Photosynthetic bacteria enhanced water quality and integrity of microbial community composition of integrated multitrophic aquaculture system of milkfish Chanos chanos coastal farming
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.
KeywordsChanos chanos Microbial composition Antibiotic resistance Water quality Photosynthetic bacteria
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.
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).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
- 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 121:993–1001PubMedPubMedCentralCrossRefGoogle 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 CrossRefPubMedPubMedCentralGoogle Scholar
- COA (2017) Enforcement rules of Veterinary Drugs Control Act. In: Council of Agriculture EYRT, editor, Council of Agriculture, Executive Yuan ROC (Taiwan)Google Scholar
- FAO (2016) The state of world fisheries and aquaculture. Contributing to food security and nutrition for all. Rome. ISBN 978-92-5-109185-2Google 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 277:34–43PubMedCrossRefGoogle 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 6:359–366Google 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 CrossRefGoogle 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:e92702PubMedPubMedCentralCrossRefGoogle 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 CrossRefPubMedPubMedCentralGoogle 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 493:68–78CrossRefGoogle 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 CrossRefPubMedPubMedCentralGoogle 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 CrossRefPubMedPubMedCentralGoogle Scholar
- WHO (2014) Antimicrobial resistance: global report on surveillance. World Health Organization, GenevaGoogle Scholar
- Wu Y, Lin F, Huang Z, Yeh SL (2014) Cloning of nitrogen fixation genes from photosynthetic bacteria Rhodovulum sulfidophilum. FRI Newslett 46:7–9Google 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 643:681–691PubMedCrossRefGoogle Scholar