate analysis (RDA) indicates the distribution of Ca. Kuenenia in both saline and freshwater conditions. To further elucidate these observations, the Monod model was integrated with Gauss equation for the evaluation of salinity-induced kinetics. Model results reveal that when nitrite concentration (SNO2) is higher than nitrite affinity constant (KNO2), salinity (over ~ 3.0%) is responsible for Candidatus Scalindua dominance over Candidatus Kuenenia. Conversely, in nitrite-depleted conditions (KNO2 ≥ SNO2), high nitrite affinity leads to the predominance of Ca. Scalindua in all salinities. This study provides fundamental insights into saline anammox applications.

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
Fig. 4

Similar content being viewed by others

References

  • Awata T, Oshiki M, Kindaichi T, Ozaki N, Ohashi A, Okabe S (2013) Physiological characterization of an anaerobic ammonium-oxidizing bacterium belonging to the “Candidatus Scalindua” group. Appl Environ Microbiol 79(13):4145–4148

    Article  CAS  Google Scholar 

  • Azari M, Lübken M, Denecke M (2017a) Simulation of simultaneous anammox and denitrification for kinetic and physiological characterization of microbial community in a granular biofilm system. Biochem Eng J 127:206–216

    Article  CAS  Google Scholar 

  • Azari M, Walter U, Rekers V, Gu JD, Denecke M (2017b) More than a decade of experience of landfill leachate treatment with a full-scale anammox plant combining activated sludge and activated carbon biofilm. Chemosphere 174:117–126

    Article  CAS  Google Scholar 

  • Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Icwsm 8:361–362

    Google Scholar 

  • Dapena-Mora A, Vázquez-Padín J, Campos J, Mosquera-Corral A, Jetten M, Méndez R (2010) Monitoring the stability of an Anammox reactor under high salinity conditions. Biochem Eng J 51(3):167–171

    Article  CAS  Google Scholar 

  • de Almeida NM, Wessels HJ, de Graaf RM, Ferousi C, Jetten MS, Keltjens JT, Kartal B (2016) Membrane-bound electron transport systems of an anammox bacterium: a complexome analysis. Biochim Biophys Acta (BBA)-Bioenergetics 1857(10):1694–1704

    Article  Google Scholar 

  • Hall TA(1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In: Nucleic acids symposium series 41(41), Information Retrieval Ltd.,c1979-c2000, London., p 95–98

  • Hao X, Heijnen JJ, Van Loosdrecht MC (2002) Model-based evaluation of temperature and inflow variations on a partial nitrification–ANAMMOX biofilm process. Water Res 36(19):4839–4849

    Article  CAS  Google Scholar 

  • Humbert S, Zopfi J, Tarnawski SE (2012) Abundance of anammox bacteria in different wetland soils. Environ Microbiol Rep 4(5):484–490

    Article  CAS  Google Scholar 

  • Jetten MS, Wagner M, Fuerst J, van Loosdrecht M, Kuenen G, Strous M (2001) Microbiology and application of the anaerobic ammonium oxidation (‘anammox’) process. Curr Opin Biotechnol 12(3):283–288

    Article  CAS  Google Scholar 

  • Ji X, Huang Y-T, Wang Q, Tan GYA, Lin J-G, Lee P-H (2015) State-of-the-Art anaerobic ammonium oxidation (anammox) technology. In: Fang, HHP and Zhang T (eds) Anaerobic biotechnology: environmental protection and resource recovery. World Scientific, pp 49–71

  • Juretschko S, Timmermann G, Schmid M, Schleifer K-H, Pommerening-Röser A, Koops H-P, 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(8):3042–3051

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kartal B, Koleva M, Arsov R, van der Star W, Jetten MS, Strous M (2006) Adaptation of a freshwater anammox population to high salinity wastewater. J Biotechnol 126(4):546–553

    Article  CAS  Google Scholar 

  • Kindaichi T, Awata T, Suzuki Y, Tanabe K, Hatamoto M, Ozaki N, Ohashi A (2011) Enrichment using an up-flow column reactor and community structure of marine anammox bacteria from coastal sediment. Microbes Environ 26(1):67–73

    Article  Google Scholar 

  • Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, van Loosdrecht MC (2014) Full-scale partial nitritation/anammox experiences–an application survey. Water Res 55:292–303

    Article  CAS  Google Scholar 

  • Liu C, Yamamoto T, Nishiyama T, Fujii T, Furukawa K (2009) Effect of salt concentration in anammox treatment using non woven biomass carrier. J Biosci Bioeng 107(5):519–523

    Article  CAS  Google Scholar 

  • Liu M, Peng Y, Wang S, Liu T, Xiao H (2014) Enhancement of anammox activity by addition of compatible solutes at high salinity conditions. Bioresour Technol 167:560–563

    Article  CAS  Google Scholar 

  • Liu Y, Ni B-J (2015) Appropriate Fe (II) addition significantly enhances anaerobic ammonium oxidation (anammox) activity through improving the bacterial growth rate. Sci Rep 5:8204

    Article  CAS  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(12):8228–8235

    Article  CAS  Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar BA, Lai T, Steppi S, Jobb G (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32(4):1363–1371

    Article  CAS  Google Scholar 

  • Mulkidjanian AY, Dibrov P, Galperin MY (2008) The past and present of sodium energetics: may the sodium-motive force be with you. Biochim Biophys Acta (BBA)-Bioenergetics 1777(7–8):985–992

    Article  CAS  Google Scholar 

  • Nakajima J, Sakka M, Kimura T, Furukawa K, Sakka K (2008) Enrichment of anammox bacteria from marine environment for the construction of a bioremediation reactor. Appl Microbiol Biotechnol 77(5):1159–1166

    Article  CAS  Google Scholar 

  • Neef A, Amann R, Schlesner H, Schleifer K-H (1998) Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiol 144(12):3257–3266

    Article  CAS  Google Scholar 

  • Nejidat A, Diaz-Reck D, Massalha N, Arbiv A, Dawas A, Dosoretz C, Sabbah I (2018) Abundance and diversity of anammox bacteria in a mainstream municipal wastewater treatment plant. Appl Microbiol Biotechnol 102(15):6713–6723

    Article  CAS  Google Scholar 

  • Oshiki M, Shimokawa M, Fujii N, Satoh H, Okabe S (2011) Physiological characteristics of the anaerobic ammonium-oxidizing bacterium “Candidatus Brocadia sinica”. Microbiol 157(6):1706–1713

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541

    Article  CAS  Google Scholar 

  • Schmid M, Walsh K, Webb R, Rijpstra WI, van de Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J, Schouten S (2003) Candidatus “Scalindua brodae”, sp. nov., Candidatus “Scalindua wagneri”, sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 26(4):529–538

    Article  CAS  Google Scholar 

  • Sonthiphand P, Hall MW, Neufeld JD (2014) Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria. Front Microbiol 5:399

    Article  Google Scholar 

  • Ter Braak CJ, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). www. canoco. com

  • Van Der Star WR, Miclea AI, Van Dongen UG, Muyzer G, Picioreanu C, van Loosdrecht M (2008) The membrane bioreactor: a novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng 101(2):286–294

    Article  Google Scholar 

  • Wang S, Peng Y, Ma B, Wang S, Zhu G (2015) Anaerobic ammonium oxidation in traditional municipal wastewater treatment plants with low-strength ammonium loading: widespread but overlooked. Water Res 84:66–75

    Article  CAS  Google Scholar 

  • Windey K, De Bo I, Verstraete W (2005) Oxygen-limited autotrophic nitrification–denitrification (OLAND) in a rotating biological contactor treating high-salinity wastewater. Water Res 39(18):4512–4520

    Article  CAS  Google Scholar 

  • Wright ES, Yilmaz LS, Noguera DR (2012) DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl Environ Microbiol 78(3):717–725

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study received funds from the Research Grants Council (RGC) General Research Fund (15273316), Collaborative Research Fund (C7044-14G), Theme-based Fund (T21-711/16-R), and grant (1-ZVJU) from the Hong Kong Polytechnic University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Po-Heng Lee.

Ethics declarations

Human and animal rights and informed consent

This paper does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

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

Electronic supplementary material

ESM 1

(PDF 252 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Z., Meng, H., Huang, X. et al. Salinity-driven heterogeneity toward anammox distribution and growth kinetics. Appl Microbiol Biotechnol 103, 1953–1960 (2019). https://doi.org/10.1007/s00253-018-9521-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-018-9521-4

Keywords

Navigation