Time Series Resolution of the Fish Necrobiome Reveals a Decomposer Succession Involving Toxigenic Bacterial Pathogens

ABSTRACT Despite progress understanding microbial communities involved in terrestrial vertebrate decomposition, little is known about the microbial decomposition of aquatic vertebrates from a functional and environmental context. Here, we analyzed temporal changes in the “necrobiome” of rainbow dart...

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Autores principales:	Briallen Lobb, Rhiannon Hodgson, Michael D. J. Lynch, Michael J. Mansfield, Jiujun Cheng, Trevor C. Charles, Josh D. Neufeld, Paul M. Craig, Andrew C. Doxey
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	necrobiome microbiome decomposition wastewater rainbow darter Aeromonas Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/59795a052e7249a3806cc1026d7d2586
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spelling	oai:doaj.org-article:59795a052e7249a3806cc1026d7d25862021-12-02T19:46:20ZTime Series Resolution of the Fish Necrobiome Reveals a Decomposer Succession Involving Toxigenic Bacterial Pathogens10.1128/mSystems.00145-202379-5077https://doaj.org/article/59795a052e7249a3806cc1026d7d25862020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00145-20https://doaj.org/toc/2379-5077ABSTRACT Despite progress understanding microbial communities involved in terrestrial vertebrate decomposition, little is known about the microbial decomposition of aquatic vertebrates from a functional and environmental context. Here, we analyzed temporal changes in the “necrobiome” of rainbow darters, which are common North American fish that are sensitive indicators of water quality. By combining 16S rRNA gene and shotgun metagenomic sequence data from four time points, we studied the progression of decomposers from both taxonomic and functional perspectives. The 16S rRNA gene profiles revealed strong community succession, with early decomposition stages associated with Aeromonas and Clostridium taxa and later stages dominated by members of the Rikenellaceae (i.e., Alistipes/Acetobacteroides genera). These results were reproducible and independent of environmental perturbation, given that exposure to wastewater treatment plant effluent did not substantially influence the necrobiome composition of fish or the associated water sample microbiota. Metagenomic analysis revealed significant changes throughout decomposition in degradation pathways for amino acids, carbohydrates/glycans, and other compounds, in addition to putrefaction pathways for production of putrescine, cadaverine, and indole. Binning of contigs confirmed a predominance of Aeromonas genome assemblies, including those from novel strains related to the pathogen Aeromonas veronii. These bins of Aeromonas genes also encoded known hemolysin toxins (e.g., aerolysin) that were particularly abundant early in the process, potentially contributing to host cell lysis during decomposition. Overall, our results demonstrate that wild-caught fish have a reproducible decomposer succession and that the fish necrobiome serves as a potential source of putative pathogens and toxigenic bacteria. IMPORTANCE The microbial decomposition of animal tissues is an important ecological process that impacts nutrient cycling in natural environments. We studied the microbial decomposition of a common North American fish (rainbow darters) over four time points, combining 16S rRNA gene and shotgun metagenomic sequence data to obtain both taxonomic and functional perspectives. Our data revealed a strong community succession that was reproduced across different fish and environments. Decomposition time point was the main driver of community composition and functional potential; fish environmental origin (upstream or downstream of a wastewater treatment plant) had a secondary effect. We also identified strains related to the putative pathogen Aeromonas veronii as dominant members of the decomposition community. These bacteria peaked early in decomposition and coincided with the metagenomic abundance of hemolytic toxin genes. Our work reveals a strong decomposer succession in wild-caught fish, providing functional and taxonomic insights into the vertebrate necrobiome.Briallen LobbRhiannon HodgsonMichael D. J. LynchMichael J. MansfieldJiujun ChengTrevor C. CharlesJosh D. NeufeldPaul M. CraigAndrew C. DoxeyAmerican Society for Microbiologyarticlenecrobiomemicrobiomedecompositionwastewaterrainbow darterAeromonasMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	necrobiome microbiome decomposition wastewater rainbow darter Aeromonas Microbiology QR1-502
spellingShingle	necrobiome microbiome decomposition wastewater rainbow darter Aeromonas Microbiology QR1-502 Briallen Lobb Rhiannon Hodgson Michael D. J. Lynch Michael J. Mansfield Jiujun Cheng Trevor C. Charles Josh D. Neufeld Paul M. Craig Andrew C. Doxey Time Series Resolution of the Fish Necrobiome Reveals a Decomposer Succession Involving Toxigenic Bacterial Pathogens
description	ABSTRACT Despite progress understanding microbial communities involved in terrestrial vertebrate decomposition, little is known about the microbial decomposition of aquatic vertebrates from a functional and environmental context. Here, we analyzed temporal changes in the “necrobiome” of rainbow darters, which are common North American fish that are sensitive indicators of water quality. By combining 16S rRNA gene and shotgun metagenomic sequence data from four time points, we studied the progression of decomposers from both taxonomic and functional perspectives. The 16S rRNA gene profiles revealed strong community succession, with early decomposition stages associated with Aeromonas and Clostridium taxa and later stages dominated by members of the Rikenellaceae (i.e., Alistipes/Acetobacteroides genera). These results were reproducible and independent of environmental perturbation, given that exposure to wastewater treatment plant effluent did not substantially influence the necrobiome composition of fish or the associated water sample microbiota. Metagenomic analysis revealed significant changes throughout decomposition in degradation pathways for amino acids, carbohydrates/glycans, and other compounds, in addition to putrefaction pathways for production of putrescine, cadaverine, and indole. Binning of contigs confirmed a predominance of Aeromonas genome assemblies, including those from novel strains related to the pathogen Aeromonas veronii. These bins of Aeromonas genes also encoded known hemolysin toxins (e.g., aerolysin) that were particularly abundant early in the process, potentially contributing to host cell lysis during decomposition. Overall, our results demonstrate that wild-caught fish have a reproducible decomposer succession and that the fish necrobiome serves as a potential source of putative pathogens and toxigenic bacteria. IMPORTANCE The microbial decomposition of animal tissues is an important ecological process that impacts nutrient cycling in natural environments. We studied the microbial decomposition of a common North American fish (rainbow darters) over four time points, combining 16S rRNA gene and shotgun metagenomic sequence data to obtain both taxonomic and functional perspectives. Our data revealed a strong community succession that was reproduced across different fish and environments. Decomposition time point was the main driver of community composition and functional potential; fish environmental origin (upstream or downstream of a wastewater treatment plant) had a secondary effect. We also identified strains related to the putative pathogen Aeromonas veronii as dominant members of the decomposition community. These bacteria peaked early in decomposition and coincided with the metagenomic abundance of hemolytic toxin genes. Our work reveals a strong decomposer succession in wild-caught fish, providing functional and taxonomic insights into the vertebrate necrobiome.
format	article
author	Briallen Lobb Rhiannon Hodgson Michael D. J. Lynch Michael J. Mansfield Jiujun Cheng Trevor C. Charles Josh D. Neufeld Paul M. Craig Andrew C. Doxey
author_facet	Briallen Lobb Rhiannon Hodgson Michael D. J. Lynch Michael J. Mansfield Jiujun Cheng Trevor C. Charles Josh D. Neufeld Paul M. Craig Andrew C. Doxey
author_sort	Briallen Lobb
title	Time Series Resolution of the Fish Necrobiome Reveals a Decomposer Succession Involving Toxigenic Bacterial Pathogens
title_short	Time Series Resolution of the Fish Necrobiome Reveals a Decomposer Succession Involving Toxigenic Bacterial Pathogens
title_full	Time Series Resolution of the Fish Necrobiome Reveals a Decomposer Succession Involving Toxigenic Bacterial Pathogens
title_fullStr	Time Series Resolution of the Fish Necrobiome Reveals a Decomposer Succession Involving Toxigenic Bacterial Pathogens
title_full_unstemmed	Time Series Resolution of the Fish Necrobiome Reveals a Decomposer Succession Involving Toxigenic Bacterial Pathogens
title_sort	time series resolution of the fish necrobiome reveals a decomposer succession involving toxigenic bacterial pathogens
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/59795a052e7249a3806cc1026d7d2586
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Time Series Resolution of the Fish Necrobiome Reveals a Decomposer Succession Involving Toxigenic Bacterial Pathogens

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