Antibiotic supplement in feed can perturb the intestinal microbial composition and function in Pacific white shrimp
The intestinal microbiota plays crucial roles in host health. The Pacific white shrimp is one of the most profitable aquaculture species in the world. Antibiotic supplement in feed is an optional practice to treat shrimp bacterial diseases. However, little is known about antibiotic effects on intestinal microbiota in pacific white shrimp. Here, shrimps were given feed supplemented with ciprofloxacin (Cip) (40 and 80 mg kg−1) and sulfonamide (Sul) (200 and 400 mg kg−1) to investigate the microbial community by targeting the V4 region of 16S rRNA genes. Within 4 days after feeding with normal feed and with antibiotics, antibiotic concentrations of Cip and Sul groups in the intestine dropped sharply. Significantly, increased abundance of antibiotic resistance genes (ARGs) of ciprofloxacin (qnrB, qnrD, and qnrS) and sulfonamide (sul1, sul2, and sul3) was observed in Cip and Sul groups (P < 0.05). A total of 3191 operational taxonomic units (OTUs) were obtained and 41 phyla were identified from 63 samples in shrimp intestine. The numbers of OTUs and Shannon index decreased rapidly at day 1 (the first day after feeding with antibiotics) and increased at day 3 (the third day after feeding with antibiotics). The relative abundance of dominant phyla and genera in Cip and Sul groups were significantly different from that in the control group (Ctrl). Furthermore, functional potentials that were related to amino acid metabolism, carbohydrate metabolism, and cellular processes and signaling varied significantly in Cip and Sul groups. These results point to an antibiotic-induced shift in shrimp intestinal microbiota, which highlights the importance of considering the microbiota in shrimp health management.
KeywordsAntibiotics Antibiotic resistance genes Intestinal microbiota Microbial composition Functional prediction Pacific white shrimp
This work was financially supported by the China Agriculture Research System (CARS-48), the Guangzhou Science Technology and Innovation Commission Project (201510010071), and the Guangdong Ocean and Fishery Bureau Project (20164200042090023).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflicts of interest.
This article does not contain any studies with human participants by any of the authors. No specific permits were required for the described field studies. No specific permissions were required for access to the artificial pond in Maoming, Guangdong Province, China. The field studies did not involve endangered or protected species. This study was reviewed and approved by the ethics committee of Sun Yat-sen University.
- Abubucker S, Segata N, Goll J, Schubert AM, Izard J, Cantarel BL, Rodriguez-Mueller B, Zucker J, Thiagarajan M, Henrissat B, White O, Kelley ST, Methe B, Schloss PD, Gevers D, Mitreva M, Huttenhower C (2012) Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLoS Comput Biol 8(6):e1002358. https://doi.org/10.1371/journal.pcbi.1002358 CrossRefGoogle Scholar
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, 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):335–336. https://doi.org/10.1038/nmeth.f.303 CrossRefGoogle Scholar
- DeLorenzo ME, Brooker J, Chung KW, Kelly M, Martinez J, Moore JG, Thomas M (2016) Exposure of the grass shrimp, Palaemonetes pugio, to antimicrobial compounds affects associated Vibrio bacterial density and development of antibiotic resistance. Environ Toxicol 31(4):469–477. https://doi.org/10.1002/tox.22060 CrossRefGoogle Scholar
- FAO (2018) Global aquaculture production. http://www.fao.org/fishery/statistics/collections/en. Accessed July 2018
- Flores-Miranda BM, Espinosa-Plascencia A, Gomez-Jimenez S, Lopez-Zavala AA, Gonzalez-Carrillo HH, Bermudez-Almada Mdel C (2012) Accumulation and elimination of enrofloxacin and ciprofloxacin in tissues of shrimp Litopenaeus vannamei under laboratory and farm conditions. ISRN Pharm 2012:374212. https://doi.org/10.5402/2012/374212 Google Scholar
- Hollister EB, Riehle K, Luna RA, Weidler EM, Rubio-Gonzales M, Mistretta T-A, Raza S, Doddapaneni HV, Metcalf GA, Muzny DM, Gibbs RA, Petrosino JF, Shulman RJ, Versalovic J (2015) Structure and function of the healthy pre-adolescent pediatric gut microbiome. Microbiome 3:36. https://doi.org/10.1186/s40168-015-0101-x CrossRefGoogle Scholar
- Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, 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(9):814–821. https://doi.org/10.1038/nbt.2676 CrossRefGoogle Scholar
- LeBlanc JG, Chain F, Martin R, Bermudez-Humaran LG, Courau S, Langella P (2017) Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microb Cell Factories 16(1):79. https://doi.org/10.1186/s12934-017-0691-z CrossRefGoogle Scholar
- Lee C-T, Chen IT, Yang Y-T, Ko T-P, Huang Y-T, Huang J-Y, Huang M-F, Lin S-J, Chen C-Y, Lin S-S, Lightner DV, Wang H-C, Wang AHJ, Wang H-C, Hor L-I, Lo C-F (2015) The opportunistic marine pathogen Vibrio parahaemolyticus becomes virulent by acquiring a plasmid that expresses a deadly toxin. Proc Natl Acad Sci U S A 112(34):10798–10803. https://doi.org/10.1073/pnas.1503129112 CrossRefGoogle Scholar
- Nobel YR, Cox LM, Kirigin FF, Bokulich NA, Yamanishi S, Teitler I, Chung J, Sohn J, Barber CM, Goldfarb DS, Raju K, Abubucker S, Zhou Y, Ruiz VE, Li H, Mitreva M, Alekseyenko AV, Weinstock GM, Sodergren E, Blaser MJ (2015) Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment. Nat Commun 6:7486. https://doi.org/10.1038/ncomms8486 CrossRefGoogle Scholar
- Pham DK, Chu J, Do NT, Brose F, Degand G, Delahaut P, De Pauw E, Douny C, Nguyen KV, Vu TD, Scippo ML, Wertheim HF (2015) Monitoring antibiotic use and residue in freshwater aquaculture for domestic use in Vietnam. Ecohealth 12(3):480–489. https://doi.org/10.1007/s10393-014-1006-z CrossRefGoogle Scholar
- Puhl NJ, Uwiera RR, Yanke LJ, Selinger LB, Inglis GD (2012) Antibiotics conspicuously affect community profiles and richness, but not the density of bacterial cells associated with mucosa in the large and small intestines of mice. Anaerobe 18(1):67–75. https://doi.org/10.1016/j.anaerobe.2011.12.007 CrossRefGoogle Scholar
- Rashid MU, Zaura E, Buijs MJ, Keijser BJ, Crielaard W, Nord CE, Weintraub A (2015) Determining the long-term effect of antibiotic administration on the human normal intestinal microbiota using culture and pyrosequencing methods. Clin Infect Dis 60(Suppl 2):S77–S84. https://doi.org/10.1093/cid/civ137 CrossRefGoogle Scholar
- Tetzner NF, Maniero MG, Rodrigues-Silva C, Rath S (2016) On-line solid phase extraction-ultra high performance liquid chromatography-tandem mass spectrometry as a powerful technique for the determination of sulfonamide residues in soils. J Chromatogr A 1452:89–97. https://doi.org/10.1016/j.chroma.2016.05.034 CrossRefGoogle Scholar
- Zhang C, Yu M, Yang Y, Mu C, Su Y, Zhu W (2017) Differential effect of early antibiotic intervention on bacterial fermentation patterns and mucosal gene expression in the colon of pigs under diets with different protein levels. Appl Microbiol Biotechnol 101(6):2493–2505. https://doi.org/10.1007/s00253-016-7985-7 CrossRefGoogle Scholar