Temporal Resistome and Microbial Community Dynamics in an Intensive Aquaculture Facility with Prophylactic Antimicrobial Treatment

Excessive use of antimicrobials in aquaculture is concerning, given possible environmental ramifications and the potential contribution to the spread of antimicrobial resistance (AR). In this study, we explored seasonal abundance of antimicrobial resistance genes and bacterial community composition...

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Main Authors: Hemant J. Patil, Joao Gatica, Avihai Zolti, Ayana Benet-Perelberg, Alon Naor, Barak Dror, Ashraf Al Ashhab, Sophi Marman, Nur A. Hasan, Rita R. Colwell, Daniel Sher, Dror Minz, Eddie Cytryn
Format: Article
Language:English
Published: MDPI AG 2020-12-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/12/1984
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spelling doaj-c612486a4148473abc4c986336f5d7312020-12-14T00:00:44ZengMDPI AGMicroorganisms2076-26072020-12-0181984198410.3390/microorganisms8121984Temporal Resistome and Microbial Community Dynamics in an Intensive Aquaculture Facility with Prophylactic Antimicrobial TreatmentHemant J. Patil0Joao Gatica1Avihai Zolti2Ayana Benet-Perelberg3Alon Naor4Barak Dror5Ashraf Al Ashhab6Sophi Marman7Nur A. Hasan8Rita R. Colwell9Daniel Sher10Dror Minz11Eddie Cytryn12Institute of Soil, Water and Environmental Sciences, Volcani Center, Agricultural Research Organization, P.O. Box 15159, RishonLezion 7528809, IsraelInstitute of Soil, Water and Environmental Sciences, Volcani Center, Agricultural Research Organization, P.O. Box 15159, RishonLezion 7528809, IsraelInstitute of Soil, Water and Environmental Sciences, Volcani Center, Agricultural Research Organization, P.O. Box 15159, RishonLezion 7528809, IsraelDor Aquaculture Research Station, Fisheries Department, Israel Ministry of Agriculture and Rural Development, Dor 3082000, IsraelDor Aquaculture Research Station, Fisheries Department, Israel Ministry of Agriculture and Rural Development, Dor 3082000, IsraelInstitute of Soil, Water and Environmental Sciences, Volcani Center, Agricultural Research Organization, P.O. Box 15159, RishonLezion 7528809, IsraelThe Dead Sea and Arava Science Center, Masada 86900, IsraelDepartment of Marine Biology, Leon H. Charney School of Marine Sciences, University of Haifa, Haifa 3498838, IsraelCosmosID Inc., Rockville, MD 20742, USACosmosID Inc., Rockville, MD 20742, USADepartment of Marine Biology, Leon H. Charney School of Marine Sciences, University of Haifa, Haifa 3498838, IsraelInstitute of Soil, Water and Environmental Sciences, Volcani Center, Agricultural Research Organization, P.O. Box 15159, RishonLezion 7528809, IsraelInstitute of Soil, Water and Environmental Sciences, Volcani Center, Agricultural Research Organization, P.O. Box 15159, RishonLezion 7528809, IsraelExcessive use of antimicrobials in aquaculture is concerning, given possible environmental ramifications and the potential contribution to the spread of antimicrobial resistance (AR). In this study, we explored seasonal abundance of antimicrobial resistance genes and bacterial community composition in the water column of an intensive aquaculture pond stocked with Silver Carp (<i>Hypophthalmichthys molitrix</i>) prophylactically treated with sulfamethoprim (25% sulfadiazine; 5% trimethoprim), relative to an adjacent unstocked reservoir. Bacterial community composition was monitored using high-throughput sequencing of 16S <i>rRNA</i> gene amplicons in eight sampling profiles to determine seasonal dynamics, representing principal stages in the fish fattening cycle. In tandem, qPCR was applied to assess relative abundance of selected antimicrobial resistance genes (<i>sul1, sul2, dfrA1, tetA </i>and <i>blaTEM</i>) and class-1 integrons (<i>int1</i>). Concomitantly, resistomes were extrapolated from shotgun metagenomes in representative profiles. Analyses revealed increased relative abundance of sulfonamide and tetracycline resistance genes in fishpond-03, relative to pre-stocking and reservoir levels, whereas no significant differences were observed for genes encoding resistance to antimicrobials that were not used in the fishpond-03. Seasons strongly dictated bacterial community composition, with high abundance of cyanobacteria in summer and increased relative abundance of <i>Flavobacterium</i> in the winter. Our results indicate that prophylactic use of sulfonamides in intensive aquaculture ponds facilitates resistance suggesting that prophylactic use of these antimicrobials in aquaculture should be restricted.https://www.mdpi.com/2076-2607/8/12/1984antimicrobialsantimicrobial resistanceaquaculturemetagenomemicrobiomeresistome
collection DOAJ
language English
format Article
sources DOAJ
author Hemant J. Patil
Joao Gatica
Avihai Zolti
Ayana Benet-Perelberg
Alon Naor
Barak Dror
Ashraf Al Ashhab
Sophi Marman
Nur A. Hasan
Rita R. Colwell
Daniel Sher
Dror Minz
Eddie Cytryn
spellingShingle Hemant J. Patil
Joao Gatica
Avihai Zolti
Ayana Benet-Perelberg
Alon Naor
Barak Dror
Ashraf Al Ashhab
Sophi Marman
Nur A. Hasan
Rita R. Colwell
Daniel Sher
Dror Minz
Eddie Cytryn
Temporal Resistome and Microbial Community Dynamics in an Intensive Aquaculture Facility with Prophylactic Antimicrobial Treatment
Microorganisms
antimicrobials
antimicrobial resistance
aquaculture
metagenome
microbiome
resistome
author_facet Hemant J. Patil
Joao Gatica
Avihai Zolti
Ayana Benet-Perelberg
Alon Naor
Barak Dror
Ashraf Al Ashhab
Sophi Marman
Nur A. Hasan
Rita R. Colwell
Daniel Sher
Dror Minz
Eddie Cytryn
author_sort Hemant J. Patil
title Temporal Resistome and Microbial Community Dynamics in an Intensive Aquaculture Facility with Prophylactic Antimicrobial Treatment
title_short Temporal Resistome and Microbial Community Dynamics in an Intensive Aquaculture Facility with Prophylactic Antimicrobial Treatment
title_full Temporal Resistome and Microbial Community Dynamics in an Intensive Aquaculture Facility with Prophylactic Antimicrobial Treatment
title_fullStr Temporal Resistome and Microbial Community Dynamics in an Intensive Aquaculture Facility with Prophylactic Antimicrobial Treatment
title_full_unstemmed Temporal Resistome and Microbial Community Dynamics in an Intensive Aquaculture Facility with Prophylactic Antimicrobial Treatment
title_sort temporal resistome and microbial community dynamics in an intensive aquaculture facility with prophylactic antimicrobial treatment
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2020-12-01
description Excessive use of antimicrobials in aquaculture is concerning, given possible environmental ramifications and the potential contribution to the spread of antimicrobial resistance (AR). In this study, we explored seasonal abundance of antimicrobial resistance genes and bacterial community composition in the water column of an intensive aquaculture pond stocked with Silver Carp (<i>Hypophthalmichthys molitrix</i>) prophylactically treated with sulfamethoprim (25% sulfadiazine; 5% trimethoprim), relative to an adjacent unstocked reservoir. Bacterial community composition was monitored using high-throughput sequencing of 16S <i>rRNA</i> gene amplicons in eight sampling profiles to determine seasonal dynamics, representing principal stages in the fish fattening cycle. In tandem, qPCR was applied to assess relative abundance of selected antimicrobial resistance genes (<i>sul1, sul2, dfrA1, tetA </i>and <i>blaTEM</i>) and class-1 integrons (<i>int1</i>). Concomitantly, resistomes were extrapolated from shotgun metagenomes in representative profiles. Analyses revealed increased relative abundance of sulfonamide and tetracycline resistance genes in fishpond-03, relative to pre-stocking and reservoir levels, whereas no significant differences were observed for genes encoding resistance to antimicrobials that were not used in the fishpond-03. Seasons strongly dictated bacterial community composition, with high abundance of cyanobacteria in summer and increased relative abundance of <i>Flavobacterium</i> in the winter. Our results indicate that prophylactic use of sulfonamides in intensive aquaculture ponds facilitates resistance suggesting that prophylactic use of these antimicrobials in aquaculture should be restricted.
topic antimicrobials
antimicrobial resistance
aquaculture
metagenome
microbiome
resistome
url https://www.mdpi.com/2076-2607/8/12/1984
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