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Aquaculture International

, Volume 27, Issue 5, pp 1513–1524 | Cite as

Isolation and characterization of heterotrophic nitrification–aerobic denitrification and sulphur-oxidizing bacterium Paracoccus saliphilus strain SPUM from coastal shrimp ponds

  • Y. D. JafferEmail author
  • H. Sanath Kumar
  • R. Vinothkumar
  • A. B. Irfan
  • N. M. Ishfaq
  • Parvaiz Ahmad Ganie
  • Raja Adil Hussain Bhat
  • A. Vennila
Article
  • 61 Downloads

Abstract

The Paracoccus sp. is one of the best-characterized prokaryote that has served as a model organism to study the dentrification and sulphur oxidation processes. However, its ability of dentrification and sulphur oxidation in coastal shrimp ponds is not reported much. In the present work, the Gram-negative, neutrophilic, facultatively lithoautotrophic bacterium Paracoccus saliphilus strain SPUM isolated from coastal shrimp ponds of Urran, Maharashtra, was studied for its efficiency of simultaneous heterotrophic nitrification–aerobic denitrification and sulphur oxidation processes. The maximum removal rate of nitrite and nitrate was 11.22 ± 0.31 and 14.17 ± 0.31 mg of NO3-N/l respectively after 24 h of incubation, while the sulphate-sulphur production observed was 190 ± 4.3 mg l−1 with a change in pH from 8.0 to 7.4 ± 0.08 after 12 days of incubation. The strain was characterized using universal 16S rRNA gene primers revealing high similarity (> 99%) with Paracoccus saliphilus belonging to α-proteobacteria. The isolate could express sulphate thiolesterase/sulphate thiohydrolase, soxB gene which is essential for sulphur oxidation. From all the results, it has been found that the strain SPUM could play a major role in simultaneous aerobic nitrification/denitrification and sulphur oxidation processes to overcome the toxicity of nitrogenous and sulphur-reducing compounds respectively in coastal aquaculture and wastewater systems.

Keywords

Paracoccus saliphilus Nitrification/denitrification Sulphate thiolesterase/sulphate thiohydrolase Coastal shrimp ponds 

Notes

Acknowledgements

The authors are grateful to Director and Vice-Chancellor, ICAR-Central Institute of Fisheries Education, Mumbai, India, for providing support and necessary facilities to carry out this experiment. The first author would like to thank P. Priti, K. Radhika and K.Rateesh for their help at different stages of this research work.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with animals performed by any of the authors.

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  2. Apha A (2005) WEF, 2005. Standard methods for the examination of water and wastewater. 21:258–259Google Scholar
  3. Bagarinao T, Lantin-Olaguer I (1999) The sulfide tolerance of milkfish and tilapia in relation to fish kills in farms and natural waters in the Philippines. Hydrobiologia 382:137–150CrossRefGoogle Scholar
  4. Baumann B, Snozzi M, Zehnder AJB, van der Meer JR (1996) Dynamics of denitrification activity of Paracoccus denitrificans in continuous culture during aerobic-anaerobic changes. J Bacteriol 178:4367–4374CrossRefGoogle Scholar
  5. Camargo JA, Alonso A (2006) Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environ Int 32:831–849CrossRefGoogle Scholar
  6. Chen Q, Ni J (2011) Heterotrophic nitrification–aerobic denitrification by novel isolated bacteria. J Ind Microbiol Biotechnol 38(9):1305–1310Google Scholar
  7. Chen Q, Ni JR (2012) Ammonium removal by Agrobacterium sp. LAD9 capable of heterotrophic nitrification-aerobic denitrification. J Biosci Bioeng 113:619–623CrossRefGoogle Scholar
  8. Cheng SY, Chen JC (1999) Haemocyanin oxygen affinity and the fractionation of oxyhemocyanin and deoxyhemocyanin for Penaeus monodom exposed to elevated nitrite. Aquat Toxicol 45:35–46CrossRefGoogle Scholar
  9. Crab R, Defoirdt T, Bossier P, Verstraete W (2012) Biofloc technology in aquaculture: beneficial effects and future challenges. Aquaculture 356:351–356CrossRefGoogle Scholar
  10. Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fischer J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259CrossRefGoogle Scholar
  11. Garcia-de-Lomas J, Corzo A, Portillo CM, Gonzalez JM, Andrades JA, Saiz-Jimenez C, Garcia-Robledo E (2007) Nitrate stimulation of indigenous nitrate-reducing, sulfideoxidizing bacterial community in wastewater anaerobic biofilms. Water Res 41:3121–3131CrossRefGoogle Scholar
  12. Ghosh W, Dam B (2009) Biochemistry and molecular biology of lithotrophicsulfur oxidation by taxonomically and ecologically diverse bacteria andarchaea. FEMS Microbiol Rev 33:999–1043CrossRefGoogle Scholar
  13. Gupta AB, Gupta SK (2001) Simultaneous carbon and nitrogen removal from high strength domestic wastewater in an aerobic RBC biofilm. Water Res 35:1714–1722Google Scholar
  14. Hayes MK, Taylor GT, Asto Y, Scranton MI (2006) Vertical distributions of thiosulfate and sulfite in the Cariaco Basin. Limnol Oceanogr 51:280–287CrossRefGoogle Scholar
  15. Hurst CJ, Crawford RL, Garland JL, Lipson DA (eds) 2007. Manual of environmental microbiology. American Society for Microbiology PressGoogle Scholar
  16. Jaffer YD, Purushothaman CS, Sanath Kumar H, Irfan AB, Gireesh-Babu P, Ganie PA, Bhat RAH, Vennila A (2019) A combined approach of 16S rRNA and a functional marker gene, soxB to reveal the diversity of sulphur-oxidising bacteria in thermal springs. Arch Microbiol.  https://doi.org/10.1007/s00203-019-01666-4
  17. Jenkins D, Medsker LL (1964) Brucine method for the determination of nitrate in ocean, estuarine, and fresh waters. Anal Chem 36:610–612CrossRefGoogle Scholar
  18. Joo HS, Hirai M, Shoda M (2006) Piggery wastewater treatment using Alcaligenes faecalis strain No. 4 with heterotrophic nitrification and aerobic denitrification. Water Res 40(16):3029–3036Google Scholar
  19. Jukes TH, Cantor CR (1969) Evolution of protein molecules. Mammalian Protein Metabolism 132Google Scholar
  20. Kelly DP, Shergill JK, Lu WP, Wood AP (1997) Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie Van Leeuwenhoek 71(1–2):95–107CrossRefGoogle Scholar
  21. Kim JK, Park KJ, Cho KS, Nam SW, Park TJ, Bajpai R (2005) Aerobic nitrification–denitrification by heterotrophic Bacillus strains. Bioresour Technol 96(17):1897–1906Google Scholar
  22. Kolmert Å, Wikström P, Hallberg KB (2000) A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures. J Microbiol Methods 41:179–184CrossRefGoogle Scholar
  23. Krom MD, Porter C, Gordin H (1985) Description of the water quality conditions in a semi intensively cultured marine fish pond in Eilat, Israel. Aquaculture 49:141–157CrossRefGoogle Scholar
  24. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  25. Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematics, pp 115–175Google Scholar
  26. Liang SC, Zhao M, Lu L, Wang CL, Zhao LY, Liu WJ (2011) Isolation and characteristic of an aerobic denitrifier with high nitrogen removal efficiency. Afr J Biotechnol 10:10648–10656CrossRefGoogle Scholar
  27. Lin SH, Wu CL (1996) Electrochemical removal nitrite and ammonia for aquaculture. Water Res 30:715–721CrossRefGoogle Scholar
  28. Luo J, Tian G, Lin W (2013) Enrichment, isolation and identification of sulfur oxidizing bacteria from sulfide removing bioreactor. J Environ Sci (China) 25:1393–1399CrossRefGoogle Scholar
  29. Meyer B, Imhoff JF, Kuever J (2007) Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria–evolution of the Sox sulfur oxidation enzyme system. Environ Microbiol 9:2957–2977CrossRefGoogle Scholar
  30. Mignard S, Flandrois JP (2006) 16S rRNA sequencing in routine bacterial identification: a 30-month experiment. J Microbiol Methods 67:574–581CrossRefGoogle Scholar
  31. Mohan TVK, Nancharaiah YV, Venugopalan VP, Sai PMS (2016) Effect of C/N ratio on denitrification of high-strength nitrate wastewater in anoxic granular sludge sequencing batch reactors. Ecol Eng 91:441–448CrossRefGoogle Scholar
  32. Patureau D, Zumstein E, Delgenes JP, Moletta R (2000) Aerobic denitrifiers isolated from diverse natural and managed ecosystems. Microb Ecol 39:145–152CrossRefGoogle Scholar
  33. Petri R, Podgorsek L, Imhoff JF (2001) Phylogeny and distribution of the soxBgene among thiosulfate oxidizing bacteria. FEMS Microbiol Lett 197:171–178CrossRefGoogle Scholar
  34. Ren YX, Yang L, Liang X (2014) The characteristics of a novel heterotrophic nitrifying and aerobic denitrifying bacterium, Acinetobacter junii YB. Bioresour Technol 171:1–9CrossRefGoogle Scholar
  35. Robertson LA, Van Niel EW, Torremans RA, Kuenen JG (1988) Simultaneous nitrification and denitrification in aerobic chemostat cultures of Thiosphaera pantotropha. Appl Environ Microbiol 54:2812–2818Google Scholar
  36. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  37. Shi Z, Zhang Y, Zhou J, Chen M, Wang X (2013) Biological removal of nitrate and ammonium under aerobic atmosphere by Paracoccus versutus LYM. Bioresour Technol 148:144–148CrossRefGoogle Scholar
  38. Starkey RL (1934) Cultivation of organisms concerned in the oxidation of thiosulfate. J Bacteriol 28:365Google Scholar
  39. Takaya N, Antonina M, Catalan-Sakairi MA, Sakaguchi Y, Kato I (2003) Aerobic denitrifying bacteria that produce low levels of nitrous oxide. Appl Environ Microbiol 69:3152–3157CrossRefGoogle Scholar
  40. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 9:3251–3270Google Scholar
  41. Timmons MB, Ebeling JM, Wheaton FW, Summerfelt ST, Vinci BJ (2002) Recirculating Aquaculture Systems, 2nd edn. Cayaga Aqua Ventures, IthacaGoogle Scholar
  42. Tseng IT, Chen JC (2004) The immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus under nitrite stress. Fish Shellfish Immunol 17:325–333CrossRefGoogle Scholar
  43. Tuttle JH, Holmes PE, Jannasch HW (1974) Growth rate stimulation of marine pseudomonads by thiosulfate. Arch Microbiol 99:1–14CrossRefGoogle Scholar
  44. Wang JK (2003) Conceptual design of a microalgae-based recirculating oyster and shrimp system. Aquac Eng 28:37–46CrossRefGoogle Scholar
  45. Wang YB, Xu ZR, Deng YS (2002) Toxicity of ammonia and nitrite to aquaculture and the control measures. Feed Ind 23(12):46–48Google Scholar
  46. Yang XP, Wang SM, Zhang DW, Zhou LX (2011) Isolation and nitrogen removal characteristics of an aerobic heterotrophic nitrifying–denitrifying bacterium, Bacillus subtilis A1. Bioresour Technol 102(2):854–862Google Scholar
  47. Yao S, Ni J, Ma T, Li C (2013) Heterotrophic nitrification and aerobic denitrification at low temperature by a newly isolated bacterium, Acinetobacter sp. HA2. Bioresour Technol 139:80–86CrossRefGoogle Scholar
  48. Zhao B, He YL, Hughes J, Zhang XF (2010) Heterotrophic nitrogen removal by a newly isolated Acinetobacter calcoaceticus HNR. Bioresour Technol 101:5194–5200CrossRefGoogle Scholar
  49. Zhu L, Ding W, Feng LJ, Kong Y, Xu J, Xu XY (2012) Isolation of aerobic denitrifiers and characterization for their potential application in the bioremediation of oligotrophic ecosystem. Bioresour Technol 108:1–7CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Division of Irrigation and Drainage EngineeringICAR-Central Soil Salinity InstituteKarnalIndia
  2. 2.Fisheries Resources, Harvest and Post Harvest DivisionICAR-Central Institute of Fisheries EducationMumbaiIndia
  3. 3.ICAR-Central Marine Fisheries InstituteKochiIndia
  4. 4.College of Fisheries ScienceBirsa Agricultural UniversityRanchiIndia
  5. 5.Division of Fish Nutrition, Biochemistry and PhysiologyICAR-Central Institute of Fisheries EducationMumbaiIndia
  6. 6.Fisheries Resource ManagementICAR-Directorate of Cold Water Fisheries ResearchBhimtalIndia
  7. 7.Fish PathologyICAR-Directorate of Cold Water Fisheries ResearchBhimtalIndia
  8. 8.Division of Crop ProductionICAR-Sugarcane Breeding InstituteCoimbatoreIndia

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