Skip to main content
Log in

Effect of NaCl on nitrification performance and extracellular polymeric substance characteristic of Klebsiella sp. TN-10

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Klebsiella sp. TN-10, isolated from tannery wastewater, exhibited excellent nitrification ability cultivated in media with NaCl contents ranging from 0 to 35 g/L. Analysis of antioxidative enzyme activities of TN-10 stressed by NaCl showed that the stain produced more superoxide dismutase (SOD) and catalase (CAT) to fight against salt stress conditions. Moreover, the auto-aggregation index of TN-10 decreased with the increment of NaCl contents, which is consistent with results of zeta potentials. Extinction-emission matrix (EEM) and Fourier-transform infrared (FT-IR) spectrum analyses showed that the compositions of extracellular polymeric substances (EPS) by TN-10 after NaCl shock were similar. Furthermore, proteins and polysaccharides were the main components of EPS, and the contents were greatly influenced by salinity. Then, circular dichroism (CD) spectrum was used to calculate the contents of each protein secondary structure. These results provided further insights into the knowledge of nitrification characteristics, auto-aggregation performance, and EPS compositions of TN-10 during NaCl shock.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adav SS, Lee D-J (2008) Single-culture aerobic granules with Acinetobacter calcoaceticus. Appl Microbiol Biot 78:551–557

    CAS  Google Scholar 

  • Amber B, Russell MH, Gladys A (2012) The Azospirillum brasilense Che1 chemotaxis pathway controls swimming velocity, which affects transient cell-to-cell clumping. J Bacteriol 194:3343–3355

    Google Scholar 

  • APHA (1998) Standard methods for the examination of water and waste water, 20th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Badireddy AR, Chellam S, Gassman PL, Engelhard MH, Lea AS, Rosso KM (2010) Role of extracellular polymeric substances in bioflocculation of activated sludge microorganisms under glucose-controlled conditions. Water Res 44:4505–4516

    CAS  Google Scholar 

  • Bassin JP, Muyzer G, Rosado AS, Loosdrecht MCMV, Dezotti M (2012) Effect of different salt adaptation strategies on the microbial diversity, activity, and settling of nitrifying sludge in sequencing batch reactors. Appl Microbiol Biot 93:1281–1294

    CAS  Google Scholar 

  • Bernstein R, Belfer S, Freger V (2011) Bacterial attachment to RO membranes surface-modified by concentration-polarization-enhanced graft polymerization. Environ Sci Technol 45:5973–5980

    CAS  Google Scholar 

  • Bin Z, Baosheng S, Min J, Taishi G, Zhenghong G (2008) Extraction and analysis of extracellular polymeric substances in membrane fouling in submerged MBR. Desalination 227:286–294

    Google Scholar 

  • Boopathy R, Gnanamani A, Mandal AB, Sekaran G (2012) A first report on the selective precipitation of sodium chloride from the evaporated residue of reverse osmosis reject salt generated from the leather industry. Ind Eng Chem Res 51:5527–5534

    CAS  Google Scholar 

  • Bourven I, Costa G, Guibaud G (2012) Qualitative characterization of the protein fraction of exopolymeric substances (EPS) extracted with EDTA from sludge. Bioresour Technol 104:486–496

    CAS  Google Scholar 

  • Cammarota MC, Sant’Anna GL Jr (1998) Metabolic blocking of exopolysaccharides synthesis: effects on microbial adhesion and biofilm accumulation. Biotechnol Lett 20:1–4

    CAS  Google Scholar 

  • Campo R, Corsino SF, Torregrossa M, Di Bella G (2018) The role of extracellular polymeric substances on aerobic granulation with stepwise increase of salinity. Sep Purif Technol 195:12–20

    CAS  Google Scholar 

  • Chen YP, Zhang P, Guo JS, Fang F, Gao X, Li C (2013) Functional groups characteristics of EPS in biofilm growing on different carriers. Chemosphere 92:633–638

    CAS  Google Scholar 

  • Clesceri L, Greenberg AS, Eaton DL (2005) Standard methods for the examinations of water and wastewater vol 56. vol 3. American Journal of Public Health & the Nations Health, Washington, DC, USA

    Google Scholar 

  • Corsino SF, Campo R, Bella GD, Torregrossa M, Viviani G (2015) Cultivation of granular sludge with hypersaline oily wastewater. Int Biodeterior Biodegrad 105:192–202

    CAS  Google Scholar 

  • Corsino SF, Capodici M, Torregrossa M, Viviani G (2017) Physical properties and extracellular polymeric substances pattern of aerobic granular sludge treating hypersaline wastewater. Bioresour Technol 229:152–159

    CAS  Google Scholar 

  • Corsino SF, Capodici M, Torregrossa M, Viviani G (2018) A comprehensive comparison between halophilic granular and flocculent sludge in withstanding short and long-term salinity fluctuations. J Water Process Eng 22:265–275

    Google Scholar 

  • Corsino SF, Capodici M, Di Pippo F, Tandoi V, Torregrossa M (2019) Comparison between kinetics of autochthonous marine bacteria in activated sludge and granular sludge systems at different salinity and SRTs. Water Res 148:425–437

    CAS  Google Scholar 

  • Damodaran S, Kinsella JE (1982) Effects of ions on protein conformation and functionality. ACS Sym Ser p. 327–357

  • Du G, Yu J (2002) Green technology for conversion of food scraps to biodegradable thermoplastic polyhydroxyalkanoates. Environ Sci Technol 36:5511–5516

    CAS  Google Scholar 

  • Formosa-Dague C, Feuillie C, Beaussart A, Derclaye S, Kucharíková S, Lasa I, van Dijck P, Dufrêne YF (2016) Sticky matrix: adhesion mechanism of the staphylococcal polysaccharide intercellular adhesin. ACS Nano 10:3443–3452

    CAS  Google Scholar 

  • Fr/Olund B, Griebe T, Nielsen PH (1995) Enzymatic activity in the activated-sludge floc matrix. Appl Microbiol Biot 43:755–761

    CAS  Google Scholar 

  • Fridovich I (1969) Superoxide Dismutases. Annu Rev Biochem 44:147–159

    Google Scholar 

  • Gui M, Chen Q, Ni J (2017) Effect of NaCl on aerobic denitrification by strain Achromobacter sp. GAD-3. Appl Microbiol Biot 101:5139–5147

    CAS  Google Scholar 

  • Guo G, He F, Tian F, Huang Y, Wang H (2016) Effect of salt contents on enzymatic activities and halophilic microbial community structure during phenanthrene degradation. Int Biodeterior Biodegrad 110:8–15

    CAS  Google Scholar 

  • Gupta A, Thakur IS (2016) Study of optimization of wastewater contaminant removal along with extracellular polymeric substances (EPS) production by a thermotolerant Bacillus sp. ISTVK1 isolated from heat shocked sewage sludge. Bioresour Technol 213:21–30

    CAS  Google Scholar 

  • Huang C, Wei G, Jie Y, Wang L, Zhou H, Ran C, Huang Z, Jia H, Anjum SA (2014) Effects of concentrations of sodium chloride on photosynthesis, antioxidative enzymes, growth and fiber yield of hybrid ramie. Plant Physiol Biochem 76:86–93

    CAS  Google Scholar 

  • Jia C, Li X, Allinson G, Liu C, Gong Z (2016) Composition and morphology characterization of exopolymeric substances produced by the PAH-degrading fungus of Mucor mucedo. Eeviron Sci Pollut R 23:8421–8430

    CAS  Google Scholar 

  • Li X-F, Li Y-J, Liu H, Hua Z-Z, Du G-C, Chen J (2008) Correlation between extracellular polymeric substances and aerobic biogranulation in membrane bioreactor. Sep Purif Technol 59:26–33

    CAS  Google Scholar 

  • Li Y, Li AM, Xu J, Li WW, Yu HQ (2013a) Formation of soluble microbial products (SMP) by activated sludge at various salinities. Biodegradation 24:69–78

    CAS  Google Scholar 

  • Li ZG, Yuan LX, Wang QL, Ding ZL, Dong CY (2013b) Combined action of antioxidant defense system and osmolytes in chilling shock-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol Plant 35:2127–2136

    CAS  Google Scholar 

  • Li D, Liang X, Jin Y, Wu C, Zhou R (2019) Isolation and nitrogen removal characteristics of an aerobic heterotrophic nitrifying-denitrifying bacterium, Klebsiella sp. TN-10. Appl Biochem Biotechnol 188(2):540–554

  • Lin L, Rosenberg M, Taylor KG, Doyle RJ (1995) Kinetic analysis of ammonium sulfate dependent aggregation of bacteria. Colloids Surf B 5:127–134

    CAS  Google Scholar 

  • Lv J, Wang Y, Zhong C, Li Y, Hao W, Zhu J (2014) The effect of quorum sensing and extracellular proteins on the microbial attachment of aerobic granular activated sludge. Bioresour Technol 152:53–58

    CAS  Google Scholar 

  • Muthukrishnan S, Sabaratnam V, Chong V (2012) Ammonia nitrogen removal by an aerobic heterotrophic bacterium, Microbacterium sp., VCM11. Malays J Sci 31:76–82

    Google Scholar 

  • Omoike A, Chorover J (2004) Spectroscopic study of extracellular polymeric substances from Bacillus subtilis: aqueous chemistry and adsorption effects. Biomacromolecules 5:1219–1230

    CAS  Google Scholar 

  • Pembrey RS, Marshall KC, Schneider RP (1999) Cell surface analysis techniques: what do cell preparation protocols do to cell surface properties? Appl Environ Microbiol 65:2877–2894

    CAS  Google Scholar 

  • Perez-Iratxeta C, Andrade-Navarro MA (2008) K2D2: estimation of protein secondary structure from circular dichroism spectra. BMC Struct Biol 8:1–5

    Google Scholar 

  • Prasad TK (1997) Role of catalase in inducing chilling tolerance in pre-emergent maize seedlings. Plant Physiol 114:1369–1376

    CAS  Google Scholar 

  • Raman CD, Kanmani S (2016) Textile dye degradation using nano zero valent iron: a review. J Environ Manag 177:341–355

    CAS  Google Scholar 

  • Raunkjær K, Hvitved-Jacobsen T, Nielsen PH (1994) Measurement of pools of protein, carbohydrate and lipid in domestic wastewater. Water Res 28:251–262

    Google Scholar 

  • Rhee SG, Yang KS, Kang SW, Woo HA, Chang TS (2005) Controlled elimination of intracellular H2O2: regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification. Antioxid Redox Signal 7:619–626

    CAS  Google Scholar 

  • Sheng GP, Yu HQ (2006) Chemical-equilibrium-based model for describing the strength of sludge: taking hydrogen-producing sludge as an example. Environ Sci Technol 40:1280–1285

    CAS  Google Scholar 

  • Sheng G-P, Yu H-Q, Yue Z-B (2005) Production of extracellular polymeric substances from Rhodopseudomonas acidophila in the presence of toxic substances. Appl Microbiol Biot 69:216–222

    CAS  Google Scholar 

  • Sreerama N, Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287:252–260

    CAS  Google Scholar 

  • Sun M, Li WW, Mu ZX, Wang HL, Yu HQ, Li YY, Harada H (2012) Selection of effective methods for extracting extracellular polymeric substances (EPSs) from Bacillus megaterium TF10. Sep Purif Technol 95:216–221

    CAS  Google Scholar 

  • Wang X-S, Han J-G (2009) Changes of proline content, activity, and active isoforms of antioxidative enzymes in two alfalfa cultivars under salt stress. Agr Sci China 8:431–440

    CAS  Google Scholar 

  • Wang Z, Zhang XX, Lu X, Liu B, Li Y, Long C, Li A (2014) Abundance and diversity of bacterial nitrifiers and denitrifiers and their functional genes in tannery wastewater treatment plants revealed by high-throughput sequencing. PLoS One 9:e113603

    Google Scholar 

  • Wang T, Li J, Zhang LH, Yu Y, Zhu YM (2017) Simultaneous heterotrophic nitrification and aerobic denitrification at high concentrations of NaCl and ammonia nitrogen by Halomonas bacteria. Water Sci Technol 76:386–395

    CAS  Google Scholar 

  • Wang X, An Q, Zhao B, Guo JS, Huang YS, Tian M (2018) Auto-aggregation properties of a novel aerobic denitrifier Enterobacter sp. strain FL. Appl Microbiol Biot 102:2019–2030

    CAS  Google Scholar 

  • Xu FJ, Li G, Jin CW, Liu WJ, Zhang SS, Zhang YS, Lin XY (2012) Aluminum-induced changes in reactive oxygen species accumulation, lipid peroxidation and antioxidant capacity in wheat root tips. Biol Plant 56:89–96

    CAS  Google Scholar 

  • Xu Y, Hou M, Ruan J, Qu M, Sun H, Xu J, Zhou S (2014) Effect of magnetic field on surface properties of Bacillus cereus CrA and its extracellular polymeric substances (EPS). J Adhes Sci Technol 28:2196–2208

    CAS  Google Scholar 

  • Zelko IN, Mariani TJ, Folz RJ (2002) Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 33:337–349

    CAS  Google Scholar 

  • Zhang P, Fang F, Chen YP, Shen Y, Zhang W, Yang JX, Li C, Guo JS, Liu SY, Huang Y, Li S, Gao X, Yan P (2014) Composition of EPS fractions from suspended sludge and biofilm and their roles in microbial cell aggregation. Chemosphere 117:59–65

    CAS  Google Scholar 

  • Zhang P, Chen M, Zhang Y, Li Y, Lu S, Li P (2018) Autoaggregation and adhesion abilities in bacteria associated with colonies of Microcystis. Hydrobiologia 823:205–216

    Google Scholar 

  • Zhao X, Ao Q, Du F, Zhu Q (2011) Conformation analysis of soybean protein in reverse micelles by circular dichroism spectroscopy. Food Anal Method 4:268–275

    Google Scholar 

  • Zhiwei L, Wenhong L, Shangyuan Y, Ping D (2010) Extraction and structural characteristics of extracellular polymeric substances (EPS), pellets in autotrophic nitrifying biofilm and activated sludge. Chemosphere 81:626–632

    Google Scholar 

  • Zhu L, Zhou J, Lv M, Yu H, Zhao H, Xu X (2015) Specific component comparison of extracellular polymeric substances (EPS) in flocs and granular sludge using EEM and SDS-PAGE. Chemosphere 121:26–32

    CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the Special Foundation for State Key Research and Development Program of China (2017YFB0308500), the National Natural Science Foundation of China (31871787), and Talent Training platform construction of Sichuan University (SCUKG017).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chongde Wu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Robert Duran

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, D., Jin, Y., Huang, J. et al. Effect of NaCl on nitrification performance and extracellular polymeric substance characteristic of Klebsiella sp. TN-10. Environ Sci Pollut Res 26, 24900–24910 (2019). https://doi.org/10.1007/s11356-019-05742-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05742-6

Keywords

Navigation