Environmental Science and Pollution Research

, Volume 22, Issue 22, pp 18230–18238 | Cite as

Ecological significance of Synergistetes in the biological treatment of tuna cooking wastewater by an anaerobic sequencing batch reactor

  • Cécile Militon
  • Olfa Hamdi
  • Valerie Michotey
  • Marie-Laure Fardeau
  • Bernard Ollivier
  • Hassib Bouallagui
  • Moktar Hamdi
  • Patricia BoninEmail author
Research Article


Lab-scale 2L-anaerobic sequencing batch reactor was operated under mesothermic conditions. The degradation of protein-rich organic matter was determined by chemical oxygen demand, biogas production, and protein-removal activity over the operation. The structure of the microbial community was determined by qPCR and next-generation sequencing on 16S rRNA genes. At the steady state, a very efficient removal of protein (92 %) was observed. Our results demonstrate a decrease of archaeal and bacterial abundance over time. Members of the phylum Synergistetes, with a peculiar emphasis for those pertaining to families Dethiosulfovibrionaceae and Aminiphilaceae, are of major ecological significance regarding the treatment of this industrial wastewater. The prominent role to be played by members of the phylum Synergistetes regarding protein and/or amino acid degradation is discussed.


Anaerobic digestion Tuna effluent Protein-rich effluent Microbial diversity Synergistetes 



We acknowledge the support of Aix Marseille University and CNRS. We thank the Tunisian Government for financial support to OH. We acknowledge S. Guasco for her technical assistance.

Conflict of interest

The authors declare that they have no competing interests.


  1. Achour M, Khelifi O, Bouazizi I, Hamdi M (2000) Design of an integrated bioprocess for the treatment of tuna processing liquid effluents. Process Biochem 35:1013–1017CrossRefGoogle Scholar
  2. ALPHA (1998) Standard methods for water and wastewater examination, 20th edn. American Public Health Association, WashingtonGoogle Scholar
  3. Aspe E, Marti MC, Jara A, Roeckel M (2001) Ammonia inhibition in the anaerobic treatment of fishery effluents. Water Environ Res 73(2):154–164CrossRefGoogle Scholar
  4. Baena S, Fardeau M-L, Labat M, Ollivier B, Thomas P, Garcia J-L, Patel BKC (1998) Aminobacterium colombiense gen nov sp nov, an amino acid-degrading anaerobe isolated from anaerobic sludge. Anaerobe 4:241–250CrossRefGoogle Scholar
  5. Baena S, Fardeau M-L, Labat M, Ollivier B, Garcia J-L, Patel BKC (2000) Aminobacterium mobile sp nov, a new anaerobic amino-acid-degrading bacterium. Int J Syst Evol Microbiol 50:259–264CrossRefGoogle Scholar
  6. Balslev-Olesen P, Lynggaard-Jensen A, Nickelsen C (1990) Pilot-scale experiments on anaerobic treatment of wastewater from a fish processing plant. Water Sci Technol 22(1–2):463–474Google Scholar
  7. Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:241–254CrossRefGoogle Scholar
  8. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Gonzalez Pena A, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336CrossRefGoogle Scholar
  9. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624CrossRefGoogle Scholar
  10. Chen Y, Cheng JJ, Creamer KS (2008) Inhibition of anaerobic digestion process: a review. Bioresour Technol 99:4044–4064CrossRefGoogle Scholar
  11. Chia LJ, Wen CK (2002) Utilization of cooking juice young tuna processed into cannel tuna as condiments: effect of enzymatic hydrolysis and membrane treatment. Fish Sci 68(6):1344–1351CrossRefGoogle Scholar
  12. Chowdhury P, Viraraghavan T, Srinivasan A (2010) Biological treatment processes for fish processing wastewater—a review. Bioresour Technol 101:439–449CrossRefGoogle Scholar
  13. Dridi B, Khelaifa S, Fardeau M-L, Ollivier B, Drancourt M (2012) Tungsten-enhanced growth of methanosphaera. BMC Res notes 5:238–240CrossRefGoogle Scholar
  14. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461CrossRefGoogle Scholar
  15. Einen J, Thorseth IH, Ovreas L (2008) Enumeration of archaea and bacteria in seafloor basalt using real-time quantitative PCR and fluorescence microscopy. Fems Microbiol Lett 282:182–187CrossRefGoogle Scholar
  16. Fardeau ML, Barsotti V, Cayol J-L, Guasco S, Michotey V, Joseph M, Bonin P, Ollivier B (2010) Caldinitratiruptor microaerophilus, gen nov, sp nov isolated from a French hot spring (Chaudes-Aigues, Massif Central): a novel cultivated facultative microaerophilic anaerobic thermophile pertaining to the Symbiobacterium branch within the Firmicutes. Extremophiles 14:241–247CrossRefGoogle Scholar
  17. Godon JJ, Moriniere J, Moletta M, Gaillac M, Bru V, Delgenes JP (2005) Rarity associated with specific ecological niches in the bacterial world: the ‘Synergistes’ example. Environ Microbiol 7:213–224CrossRefGoogle Scholar
  18. Gonzalez JF (1996) Wastewater treatment in the fishery industry FAO Fisheries Technical Paper (FAO), No 355/FAO, Rome (Italy), Fisheries DeptGoogle Scholar
  19. Good IL (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264CrossRefGoogle Scholar
  20. Hamdi O, Ben Hania W, Postec A, Bouallagui H, Hamdi M, Bonin P, Ollivier B, Fardeau ML (2014) Aminobacterium thunnarium sp. nov., a mesophilic, amino acid-degrading bacterium isolated from an anaerobic sludge digester, pertaining to the phylum Synergistetes. Int J Syst Evol Microbiol. doi: 10.1099/ijs.0.068965-0 Google Scholar
  21. Honda T, Fujita T, Tonouchi A (2013) Aminovibrio pyruvatiphilus gen. nov, sp Nov, an anaerobic, amino-acid-degrading bacterium from the soil of a Japanese rice field. Int J Syst Evol Microbiol 63:3679–3686CrossRefGoogle Scholar
  22. Huilinir C, Roa E, Vargas D, Roeckel M, Aspe E (2008) Kinetics of syntrophic acetogenesis in a saline medium. J Chem Tech Biotechnol 83:1433–1440CrossRefGoogle Scholar
  23. Jaouen P, Quéméneur F (1992) Fish processing technology, hall, GM, 212–248. Blackie & Son Ltd, GlasgowGoogle Scholar
  24. Jumas-Bilak E, Roudiere L, Marchandin H (2009) Description of ‘Synergistetes’ phyl nov and emended description of the phylum ‘Deferribacteres’ and of the family Syntrophomonadaceae, phylum ‘Firmicutes’. Int J Syst Evol Microbiol 59:1028–1035CrossRefGoogle Scholar
  25. Kapley A, De Baere T, Purohit HJ (2007a) Eubacterial diversity of activated biomass from a common effluent treatment plant. Res Microbiol 158:494–500CrossRefGoogle Scholar
  26. Kapley A, Prasad S, Purohit HJ (2007b) Changes in microbial diversity in fed-batch reactor operation with wastewater containing nitroaromatic residues. Bioresour Technol 98:2479–2484CrossRefGoogle Scholar
  27. Kaspar HF, Wuhrmann K (1978) Kinetic parameters and relative turnovers of some important catabolic reactions in digesting sludge. Appl Environ Microbiol 36:1–7Google Scholar
  28. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights DA, Reyes J, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821CrossRefGoogle Scholar
  29. Lefebvre O, Moletta R (2006) Treatment of organic pollution in industrial saline wastewater: a literature review. Water Res 40:3671–3682CrossRefGoogle Scholar
  30. Liu Y, Zhang T, Fang HHP (2005) Microbial community analysis and performance of phosphate removing activated sludge. Bioresour Technol 96:1205–1214CrossRefGoogle Scholar
  31. Manefield M, Griffiths RI, Leigh MB, Fisher R, Andrew SW (2005) Functional and compositional comparison of two activated sludge communities remediating cooking effluent. Environ Microbiol 7:715–722CrossRefGoogle Scholar
  32. Mata-Alvarez J (2003) Biomethanization of the organic fraction of municipal solid wastes. IWA Publishing, London, p 323Google Scholar
  33. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610–618CrossRefGoogle Scholar
  34. Michotey V, Guasco S, Boeuf D, Morezzi N, Durieux B, Charpy L, Bonin P (2012) Spatio-temporal diversity of free-living and particle-attached prokaryotes in the tropical lagoon of Ahe atoll (Tuamotu Archipelago) and its surrounding oceanic waters. Mar Pollut Bull 65:525–537CrossRefGoogle Scholar
  35. Möller B, Hippe H, Gottschalk G (1986) Degradation of various amine compounds by mesophilic Clostridia. Arch Microbiol 1145:85–90CrossRefGoogle Scholar
  36. Nie Y, Liu H, Du G, Chen J (2008) Acetate yield increased by gas circulation and fed batch fermentation in a novel syntrophic acetogenesis and homoacetogenesis coupling system. Bioresour Technol 99:2989–2995CrossRefGoogle Scholar
  37. Palenzuela-Rollon A, Zeeman G, Lubberding HJ, Lettinga G, Alaerts GJ (2002) Treatment of fish processing wastewater in a one- or two-step upflow anaerobic sludge blanket (UASB) reactor. Water Sci Technol 45(10):207–212Google Scholar
  38. Sawyer CN, McCarty PL (1967) Chemistry for sanitary engineers, 2nd edn. McGraw, Hill Book Co, New YorkGoogle Scholar
  39. Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61(2):262–280Google Scholar
  40. Soto M, Mendes R, Lema JM (1991) Biodegradability and toxicity in the anaerobic treatment of fish canning wastewaters. Environ Technol 12:667–669CrossRefGoogle Scholar
  41. Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:50–66Google Scholar
  42. Toumi J, Bouallagui H, Hamdi M, Nouira S (2010) Improvement of dairy manufacture effluent anaerobic digestion with biological waste addition using a Chinese dome digester. Bioresour Technol 101:3743–3746CrossRefGoogle Scholar
  43. Vartoukian SR, Palmer RM, Wade WG (2007) The division “Synergistes”. Anaerobe 13:99–106CrossRefGoogle Scholar
  44. Veiga MC, Méndez R, Lema JM (1994) Waste water treatment for fisheries operations. In Fisheries Processing . Springer US, pp 344–369Google Scholar
  45. Walha K, Ben Amar R, Bourseau P, Jaouen P (2009) Nanofiltration of concentrated and salted tuna cooking juices. Process Saf Environ 87:331–335CrossRefGoogle Scholar
  46. Yenigüm O, Dermirel B (2013) Ammonia inhibition in anaerobic digestion: review. Process Biochem 48:901–911CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Cécile Militon
    • 1
  • Olfa Hamdi
    • 1
    • 2
  • Valerie Michotey
    • 1
  • Marie-Laure Fardeau
    • 1
  • Bernard Ollivier
    • 1
  • Hassib Bouallagui
    • 2
  • Moktar Hamdi
    • 2
  • Patricia Bonin
    • 1
    Email author
  1. 1.Aix Marseille Université, CNRS, Université de Toulon, IRD, MIO UM 110MarseilleFrance
  2. 2.Laboratoire d’écologie et biotechnologie microbienne, Institut National des Sciences AppliquéesUniversité de CarthageTunis CedexTunisie

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