Temporal Bacterial Surveillance of Salmon Aquaculture Sites Indicates a Long Lasting Benthic Impact With Minimal Recovery

Coastal aquaculture has experienced substantial growth in the last few decades and associated impacts on natural environments are of increasing importance. Understanding both the effects of aquaculture on marine ecosystems and the processes of recovery during fallowing periods is crucial for the dev...

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Main Authors: Joost T. P. Verhoeven, Flora Salvo, Robyn Knight, Dounia Hamoutene, Suzanne C. Dufour
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.03054/full
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author Joost T. P. Verhoeven
Flora Salvo
Robyn Knight
Dounia Hamoutene
Suzanne C. Dufour
author_facet Joost T. P. Verhoeven
Flora Salvo
Robyn Knight
Dounia Hamoutene
Suzanne C. Dufour
author_sort Joost T. P. Verhoeven
collection DOAJ
description Coastal aquaculture has experienced substantial growth in the last few decades and associated impacts on natural environments are of increasing importance. Understanding both the effects of aquaculture on marine ecosystems and the processes of recovery during fallowing periods is crucial for the development of a more environmentally sustainable industry. Because bacteria are sensitive to environmental change, surveying fluctuations in bacterial communities is a promising tool for monitoring the status of benthic environments. Here, we used 16S rRNA gene high-throughput sequencing to characterize bacterial communities in flocculent matter samples collected over a period of 3 years and at various distances from cages (0–200 meters) at production and fallow (3–35 months) salmon aquaculture sites in southern Newfoundland to evaluate the environmental impact of aquaculture on predominantly hard-bottom substrates. Bacterial composition analysis revealed four clusters, three of which (defined as “recently disturbed,” “intermediate impact,” and “high impact”) differed markedly from a fourth “low impact” cluster that contained far-field samples collected >500 m from cages. Samples within the high impact group were most often collected directly under cages, whereas those in the intermediate impact group were mainly sampled from 20 to 40 m from cages. Large scale phylum shifts (increases of Bacteroidetes, Firmicutes, Spirochaetes, and decreases in Proteobacteria and Epsilonbacteraeota) and a decline in bacterial diversity were observed in the high impact cluster, indicating significant ecological change. Samples from sites of different fallow duration were found in the high impact cluster, indicating a lack of recovery, even after 35 months of fallowing. Finally, we identified 28 genera as bacterial biomarkers, specific to one or more clusters, including genera associated with organically enriched environments and previously reported in the context of aquaculture impacts. Tracking the relative abundance of biomarkers in relation to different lengths of fallowing in the three more impacted clusters showed that these markers remained significantly above low impact cluster levels at all times, further pointing toward incomplete recovery. Our results suggest that coastal aquaculture on hard-bottom substrates is prone to long lasting impacts on bacterial communities, especially below cages, and that effects can be accurately tracked using bacterial community profiles or specific biomarkers.
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spelling doaj.art-c8c5154c00cb4ab88e5cc826fd18def62022-12-22T03:24:17ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-12-01910.3389/fmicb.2018.03054402703Temporal Bacterial Surveillance of Salmon Aquaculture Sites Indicates a Long Lasting Benthic Impact With Minimal RecoveryJoost T. P. Verhoeven0Flora Salvo1Robyn Knight2Dounia Hamoutene3Suzanne C. Dufour4Department of Biology, Memorial University of Newfoundland, St. John’s, NL, CanadaAquaculture, Biotechnology and Aquatic Animal Health Section, Fisheries and Oceans Canada, Northwest Atlantic Fisheries Center, St. John’s, NL, CanadaDepartment of Biology, Memorial University of Newfoundland, St. John’s, NL, CanadaAquaculture, Biotechnology and Aquatic Animal Health Section, Fisheries and Oceans Canada, Northwest Atlantic Fisheries Center, St. John’s, NL, CanadaDepartment of Biology, Memorial University of Newfoundland, St. John’s, NL, CanadaCoastal aquaculture has experienced substantial growth in the last few decades and associated impacts on natural environments are of increasing importance. Understanding both the effects of aquaculture on marine ecosystems and the processes of recovery during fallowing periods is crucial for the development of a more environmentally sustainable industry. Because bacteria are sensitive to environmental change, surveying fluctuations in bacterial communities is a promising tool for monitoring the status of benthic environments. Here, we used 16S rRNA gene high-throughput sequencing to characterize bacterial communities in flocculent matter samples collected over a period of 3 years and at various distances from cages (0–200 meters) at production and fallow (3–35 months) salmon aquaculture sites in southern Newfoundland to evaluate the environmental impact of aquaculture on predominantly hard-bottom substrates. Bacterial composition analysis revealed four clusters, three of which (defined as “recently disturbed,” “intermediate impact,” and “high impact”) differed markedly from a fourth “low impact” cluster that contained far-field samples collected >500 m from cages. Samples within the high impact group were most often collected directly under cages, whereas those in the intermediate impact group were mainly sampled from 20 to 40 m from cages. Large scale phylum shifts (increases of Bacteroidetes, Firmicutes, Spirochaetes, and decreases in Proteobacteria and Epsilonbacteraeota) and a decline in bacterial diversity were observed in the high impact cluster, indicating significant ecological change. Samples from sites of different fallow duration were found in the high impact cluster, indicating a lack of recovery, even after 35 months of fallowing. Finally, we identified 28 genera as bacterial biomarkers, specific to one or more clusters, including genera associated with organically enriched environments and previously reported in the context of aquaculture impacts. Tracking the relative abundance of biomarkers in relation to different lengths of fallowing in the three more impacted clusters showed that these markers remained significantly above low impact cluster levels at all times, further pointing toward incomplete recovery. Our results suggest that coastal aquaculture on hard-bottom substrates is prone to long lasting impacts on bacterial communities, especially below cages, and that effects can be accurately tracked using bacterial community profiles or specific biomarkers.https://www.frontiersin.org/article/10.3389/fmicb.2018.03054/fullflocculent matteraquaculture microbiologybacterial communitiesbiomarkersbenthic indicatorsbiodiversity
spellingShingle Joost T. P. Verhoeven
Flora Salvo
Robyn Knight
Dounia Hamoutene
Suzanne C. Dufour
Temporal Bacterial Surveillance of Salmon Aquaculture Sites Indicates a Long Lasting Benthic Impact With Minimal Recovery
Frontiers in Microbiology
flocculent matter
aquaculture microbiology
bacterial communities
biomarkers
benthic indicators
biodiversity
title Temporal Bacterial Surveillance of Salmon Aquaculture Sites Indicates a Long Lasting Benthic Impact With Minimal Recovery
title_full Temporal Bacterial Surveillance of Salmon Aquaculture Sites Indicates a Long Lasting Benthic Impact With Minimal Recovery
title_fullStr Temporal Bacterial Surveillance of Salmon Aquaculture Sites Indicates a Long Lasting Benthic Impact With Minimal Recovery
title_full_unstemmed Temporal Bacterial Surveillance of Salmon Aquaculture Sites Indicates a Long Lasting Benthic Impact With Minimal Recovery
title_short Temporal Bacterial Surveillance of Salmon Aquaculture Sites Indicates a Long Lasting Benthic Impact With Minimal Recovery
title_sort temporal bacterial surveillance of salmon aquaculture sites indicates a long lasting benthic impact with minimal recovery
topic flocculent matter
aquaculture microbiology
bacterial communities
biomarkers
benthic indicators
biodiversity
url https://www.frontiersin.org/article/10.3389/fmicb.2018.03054/full
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