Skip to main content
SpringerLink
Log in

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

  • Published:
Aquaculture International Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

  • Al Ashhab A, Herzberg M, Gillor O (2014) Biofouling of reverse-osmosis membranes during tertiary wastewater desalination: microbial community composition. Water Res 50:341–349

    Article  PubMed  CAS  Google Scholar 

  • Avendaño-Herrera RE, Riquelme CE (2007) Production of a diatom-bacteria biofilm in a photobioreactor for aquaculture applications. Aquac Eng 36:97–104

    Article  Google Scholar 

  • Avnimelech Y (1999) Carbon/nitrogen ratio as a control element in aquaculture systems. Aquaculture 176:227–235

    Article  CAS  Google Scholar 

  • 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 484:259–267

    Article  CAS  Google Scholar 

  • 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 45:944–948

    Article  Google Scholar 

  • Béjà O, Suzuki MT (2008) Photoheterotrophic marine prokaryotes. In: Kirchman DL (ed) Microbial ecology of the oceans, 2nd edn. Wiley & Sons, New York, pp 131–157

    Google Scholar 

  • 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 76:2623–2632

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 195:81–94

    Article  Google Scholar 

  • Coyne MJ, Comstock LE (2008) Niche-specific features of the intestinal bacteroidales. J Bacteriol 190:736–742

    Article  PubMed  CAS  Google Scholar 

  • 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 74:52–60

    Article  PubMed  CAS  Google Scholar 

  • De Schryver P, Crab R, Defoirdt T, Boon N, Verstraete W (2008) The basics of bio-flocs technology: the added value for aquaculture. Aquaculture 277:125–137

    Article  CAS  Google Scholar 

  • 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 301–328

    Google Scholar 

  • 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 91–109

  • Funge-Smith SJ, Briggs MRP (1998) Nutrient budgets in intensive shrimp ponds: implications for sustainability. Aquaculture 164:117–133

    Article  Google Scholar 

  • 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 system

  • 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/

  • Gutierrez-Wing MT, Malone RF (2006) Biological filters in aquaculture: trends and research directions for freshwater and marine applications. Aquac Eng 34:163–171

    Article  Google Scholar 

  • 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 271:196–205

    Article  CAS  Google Scholar 

  • 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–e1

    Article  PubMed  CAS  Google Scholar 

  • Lage OM, Graça AP (2016) Biofilms: an extra coat on macroalgae, algae-organisms for imminent biotechnology. InTech

  • 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 46:174–182

    Article  PubMed  CAS  Google Scholar 

  • 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:fnx017

    Article  CAS  Google Scholar 

  • 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 7:131–148

    Article  Google Scholar 

  • 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 48:2047–2054

    Article  CAS  Google Scholar 

  • Martinez-Porchas M, Martinez-Cordova LR (2012) World aquaculture: environmental impacts and troubleshooting alternatives. Sci World J 2012:9

    Article  Google Scholar 

  • 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 272:161–168

    Article  CAS  Google Scholar 

  • 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 418:9–18

    Article  CAS  Google Scholar 

  • Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 167–188

    Google Scholar 

  • Robinson EH, Li MH (2010) Channel catfish, Ictalurus punctatus, size and feed conversion ratio. J World Aquac Soc 41:829–833

    Article  Google Scholar 

  • 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 77:318–326

    Article  Google Scholar 

  • Rurangwa E, Verdegem MCJ (2015) Microorganisms in recirculating aquaculture systems and their management. Rev Aquac 7:117–130

    Article  Google Scholar 

  • Song X, Xue S, Chen Y, Yiming SXXSC (2012) Effect of nano-ecobase on treatment of aquaculture wastewater. Chin J Environ Eng 7:024

    Google Scholar 

  • 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 3710–3731

    Chapter  Google Scholar 

  • 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 152:153–160

    Article  CAS  Google Scholar 

  • 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 8:121–137

    Article  Google Scholar 

  • Thakur DP, Lin CK (2003) Water quality and nutrient budget in closed shrimp (Penaeus monodon) culture systems. Aquac Eng 27:159–176

    Article  Google Scholar 

  • 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 80

  • Thompson FL, Abreu PC, Wasielesky W (2002) Importance of biofilm for water quality and nourishment in intensive shrimp culture. Aquaculture 203:263–278

    Article  Google Scholar 

  • 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 44:783–794

    Article  Google Scholar 

  • 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 47:2528–2542

    Article  CAS  Google Scholar 

  • Wood DE, Salzberg SL (2014) Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 15:R46

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu G, Peng Y, Li B, Guo J, Yang Q, Wang S (2008) Biological removal of nitrogen from wastewater. Rev Environ Contam Toxicol 192:159–195

    Article  PubMed  CAS  Google Scholar 

  • 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 192:603–610

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Coordinación de Tecnología de Alimentos de Origen Animal, Centro de Investigación en Alimentación y Desarrollo A.C. (CIAD), Carretera a La Victoria km. 0.6, 83304, Hermosillo, Sonora, Mexico

    Ángel Martín Ortiz-Estrada, Teresa Gollas-Galván, Susana María Scheuren-Acevedo & Marcel Martínez-Porchas

  2. Departamento de Investigaciones Científicas y Tecnológicas (DICTUS), Universidad de Sonora, Blvd. Luis Donaldo Colosio S/N, Col. Centro, Hermosillo, Sonora, Mexico

    Luis Rafael Martínez-Córdova

  3. Departamento de Investigación y Posgrado en Alimentos (DIPA), Universidad de Sonora, Blvd. Luis Encinas y Rosales S/N, Col. Centro, CP 83000, Hermosillo, Sonora, Mexico

    Armando Burgos-Hernández

  4. Laboratorio De Aquicultura (LAQ), Universidade Estadual De Santa Catarina (UDESC), Laguna, Santa Catarina, Brazil

    Mauricio Emerenciano

Authors
  1. Ángel Martín Ortiz-Estrada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teresa Gollas-Galván
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luis Rafael Martínez-Córdova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Armando Burgos-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Susana María Scheuren-Acevedo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mauricio Emerenciano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcel Martínez-Porchas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcel Martínez-Porchas.

Ethics declarations

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.

Additional information

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

Ortiz-Estrada, Á.M., Gollas-Galván, T., Martínez-Córdova, L.R. et al. Diversity and bacterial succession of a phototrophic biofilm used as complementary food for shrimp raised in a super-intensive culture. Aquacult Int 27, 581–596 (2019). https://doi.org/10.1007/s10499-019-00345-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-019-00345-x

Keywords

Search

Navigation