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Faecal contamination determines bacterial assemblages over natural environmental parameters within intermittently opened and closed lagoons (ICOLLs) during high rainfall

Faecal contamination determines bacterial assemblages over natural environmental parameters within intermittently opened and closed lagoons (ICOLLs) during high rainfall
Faecal contamination determines bacterial assemblages over natural environmental parameters within intermittently opened and closed lagoons (ICOLLs) during high rainfall

Intermittently closed and opened lakes and lagoons (ICOLLs) provide important ecosystem services, including food provision and nutrient cycling. These ecosystems generally experience low watershed outflow, resulting in substantial fluctuations in physicochemical parameters that are often compounded by anthropogenic contamination, however, how this impacts the patterns in microbiology within these environments remains uncharacterised. Therefore, we aimed to determine how seasonal heterogeneity in the physicochemical parameters, in comparison to faecal contamination, alter the dynamics of bacterial communities inhabiting ICOLLs on the eastern Australian coast. To address these aims, we sampled four ICOLLs on a monthly basis for one year, using 16S rRNA gene amplicon sequencing to monitor patterns in bacterial diversity and qPCR-based methods to measure faecal contamination from humans (sewage), dogs, and birds. Additionally, we used qPCR to monitor patterns of a suite of antibiotic resistance genes (ARGs) including sulI, tetA, qnrS, dfrA1, and vanB. Differences in bacterial community composition were often associated with temporal shifts in salinity, temperature, pH, dissolved oxygen, and dissolved organic matter, but following periods of high rainfall, bacterial assemblages in two of four ICOLLs changed in direct response to sewage inputs. Within these ICOLLs, indicator taxa for stormwater identified using the 16S rRNA amplicon sequencing data, as well as markers for sewage and dog faeces, and levels of the antibiotic resistance genes (ARGs) sulI, tetA, and dfrA1 were significantly more abundant after rainfall. Notably many of the stormwater indicator taxa were potential human pathogens including Arcobacter and Aeromonas hydrophilia, which also displayed significant correlations, albeit weak to moderate, with levels of the ARGs sulI, tetA, and dfrA1. This broad-scale shift in the nature of the bacterial community following rainfall will likely lead to a substantial, and perhaps detrimental, divergence in the ecosystem services provided by the bacterial assemblages within these ICOLLs. We conclude that following rainfall events, sewage was a principal driver of shifts in the microbiology of ICOLLs exposed to stormwater, while natural seasonal shifts in the physicochemical parameters controlled bacterial communities at other times. Increased occurrence of intense precipitation events is predicted as a ramification of climate change, which will lead to increased impacts of stormwater and sewage contamination on important ICOLL ecosystems in the future.

Antimicrobial resistance genes (ARGs), Antimicrobial resistant bacteria (ARB), ICOLLS, Indicator species, Microbial source tracking (MST), Rainfall events and faecal contaminatiion
0043-1354
Williams, Nathan L.R.
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Siboni, Nachshon
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Potts, Jaimie
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Scanes, Peter
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Johnson, Colin
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James, Melanie
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McCann, Vanessa
f2eeebde-b278-49dc-bbf7-6e14f286ceee
Reun, Nine Le
d472979d-a2a2-427f-92fe-36ee0ce8a679
King, William L.
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Seymour, Justin R.
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Williams, Nathan L.R.
7dca1dd0-2b53-413d-8499-f2558158265d
Siboni, Nachshon
cd5ba51e-896e-4b3f-be74-ab136fd96675
Potts, Jaimie
a3218b35-ba15-44f3-b907-8c8b23ed7921
Scanes, Peter
f4c9a0f0-fa56-4135-94e3-a09c99efcf35
Johnson, Colin
e50aa9cd-8c61-4fe3-a0b3-f51cc3a6c74a
James, Melanie
17d5fa27-3b03-4c0e-9318-4031ec32455d
McCann, Vanessa
f2eeebde-b278-49dc-bbf7-6e14f286ceee
Reun, Nine Le
d472979d-a2a2-427f-92fe-36ee0ce8a679
King, William L.
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Seymour, Justin R.
9b8a8df1-b392-4a9b-a513-54ea4c7172c7

Williams, Nathan L.R., Siboni, Nachshon, Potts, Jaimie, Scanes, Peter, Johnson, Colin, James, Melanie, McCann, Vanessa, Reun, Nine Le, King, William L. and Seymour, Justin R. (2025) Faecal contamination determines bacterial assemblages over natural environmental parameters within intermittently opened and closed lagoons (ICOLLs) during high rainfall. Water Research, 268, [122670]. (doi:10.1016/j.watres.2024.122670).

Record type: Article

Abstract

Intermittently closed and opened lakes and lagoons (ICOLLs) provide important ecosystem services, including food provision and nutrient cycling. These ecosystems generally experience low watershed outflow, resulting in substantial fluctuations in physicochemical parameters that are often compounded by anthropogenic contamination, however, how this impacts the patterns in microbiology within these environments remains uncharacterised. Therefore, we aimed to determine how seasonal heterogeneity in the physicochemical parameters, in comparison to faecal contamination, alter the dynamics of bacterial communities inhabiting ICOLLs on the eastern Australian coast. To address these aims, we sampled four ICOLLs on a monthly basis for one year, using 16S rRNA gene amplicon sequencing to monitor patterns in bacterial diversity and qPCR-based methods to measure faecal contamination from humans (sewage), dogs, and birds. Additionally, we used qPCR to monitor patterns of a suite of antibiotic resistance genes (ARGs) including sulI, tetA, qnrS, dfrA1, and vanB. Differences in bacterial community composition were often associated with temporal shifts in salinity, temperature, pH, dissolved oxygen, and dissolved organic matter, but following periods of high rainfall, bacterial assemblages in two of four ICOLLs changed in direct response to sewage inputs. Within these ICOLLs, indicator taxa for stormwater identified using the 16S rRNA amplicon sequencing data, as well as markers for sewage and dog faeces, and levels of the antibiotic resistance genes (ARGs) sulI, tetA, and dfrA1 were significantly more abundant after rainfall. Notably many of the stormwater indicator taxa were potential human pathogens including Arcobacter and Aeromonas hydrophilia, which also displayed significant correlations, albeit weak to moderate, with levels of the ARGs sulI, tetA, and dfrA1. This broad-scale shift in the nature of the bacterial community following rainfall will likely lead to a substantial, and perhaps detrimental, divergence in the ecosystem services provided by the bacterial assemblages within these ICOLLs. We conclude that following rainfall events, sewage was a principal driver of shifts in the microbiology of ICOLLs exposed to stormwater, while natural seasonal shifts in the physicochemical parameters controlled bacterial communities at other times. Increased occurrence of intense precipitation events is predicted as a ramification of climate change, which will lead to increased impacts of stormwater and sewage contamination on important ICOLL ecosystems in the future.

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More information

Accepted/In Press date: 19 October 2024
Published date: 1 January 2025
Additional Information: Publisher Copyright: © 2024
Keywords: Antimicrobial resistance genes (ARGs), Antimicrobial resistant bacteria (ARB), ICOLLS, Indicator species, Microbial source tracking (MST), Rainfall events and faecal contaminatiion

Identifiers

Local EPrints ID: 496681
URI: http://eprints.soton.ac.uk/id/eprint/496681
ISSN: 0043-1354
PURE UUID: 1129a6cc-8dd6-4a28-8c09-6351a06439d7
ORCID for William L. King: ORCID iD orcid.org/0000-0001-7272-8242

Catalogue record

Date deposited: 07 Jan 2025 22:01
Last modified: 21 Aug 2025 02:48

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Contributors

Author: Nathan L.R. Williams
Author: Nachshon Siboni
Author: Jaimie Potts
Author: Peter Scanes
Author: Colin Johnson
Author: Melanie James
Author: Vanessa McCann
Author: Nine Le Reun
Author: William L. King ORCID iD
Author: Justin R. Seymour

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