Advertisement

Diversity and bacterial succession of a phototrophic biofilm used as complementary food for shrimp raised in a super-intensive culture

  • Ángel Martín Ortiz-Estrada
  • Teresa Gollas-Galván
  • Luis Rafael Martínez-Córdova
  • Armando Burgos-Hernández
  • Susana María Scheuren-Acevedo
  • Mauricio Emerenciano
  • Marcel Martínez-PorchasEmail author
Article
  • 29 Downloads

Abstract

Biofilm-based systems for shrimp aquaculture have emerged as a novel alternative to improve the water quality and obtain a better performance into ponds using zero or limited water exchange. The aims of this work were (1) to evaluate the production response and water quality of a super-intensive shrimp culture using a phototrophic biofilm as complementary food and (2) to study the bacterial diversity of these biofilms. A trial was performed, consisting of a shrimp culture system using biofilms as food source and a control without biofilms. Results showed that the biofilm-based system had better water quality and shrimp registered a higher growth performance compared to the control. Regarding the taxonomic profile of bacterial populations detected in the biofilm, results revealed that Proteobacteria, Bacteroidetes, and Planctomycetes were the three most abundant phyla; of these, eight bacterial orders belonging Rhizobiales, Clostridiales, Cytophagales, Actinomycetales, Vibrionales, Flavobacterales, Planctomycetales, Chlamydiales, and Rhodobacterales constituted a microbial core maintained over time. Some of these are related to anaerobic and aerobic removal processes of nitrogen. The results of this study are a first approach to understand how the bacterial communities forming biofilms are related to water quality of ponds and production performance of aquaculture farms, and how the microbial succession may cause changes on the taxonomic profile biofilms.

Keywords

Bacterial diversity Litopenaeus vannamei Photoautotrophic biofilm Super-intensive shrimp culture Eco-friendly aquaculture Complementary aquafeed 

Notes

Acknowledgments

We thank MS Estefania Garibay-Valdéz and BS Silvia Cristina Valdéz-Verduzco for their contributions during the trial. The technical support of MS José Luis Niebla-Larreta during bioassay is acknowledged.

Compliance with ethical standards

All procedures involving animals were in accordance with the Guidelines for Ethical Conduct in the Care and Use of Nonhuman Animals in Research.

Conflict of interest

The authors declare that they have no conflict of interests.

References

  1. Al Ashhab A, Herzberg M, Gillor O (2014) Biofouling of reverse-osmosis membranes during tertiary wastewater desalination: microbial community composition. Water Res 50:341–349CrossRefGoogle Scholar
  2. Avendaño-Herrera RE, Riquelme CE (2007) Production of a diatom-bacteria biofilm in a photobioreactor for aquaculture applications. Aquac Eng 36:97–104CrossRefGoogle Scholar
  3. Avnimelech Y (1999) Carbon/nitrogen ratio as a control element in aquaculture systems. Aquaculture 176:227–235CrossRefGoogle Scholar
  4. Bakhshi F, Najdegerami EH, Manaffar R, Tukmechi A, Farah KR (2018) Use of different carbon sources for the biofloc system during the grow-out culture of common carp (Cyprinus carpio L.) fingerlings. Aquaculture 484:259–267CrossRefGoogle Scholar
  5. Becerra-Dorame MJ, Martinez-Cordova LR, Martínez-Porchas M, Hernández-López J, López-Elías JA, Mendoza-Cano F (2014) Effect of using autotrophic and heterotrophic microbial-based-systems for the pre-grown of Litopenaeus vannamei, on the production performance and selected haemolymph parameters. Aquac Res 45:944–948CrossRefGoogle Scholar
  6. Béjà O, Suzuki MT (2008) Photoheterotrophic marine prokaryotes. In: Kirchman DL (ed) Microbial ecology of the oceans, 2nd edn. Wiley & Sons, New York, pp 131–157Google Scholar
  7. Bereschenko L, Stams A, Euverink G, Van Loosdrecht M (2010) Biofilm formation on reverse osmosis membranes is initiated and dominated by Sphingomonas spp. Appl Environ Microbiol 76:2623–2632CrossRefGoogle Scholar
  8. Bratvold D, Browdy CL (2001) Effects of sand sediment and vertical surfaces (AquaMatsTM) on production, water quality, and microbial ecology in an intensive Litopenaeus vannamei culture system. Aquaculture 195:81–94CrossRefGoogle Scholar
  9. Coyne MJ, Comstock LE (2008) Niche-specific features of the intestinal bacteroidales. J Bacteriol 190:736–742CrossRefGoogle Scholar
  10. Dang H, Li T, Chen M, Huang G (2008) Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters. Appl Environ Microbiol 74:52–60CrossRefGoogle Scholar
  11. De Schryver P, Crab R, Defoirdt T, Boon N, Verstraete W (2008) The basics of bio-flocs technology: the added value for aquaculture. Aquaculture 277:125–137CrossRefGoogle Scholar
  12. Emerenciano M, Gaxiola G, Cuzon G (2013) Biofloc technology (BFT): a review for aquaculture application and animal food industry. In: Matovic MD (ed) Biomass now-cultivation and utilization. InTech, Belfast, pp 301–328Google Scholar
  13. Emerenciano M, Martinez-Cordova LR, Martinez-Porchas M, Miranda-Baeza A (2017) Biofloc technology (BFT): A tool for water quality management in aquaculture. In: Tutu H (ed) Water quality. Intech, pp 91–109Google Scholar
  14. Funge-Smith SJ, Briggs MRP (1998) Nutrient budgets in intensive shrimp ponds: implications for sustainability. Aquaculture 164:117–133CrossRefGoogle Scholar
  15. Gao X-Y, Xu Y, Liu Y, Liu Z-P (2011) Bacterial diversity, community structure and function associated with biofilm development in a biological aerated filter in a recirculating marine aquaculture systemGoogle Scholar
  16. Goepel K (2013) Implementing the analytic hierarchy process as a standard method for multi-criteria decision making in corporate enterprises – a new AHP excel template with multiple inputs. In: Proceedings of the international symposium on the analytic hierarchy process, Kuala Lumpur. pp 1–10. Retrieved from: https://bpmsg.com/bpmsg-diversity-calculator-excel/
  17. Gutierrez-Wing MT, Malone RF (2006) Biological filters in aquaculture: trends and research directions for freshwater and marine applications. Aquac Eng 34:163–171CrossRefGoogle Scholar
  18. Khatoon H, Yusoff FM, Banerjee S, Shariff M, Mohamed S (2007) Use of periphytic cyanobacterium and mixed diatoms coated substrate for improving water quality, survival and growth of Penaeus monodon Fabricius postlarvae. Aquaculture 271:196–205CrossRefGoogle Scholar
  19. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1–e1CrossRefGoogle Scholar
  20. Lage OM, Graça AP (2016) Biofilms: an extra coat on macroalgae, algae-organisms for imminent biotechnology. InTechGoogle Scholar
  21. Lee J-W, Nam J-H, Kim Y-H, Lee K-H, Lee D-H (2008) Bacterial communities in the initial stage of marine biofilm formation on artificial surfaces. J Microbiol 46:174–182CrossRefGoogle Scholar
  22. Li Z, Che J, Xie J, Wang G, Yu E, Xia Y, Yu D, Zhang K (2017) Microbial succession in biofilms growing on artificial substratum in subtropical freshwater aquaculture ponds. FEMS Microbiol Lett 364:fnx017CrossRefGoogle Scholar
  23. Martínez-Córdova LR, Emerenciano M, Miranda-Baeza A, Martínez-Porchas M (2015) Microbial-based systems for aquaculture of fish and shrimp: an updated review. Rev Aquac 7:131–148CrossRefGoogle Scholar
  24. Martínez-Córdova LR, Martínez-Porchas M, Porchas-Cornejo MA, Gollas-Galván T, Scheuren-Acevedo SM, Arvayo MA, López-Elías JA, López-Torres MA (2017) Bacterial diversity studied by next-generation sequencing in a mature phototrophic Navicula sp-based biofilm promoted into a shrimp culture system. Aquac Res 48:2047–2054CrossRefGoogle Scholar
  25. Martinez-Porchas M, Martinez-Cordova LR (2012) World aquaculture: environmental impacts and troubleshooting alternatives. Sci World J 2012:9CrossRefGoogle Scholar
  26. Meng F, Zhang H, Yang F, Li Y, Xiao J, Zhang X (2006) Effect of filamentous bacteria on membrane fouling in submerged membrane bioreactor. J Membr Sci 272:161–168CrossRefGoogle Scholar
  27. Nagaraj V, Skillman L, Li D, Foreman A, Xie Z, Ho G (2017) Characterisation of extracellular polysaccharides from bacteria isolated from a full-scale desalination plant. Desalination 418:9–18CrossRefGoogle Scholar
  28. Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124CrossRefGoogle Scholar
  29. Ray A (2012) Biofloc technology for super-intensive shrimp culture. In: Browdy CL (ed) Biofloc technology-a practical guide book, 2nd edn. The World Aquaculture Society, Baton Rouge, pp 167–188Google Scholar
  30. Robinson EH, Li MH (2010) Channel catfish, Ictalurus punctatus, size and feed conversion ratio. J World Aquac Soc 41:829–833CrossRefGoogle Scholar
  31. Ruan Y-J, Guo X-S, Ye Z-Y, Liu Y, Zhu S-M (2015) Bacterial community analysis of different sections of a biofilter in a full-scale marine recirculating aquaculture system. N Am J Aquac 77:318–326CrossRefGoogle Scholar
  32. Rurangwa E, Verdegem MCJ (2015) Microorganisms in recirculating aquaculture systems and their management. Rev Aquac 7:117–130CrossRefGoogle Scholar
  33. Song X, Xue S, Chen Y, Yiming SXXSC (2012) Effect of nano-ecobase on treatment of aquaculture wastewater. Chin J Environ Eng 7:024Google Scholar
  34. Staley J, Fuerst J, Giovannoni S, Schlesner H (1992) The order Planctomycetales and the genera Planctomyces, Pirellula, Gemmata, and Isosphaera. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 3710–3731CrossRefGoogle Scholar
  35. Starke R, Müller M, Gaspar M, Marz M, Küsel K, Totsche KU, von Bergen M, Jehmlich N (2017) Candidate Brocadiales dominates C, N and S cycling in anoxic groundwater of a pristine limestone-fracture aquifer. J Proteome 152:153–160CrossRefGoogle Scholar
  36. Tacon AGJ, Cody JJ, Conquest LD, Divakaran S, Forster IP, Decamp OE (2002) Effect of culture system on the nutrition and growth performance of Pacific white shrimp Litopenaeus vannamei (Boone) fed different diets. Aquac Nutr 8:121–137CrossRefGoogle Scholar
  37. Thakur DP, Lin CK (2003) Water quality and nutrient budget in closed shrimp (Penaeus monodon) culture systems. Aquac Eng 27:159–176CrossRefGoogle Scholar
  38. The World Bank (2014) Fish to 2030: prospects for fisheries and aquaculture. In: Agriculture and environment services discussion paper 03. World Bank report number 83177-GLB. Washington, DC, p 80Google Scholar
  39. Thompson FL, Abreu PC, Wasielesky W (2002) Importance of biofilm for water quality and nourishment in intensive shrimp culture. Aquaculture 203:263–278CrossRefGoogle Scholar
  40. Viau VE, Souza DM, Rodríguez EM, Wasielesky W, Abreu PC, Ballester ELC (2013) Biofilm feeding by postlarvae of the pink shrimp Farfantepenaeus brasiliensis (Decapoda, Penaidae). Aquac Res 44:783–794CrossRefGoogle Scholar
  41. Viau VE, Marciano A, Iriel A, López-Greco LS (2016) Assessment of a biofilm-based culture system within zero water exchange on water quality and on survival and growth of the freshwater shrimp Neocaridina heteropoda heteropoda. Aquac Res 47:2528–2542CrossRefGoogle Scholar
  42. Wood DE, Salzberg SL (2014) Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 15:R46CrossRefGoogle Scholar
  43. Zhu G, Peng Y, Li B, Guo J, Yang Q, Wang S (2008) Biological removal of nitrogen from wastewater. Rev Environ Contam Toxicol 192:159–195CrossRefGoogle Scholar
  44. Zhu S-M, Deng Y-L, Ruan Y-J, Guo X-S, Shi M-M, Shen J-Z (2015) Biological denitrification using poly(butylene succinate) as carbon source and biofilm carrier for recirculating aquaculture system effluent treatment. Bioresour Technol 192:603–610CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Ángel Martín Ortiz-Estrada
    • 1
  • Teresa Gollas-Galván
    • 1
  • Luis Rafael Martínez-Córdova
    • 2
  • Armando Burgos-Hernández
    • 3
  • Susana María Scheuren-Acevedo
    • 1
  • Mauricio Emerenciano
    • 4
  • Marcel Martínez-Porchas
    • 1
    Email author
  1. 1.Coordinación de Tecnología de Alimentos de Origen AnimalCentro de Investigación en Alimentación y Desarrollo A.C. (CIAD)HermosilloMexico
  2. 2.Departamento de Investigaciones Científicas y Tecnológicas (DICTUS)Universidad de SonoraHermosilloMexico
  3. 3.Departamento de Investigación y Posgrado en Alimentos (DIPA)Universidad de SonoraHermosilloMexico
  4. 4.Laboratorio De Aquicultura (LAQ)Universidade Estadual De Santa Catarina (UDESC)Santa CatarinaBrazil

Personalised recommendations