Skip to main content

Advertisement

Log in

Photosynthetic bacteria enhanced water quality and integrity of microbial community composition of integrated multitrophic aquaculture system of milkfish Chanos chanos coastal farming

  • Original Article
  • Aquaculture
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

Aquaculture faces substantial challenges in mitigating the detrimental environmental impacts of intensive farming. Traditional methods have given rise to serious concerns, leading to the search for alternative approaches using probiotics. An indigenously isolated photosynthetic purple bacterium, Rhodovulum sulfidophilum, was introduced into a marine integrated multitrophic aquaculture system cultivating Chanos chanos in southwestern Taiwan. The effects of R. sulfidophilum on water quality parameters, the relative levels of nitrogenase-encoding nifH and nitrous oxide reductase-encoding nosZ genes, the occurrence of sulfonamide resistance, the presence of sulfonamide resistance genes, and microbial community structure were determined. Supplementation with R. sulfidophilum decreased the chemical oxygen demand, the nitrate levels, and the occurrence of sulfonamide-resistant bacteria in the fishpond water compared with that of the control after rearing. The level of the sulfonamide resistance gene sul2 decreased in R. sulfidophilum-supplemented water samples, while the control exhibited an elevated level of sul2 after rearing. Supplementation with R. sulfidophilum also maintained the integrity of the bacterial community structure. In conclusion, our results suggest that R. sulfidophilum is an attractive supplement for enhanced disease emergence control, microbial biodiversity maintenance, and sustainable marine aquaculture practice.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ashbolt NJ, Amézquita A, Backhaus T, Borriello P, Brandt KK, Collignon P, Coors A, Finley R, Gaze WH, Heberer T, Lawrence JR, Larsson DG, McEwen SA, Ryan JJ, Schönfeld J, Silley P, Snape JR, Van den Eede C, Topp E (2013) Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ Health Perspect 121:993–1001

    Article  PubMed  PubMed Central  Google Scholar 

  • Balcázar JL, de Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Múzquiz JL (2006) The role of probiotics in aquaculture. Vet Microbiol 114:173–186

    Article  PubMed  Google Scholar 

  • Bentzon-Tilia M, Sonnenschein EC, Gram L (2016) Monitoring and managing microbes in aquaculture -Towards a sustainable industry. Microb Biotechnol 9:576–584

    Article  PubMed  PubMed Central  Google Scholar 

  • Bothe H, Jost G, Schloter M, Ward BB, Witzel KP (2000) Molecular analysis of ammonia oxidation and denitrification in natural environments. FEMS Microb Rev 24:673–690

    Article  CAS  Google Scholar 

  • Broaders E, Gahan CG, Marchesi JR (2013) Mobile genetic elements of the human gastrointestinal tract: potential for spread of antibiotic resistance genes. Gut Microbes 4:271–280

    Article  PubMed  PubMed Central  Google Scholar 

  • Bryant DA, Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microb 14:488–496

    Article  CAS  Google Scholar 

  • Bull A, Stach J, Ward A, Goodfellow M (2005) Marine actinobacteria: perspectives, challenges, future directions. Antonie Van Leeuwenhoek 87:65–79

    Article  PubMed  Google Scholar 

  • Campbell AM, Fleisher J, Sinigalliano C, White JR, Lopez JV (2015) Dynamics of marine bacterial community diversity of the coastal waters of the reefs, inlets, and wastewater outfalls of southeast Florida. MicrobiologyOpen 4:390–408. https://doi.org/10.1002/mbo3.245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen B, Yang Y, Liang X, Yu K, Zhang T, Li X (2013) Metagenomic profiles of antibiotic resistance genes (ARGs) between human impacted estuary and deep ocean sediments. Environ Sci Technol 47:12753–12760

    Article  CAS  PubMed  Google Scholar 

  • Chopin T, Buschmann AH, Halling C, Troell M, Kautsky N, Neori A, Kraemer GP, Zertuche-Gonzalez JA, Yarish C, Neefus C (2001) Integrating seaweeds into marine aquaculture systems: a key toward sustainability. J Phycol 37:975–986

    Article  Google Scholar 

  • Chun S, Cui Y, Ahn C, Oh H (2018) Improving water quality using settleable microalga Ettlia sp. and the bacterial community in freshwater recirculating aquaculture system of Danio rerio. Water Res 135:112–121

    Article  CAS  PubMed  Google Scholar 

  • COA (2017) Enforcement rules of Veterinary Drugs Control Act. In: Council of Agriculture EYRT, editor, Council of Agriculture, Executive Yuan ROC (Taiwan)

  • Davidson J, Good C, Welsh C, Summerfelt SJ (2014) Comparing the effects of high vs. low nitrate on the health, performance, and welfare of juvenile rainbow trout Oncorhynchus mykiss within water recirculating aquaculture systems. Aquac Eng 59:30–40

    Article  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • FAO (2016) The state of world fisheries and aquaculture. Contributing to food security and nutrition for all. Rome. ISBN 978-92-5-109185-2

  • Foster ZS, Sharpton TJ, Grunwald NJ (2017) Metacoder: an R package for visualization and manipulation of community taxonomic diversity data. PLOS Comput Biol 13:e1005404. https://doi.org/10.1371/journal.pcbi.1005404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillings MR, Gaze WH, Pruden A, Smalla K, Tiedje JM, Zhu Y (2015) Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J 9:1269–1279

    Article  CAS  PubMed  Google Scholar 

  • Harnisz M, Korzeniewska E, Ciesielski S, Golas I (2015) tet genes as indicators of changes in the water environment: relationships between culture-dependent and culture-independent approaches. Sci Total Environ 505:704–711

    Article  CAS  PubMed  Google Scholar 

  • Hatosy SM, Martiny AC (2015) The ocean as a global reservoir of antibiotic resistance genes. Appl Environ Microbiol 81:7593–7599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu JT, Chen CY, Young CW, Chao WL, Li MH, Liu YH, Lin C, Ying C (2014) Prevalence of sulfonamide-resistant bacteria, resistance genes and integron-associated horizontal gene transfer in natural water bodies and soils adjacent to a swine feedlot in northern Taiwan. J Hazard Mater 277:34–43

    Article  CAS  PubMed  Google Scholar 

  • Hsu SF, Buckley DH (2009) Evidence for the functional significance of diazotroph community structure in soil. ISME J 3:124–136

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Jaffé PR (2018) Isolation and characterization of an ammonium-oxidizing iron reducer: Acidimicrobiaceae sp. A6. PLoS ONE 13:e0194007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang L, Xu YB, Xu JX, Ling JY, Chen JL, Zhou JL, Zheng L, Du QP (2017) Antibiotic resistance genes (ARGs) in duck and fish production ponds with integrated or non-integrated mode. Chemosphere 168:1107–1114

    Article  CAS  PubMed  Google Scholar 

  • Hvistendahl M (2012) Public health. China takes aim at rampant antibiotic resistance. Science 336:795

    Article  CAS  PubMed  Google Scholar 

  • Ji B, Yang K, Zhu L, Jiang Y, Wang H, Zhou J, Zhang H (2015) Aerobic denitrification: a review of important advances of the last 30 years. Biotechnol Bioprocess Eng 20:643–651

    Article  CAS  Google Scholar 

  • Kathiravan V, Krishnani KK, Azad IS, Kailasam M, Ponniah AG (2012) Diversity of nitrite oxidizers in greenwater system of coastal aquaculture by metagenomic approach targeting nxrB genes. BioTechnol Indian J 6:359–366

    CAS  Google Scholar 

  • Martínez-Espinosa RM, Cole JA, Richardson DJ, Watmough NJ (2011) Enzymology and ecology of the nitrogen cycle. Biochem Soc Trans 39:175–178

    Article  CAS  PubMed  Google Scholar 

  • Martínez JL (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365–367

    Article  CAS  PubMed  Google Scholar 

  • Maugeri TL, Gugliandolo C, Lentini V (2013) Diversity of prokaryotes at a shallow submarine vent of Panarea Island (Italy) by high-throughput sequencing. Atti della Accademia Peloritana dei Pericolanti-Classe di Scienze Fisiche: Matematiche e Naturali 91:A1. https://doi.org/10.1478/AAPP.912A1

    Article  Google Scholar 

  • Muziasari WI, Managaki S, Parnanen K, Karkman A, Lyra C, Tamminen M, Suzuki S, Virta M (2014) Sulphonamide and trimethoprim resistance genes persist in sediments at Baltic Sea aquaculture farms but are not detected in the surrounding environment. PLoS ONE 9:e92702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penton CR, Yang C, Wu L, Wang Q, Zhang J, Liu F, Qin Y, Deng Y, Hemme CL, Zheng T, Schuur EAG, Tiedje J, Zhou J (2016) NifH-harboring bacterial community composition across an Alaskan permafrost thaw gradient. Front Microbiol 7:1894. https://doi.org/10.3389/fmicb.2016.01894

    Article  PubMed  PubMed Central  Google Scholar 

  • Piedrahita RH (2003) Reducing the potential environmental impact of tank aquaculture effluents through intensification and recirculation. Aquaculture 226:35–44

    Article  CAS  Google Scholar 

  • Qi Z, Zhang X, Boon N, Bossier P (2009) Probiotics in aquaculture of China: current state, problems and prospect. Aquaculture 290:15–21

    Article  Google Scholar 

  • Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554

    Article  CAS  PubMed  Google Scholar 

  • Reed SC, Townsend AR, Cleveland CC, Nemergut DR (2010) Microbial community shifts influence patterns in tropical forest nitrogen fixation. Oecologia 164:521–531

    Article  PubMed  Google Scholar 

  • Shiung I, Chang M, Chang Y, Yeh S, Chang S, Ying C, Chao W (2018) Photosynthetic purple sulfur bacterium Marichromatium purpuratum RuA2 induces changes in water quality parameters, the occurrence of sulfonamide resistance gene and microbial community structure of marine aquaculture. Aquaculture 493:68–78

    Article  CAS  Google Scholar 

  • Su H, Liu S, Hu X, Xu X, Xu W, Xu Y, Li Z, Wen G, Liu Y, Cao Y (2017) Occurrence and temporal variation of antibiotic resistance genes (ARGs) in shrimp aquaculture: ARGs dissemination from farming source to reared organisms. Sci Total Environ 607–608:357–366

    Article  CAS  PubMed  Google Scholar 

  • Suzuki S, Ogo M, Miller TW, Shimizu A, Takada H, Siringan MA (2013) Who possesses drug resistance genes in the aquatic environment?: sulfamethoxazole (SMX) resistance genes among the bacterial community in water environment of Metro-Manila, Philippines. Front Microbiol 4:102. https://doi.org/10.3389/fmicb.2013.00102

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang K, Zhang Y, Lin D, Han Y, Chen C-TA, Wang D, Lin Y-S, Sun J, Zheng Q, Jiao N (2018) Cultivation-independent and cultivation-dependent analysis of microbes in the shallow-sea hydrothermal system off Kueishantao Island, Taiwan: unmasking heterotrophic bacterial diversity and functional capacity. Front Microbiol 9:279. https://doi.org/10.3389/fmicb.2018.00279

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsygankov AA, Khusnutdinova AN (2015) Hydrogen in metabolism of purple bacteria and prospects of practical application. Microbiology 84:1–22

    Article  CAS  Google Scholar 

  • Turk KA, Rees AP, Zehr JP, Pereira N, Swift P, Shelley R, Lohan M, Woodward EMS, Gilbert J (2011) Nitrogen fixation and nitrogenase (nifH) expression in tropical waters of the eastern North Atlantic. ISME J 5:1201–1212

    Article  CAS  PubMed  Google Scholar 

  • Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J (2014) Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci USA 111:15202–15207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Cheung MK, Kwan HS, Hwang JS, Wong CK (2015) Microbial diversity in shallow-water hydrothermal sediments of Kueishan Island, Taiwan as revealed by pyrosequencing. J Basic Microbiol 55:1308–1318

    Article  PubMed  Google Scholar 

  • Wang HL, Zhang J, Sun QL, Lian C, Sun L (2017) A comparative study revealed first insights into the diversity and metabolisms of the microbial communities in the sediments of Pacmanus and Desmos hydrothermal fields. PLoS ONE 12:e0181048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watts JEM, Schreier HJ, Lanska L, Hale MS (2017) The rising tide of antimicrobial resistance in aquaculture: sources, sinks and solutions. Mar Drugs 15:158. https://doi.org/10.3390/md15060158

    Article  CAS  PubMed Central  Google Scholar 

  • Willison J (1993) Biochemical genetics revisited: the use of mutants to study carbon and nitrogen metabolism in the photosynthetic bacteria. FEMS Microb Rev 24:1–38

    Article  Google Scholar 

  • WHO (2014) Antimicrobial resistance: global report on surveillance. World Health Organization, Geneva

    Google Scholar 

  • Wu Y, Lin F, Huang Z, Yeh SL (2014) Cloning of nitrogen fixation genes from photosynthetic bacteria Rhodovulum sulfidophilum. FRI Newslett 46:7–9

    Google Scholar 

  • Yeh SL, Dahms HU, Chiu YJ, Chang SJ, Wang YK (2017) Increased production and water remediation by land-based farm-scale sequentially integrated multi-trophic aquaculture systems—an example from southern Taiwan. Sustainability 9:2173. https://doi.org/10.3390/su9122173

    Article  CAS  Google Scholar 

  • Yildiz H, Robaina L, Pirhonen J, Mente E, Domínguez D, Parisi G (2017) Fish welfare in aquaponic systems: its relation to water quality with an emphasis on feed and faeces—a review. Water 9:13

    Article  Google Scholar 

  • Ying C, Chang MJ, Hu CH, Chang YT, Chao WL, Yeh SL, Chang SJ, Hsu JT (2018) The effects of marine farm-scale sequentially integrated multi-trophic aquaculture systems on microbial community composition, prevalence of sulfonamide-resistant bacteria and sulfonamide resistance gene sul1. Sci Total Environ 643:681–691

    Article  CAS  PubMed  Google Scholar 

  • Zehr JP, Kudela RM (2011) Nitrogen cycle of the open ocean: from genes to ecosystems. Ann Rev Mar Sci 3:197–225

    Article  PubMed  Google Scholar 

  • Zehr JP, Capone DG (1996) Problems and promises of assaying the genetic potential for nitrogen fixation in the marine environment. Microb Ecol 32:263–281

    Article  CAS  PubMed  Google Scholar 

  • Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA 110:3435–3440

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao W, Wang B, Yu G (2018) Antibiotic resistance genes in China: occurrence, risk, and correlation among different parameters. Environ Sci Pollut Res 25:21467–21482

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Chia-Hsin Hu (Soochow University, Taiwan) and Dr. Su-Jung Chang (COA, Taiwan) for their assistance in sampling. Our gratitude also goes to Ya-Chen Lin (Soochow University, Taiwan) for her excellent artwork in the schematic illustration.

Funding

This work was funded in part by the National Ministry of Science and Technology (MOST), Republic of China (MOST 106-2632-B-031-001, MOST 105-2632-B-031-001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chingwen Ying.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 911 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ying, C., Chang, MJ., Chang, YT. et al. Photosynthetic bacteria enhanced water quality and integrity of microbial community composition of integrated multitrophic aquaculture system of milkfish Chanos chanos coastal farming. Fish Sci 86, 329–338 (2020). https://doi.org/10.1007/s12562-019-01387-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-019-01387-z

Keywords

Navigation