Gut Microbiome as a Potential Biomarker in Fish: Dietary Exposure to Petroleum Hydrocarbons and Metals, Metabolic Functions and Cytokine Expression in Juvenile Lates calcarifer

The gut microbiome of fish contains core taxa whose relative abundances are modulated in response to diet, environmental factors, and exposure to toxicogenic chemicals, influencing the health of the host fish. Recent advances in genomics and metabolomics have suggested the potential of microbiome an...

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Main Authors: Spilsbury, Francis, Foysal, Md Javed, Tay, A., Gagnon, Monique
Format: Journal Article
Language:English
Published: FRONTIERS MEDIA SA 2022
Subjects:
Online Access:http://purl.org/au-research/grants/arc/LP170101000
http://hdl.handle.net/20.500.11937/89498
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author Spilsbury, Francis
Foysal, Md Javed
Tay, A.
Gagnon, Monique
author_facet Spilsbury, Francis
Foysal, Md Javed
Tay, A.
Gagnon, Monique
author_sort Spilsbury, Francis
building Curtin Institutional Repository
collection Online Access
description The gut microbiome of fish contains core taxa whose relative abundances are modulated in response to diet, environmental factors, and exposure to toxicogenic chemicals, influencing the health of the host fish. Recent advances in genomics and metabolomics have suggested the potential of microbiome analysis as a biomarker for exposure to toxicogenic compounds. In this 35-day laboratory study, 16S RNA sequencing and multivariate analysis were used to explore changes in the gut microbiome of juvenile Lates calcarifer exposed to dietary sub-lethal doses of three metals: vanadium (20 mg/kg), nickel (480 mg/kg), and iron (470 mg/kg), and to two oils: bunker C heavy fuel oil (HFO) (1% w/w) and Montara, a typical Australian medium crude oil (ACO) (1% w/w). Diversity of the gut microbiome was significantly reduced compared to negative controls in fish exposed to metals, but not petroleum hydrocarbons. The core taxa in the microbiome of negative control fish comprised phyla Proteobacteria (62%), Firmicutes (7%), Planctomycetes (3%), Actinobacteria (2%), Bacteroidetes (1%), and others (25%). Differences in the relative abundances of bacterial phyla of metal-exposed fish were pronounced, with the microbiome of Ni-, V-, and Fe-exposed fish dominated by Proteobacteria (81%), Firmicutes (68%), and Bacteroidetes (48%), respectively. The genus Photobacterium was enriched proportionally to the concentration of polycyclic aromatic hydrocarbons (PAHs) in oil-exposed fish. The probiotic lactic acid bacterium Lactobacillus was significantly reduced in the microbiota of fish exposed to metals. Transcription of cytokines IL-1, IL-10, and TNF-a was significantly upregulated in fish exposed to metals but unchanged in oil-exposed fish compared to negative controls. However, IL-7 was significantly downregulated in fish exposed to V, Ni, Fe, and HFOs. Fish gut microbiome exhibits distinctive changes in response to specific toxicants and shows potential for use as biomarkers of exposure to V, Ni, Fe, and to PAHs present in crude oil.
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institution Curtin University Malaysia
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spelling curtin-20.500.11937-894982022-10-31T03:08:02Z Gut Microbiome as a Potential Biomarker in Fish: Dietary Exposure to Petroleum Hydrocarbons and Metals, Metabolic Functions and Cytokine Expression in Juvenile Lates calcarifer Spilsbury, Francis Foysal, Md Javed Tay, A. Gagnon, Monique Science & Technology Life Sciences & Biomedicine Microbiology barramundi ecotoxicology metals crude oil gut microbiome cytokines bioinformatics biomarkers LACTIC-ACID BACTERIA RIBOSOMAL-RNA GENE WATER HORIZON OIL GULF-OF-MEXICO INTESTINAL MICROBIOTA CRUDE-OIL RAINBOW-TROUT END-POINT ICP-MS RESPONSES The gut microbiome of fish contains core taxa whose relative abundances are modulated in response to diet, environmental factors, and exposure to toxicogenic chemicals, influencing the health of the host fish. Recent advances in genomics and metabolomics have suggested the potential of microbiome analysis as a biomarker for exposure to toxicogenic compounds. In this 35-day laboratory study, 16S RNA sequencing and multivariate analysis were used to explore changes in the gut microbiome of juvenile Lates calcarifer exposed to dietary sub-lethal doses of three metals: vanadium (20 mg/kg), nickel (480 mg/kg), and iron (470 mg/kg), and to two oils: bunker C heavy fuel oil (HFO) (1% w/w) and Montara, a typical Australian medium crude oil (ACO) (1% w/w). Diversity of the gut microbiome was significantly reduced compared to negative controls in fish exposed to metals, but not petroleum hydrocarbons. The core taxa in the microbiome of negative control fish comprised phyla Proteobacteria (62%), Firmicutes (7%), Planctomycetes (3%), Actinobacteria (2%), Bacteroidetes (1%), and others (25%). Differences in the relative abundances of bacterial phyla of metal-exposed fish were pronounced, with the microbiome of Ni-, V-, and Fe-exposed fish dominated by Proteobacteria (81%), Firmicutes (68%), and Bacteroidetes (48%), respectively. The genus Photobacterium was enriched proportionally to the concentration of polycyclic aromatic hydrocarbons (PAHs) in oil-exposed fish. The probiotic lactic acid bacterium Lactobacillus was significantly reduced in the microbiota of fish exposed to metals. Transcription of cytokines IL-1, IL-10, and TNF-a was significantly upregulated in fish exposed to metals but unchanged in oil-exposed fish compared to negative controls. However, IL-7 was significantly downregulated in fish exposed to V, Ni, Fe, and HFOs. Fish gut microbiome exhibits distinctive changes in response to specific toxicants and shows potential for use as biomarkers of exposure to V, Ni, Fe, and to PAHs present in crude oil. 2022 Journal Article http://hdl.handle.net/20.500.11937/89498 10.3389/fmicb.2022.827371 English http://purl.org/au-research/grants/arc/LP170101000 http://creativecommons.org/licenses/by/4.0/ FRONTIERS MEDIA SA fulltext
spellingShingle Science & Technology
Life Sciences & Biomedicine
Microbiology
barramundi
ecotoxicology
metals
crude oil
gut microbiome
cytokines
bioinformatics
biomarkers
LACTIC-ACID BACTERIA
RIBOSOMAL-RNA GENE
WATER HORIZON OIL
GULF-OF-MEXICO
INTESTINAL MICROBIOTA
CRUDE-OIL
RAINBOW-TROUT
END-POINT
ICP-MS
RESPONSES
Spilsbury, Francis
Foysal, Md Javed
Tay, A.
Gagnon, Monique
Gut Microbiome as a Potential Biomarker in Fish: Dietary Exposure to Petroleum Hydrocarbons and Metals, Metabolic Functions and Cytokine Expression in Juvenile Lates calcarifer
title Gut Microbiome as a Potential Biomarker in Fish: Dietary Exposure to Petroleum Hydrocarbons and Metals, Metabolic Functions and Cytokine Expression in Juvenile Lates calcarifer
title_full Gut Microbiome as a Potential Biomarker in Fish: Dietary Exposure to Petroleum Hydrocarbons and Metals, Metabolic Functions and Cytokine Expression in Juvenile Lates calcarifer
title_fullStr Gut Microbiome as a Potential Biomarker in Fish: Dietary Exposure to Petroleum Hydrocarbons and Metals, Metabolic Functions and Cytokine Expression in Juvenile Lates calcarifer
title_full_unstemmed Gut Microbiome as a Potential Biomarker in Fish: Dietary Exposure to Petroleum Hydrocarbons and Metals, Metabolic Functions and Cytokine Expression in Juvenile Lates calcarifer
title_short Gut Microbiome as a Potential Biomarker in Fish: Dietary Exposure to Petroleum Hydrocarbons and Metals, Metabolic Functions and Cytokine Expression in Juvenile Lates calcarifer
title_sort gut microbiome as a potential biomarker in fish: dietary exposure to petroleum hydrocarbons and metals, metabolic functions and cytokine expression in juvenile lates calcarifer
topic Science & Technology
Life Sciences & Biomedicine
Microbiology
barramundi
ecotoxicology
metals
crude oil
gut microbiome
cytokines
bioinformatics
biomarkers
LACTIC-ACID BACTERIA
RIBOSOMAL-RNA GENE
WATER HORIZON OIL
GULF-OF-MEXICO
INTESTINAL MICROBIOTA
CRUDE-OIL
RAINBOW-TROUT
END-POINT
ICP-MS
RESPONSES
url http://purl.org/au-research/grants/arc/LP170101000
http://hdl.handle.net/20.500.11937/89498