Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, <named-content content-type="genus-species">Scomber japonicus</named-content>

ABSTRACT Changing ocean conditions driven by anthropogenic activities may have a negative impact on fisheries by increasing stress and disease. To understand how environment and host biology drives mucosal microbiomes in a marine fish, we surveyed five body sites (gill, skin, digesta, gastrointestin...

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Autores principales:	Jeremiah J. Minich, Semar Petrus, Julius D. Michael, Todd P. Michael, Rob Knight, Eric E. Allen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	fish microbiome mackerel microbial ecology microbial biogeography Scomber japonicus marine microbiology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2c65ababfd8141b1b1188ea52dbb657d
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spelling	oai:doaj.org-article:2c65ababfd8141b1b1188ea52dbb657d2021-11-15T15:30:15ZTemporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, <named-content content-type="genus-species">Scomber japonicus</named-content>10.1128/mSphere.00401-202379-5042https://doaj.org/article/2c65ababfd8141b1b1188ea52dbb657d2020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00401-20https://doaj.org/toc/2379-5042ABSTRACT Changing ocean conditions driven by anthropogenic activities may have a negative impact on fisheries by increasing stress and disease. To understand how environment and host biology drives mucosal microbiomes in a marine fish, we surveyed five body sites (gill, skin, digesta, gastrointestinal tract [GI], and pyloric ceca) from 229 Pacific chub mackerel, Scomber japonicus, collected across 38 time points spanning 1 year from the Scripps Institution of Oceanography Pier (La Jolla, CA). Mucosal sites had unique microbial communities significantly different from the surrounding seawater and sediment communities with over 10 times more total diversity than seawater. The external surfaces of skin and gill were more similar to seawater, while digesta was more similar to sediment. Alpha and beta diversity of the skin and gill was explained by environmental and biological factors, specifically, sea surface temperature, chlorophyll a, and fish age, consistent with an exposure gradient relationship. We verified that seasonal microbial changes were not confounded by regional migration of chub mackerel subpopulations by nanopore sequencing a 14,769-bp region of the 16,568-bp mitochondria across all temporal fish specimens. A cosmopolitan pathogen, Photobacterium damselae, was prevalent across multiple body sites all year but highest in the skin, GI, and digesta between June and September, when the ocean is warmest. The longitudinal fish microbiome study evaluates the extent to which the environment and host biology drives mucosal microbial ecology and establishes a baseline for long-term surveys linking environment stressors to mucosal health of wild marine fish. IMPORTANCE Pacific chub mackerel, Scomber japonicus, are one of the largest and most economically important fisheries in the world. The fish is harvested for both human consumption and fish meal. Changing ocean conditions driven by anthropogenic stressors like climate change may negatively impact fisheries. One mechanism for this is through disease. As waters warm and chemistry changes, the microbial communities associated with fish may change. In this study, we performed a holistic analysis of all mucosal sites on the fish over a 1-year time series to explore seasonal variation and to understand the environmental drivers of the microbiome. Understanding seasonality in the fish microbiome is also applicable to aquaculture production for producers to better understand and predict when disease outbreaks may occur based on changing environmental conditions in the ocean.Jeremiah J. MinichSemar PetrusJulius D. MichaelTodd P. MichaelRob KnightEric E. AllenAmerican Society for Microbiologyarticlefish microbiomemackerelmicrobial ecologymicrobial biogeographyScomber japonicusmarine microbiologyMicrobiologyQR1-502ENmSphere, Vol 5, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	fish microbiome mackerel microbial ecology microbial biogeography Scomber japonicus marine microbiology Microbiology QR1-502
spellingShingle	fish microbiome mackerel microbial ecology microbial biogeography Scomber japonicus marine microbiology Microbiology QR1-502 Jeremiah J. Minich Semar Petrus Julius D. Michael Todd P. Michael Rob Knight Eric E. Allen Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, <named-content content-type="genus-species">Scomber japonicus</named-content>
description	ABSTRACT Changing ocean conditions driven by anthropogenic activities may have a negative impact on fisheries by increasing stress and disease. To understand how environment and host biology drives mucosal microbiomes in a marine fish, we surveyed five body sites (gill, skin, digesta, gastrointestinal tract [GI], and pyloric ceca) from 229 Pacific chub mackerel, Scomber japonicus, collected across 38 time points spanning 1 year from the Scripps Institution of Oceanography Pier (La Jolla, CA). Mucosal sites had unique microbial communities significantly different from the surrounding seawater and sediment communities with over 10 times more total diversity than seawater. The external surfaces of skin and gill were more similar to seawater, while digesta was more similar to sediment. Alpha and beta diversity of the skin and gill was explained by environmental and biological factors, specifically, sea surface temperature, chlorophyll a, and fish age, consistent with an exposure gradient relationship. We verified that seasonal microbial changes were not confounded by regional migration of chub mackerel subpopulations by nanopore sequencing a 14,769-bp region of the 16,568-bp mitochondria across all temporal fish specimens. A cosmopolitan pathogen, Photobacterium damselae, was prevalent across multiple body sites all year but highest in the skin, GI, and digesta between June and September, when the ocean is warmest. The longitudinal fish microbiome study evaluates the extent to which the environment and host biology drives mucosal microbial ecology and establishes a baseline for long-term surveys linking environment stressors to mucosal health of wild marine fish. IMPORTANCE Pacific chub mackerel, Scomber japonicus, are one of the largest and most economically important fisheries in the world. The fish is harvested for both human consumption and fish meal. Changing ocean conditions driven by anthropogenic stressors like climate change may negatively impact fisheries. One mechanism for this is through disease. As waters warm and chemistry changes, the microbial communities associated with fish may change. In this study, we performed a holistic analysis of all mucosal sites on the fish over a 1-year time series to explore seasonal variation and to understand the environmental drivers of the microbiome. Understanding seasonality in the fish microbiome is also applicable to aquaculture production for producers to better understand and predict when disease outbreaks may occur based on changing environmental conditions in the ocean.
format	article
author	Jeremiah J. Minich Semar Petrus Julius D. Michael Todd P. Michael Rob Knight Eric E. Allen
author_facet	Jeremiah J. Minich Semar Petrus Julius D. Michael Todd P. Michael Rob Knight Eric E. Allen
author_sort	Jeremiah J. Minich
title	Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, <named-content content-type="genus-species">Scomber japonicus</named-content>
title_short	Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, <named-content content-type="genus-species">Scomber japonicus</named-content>
title_full	Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, <named-content content-type="genus-species">Scomber japonicus</named-content>
title_fullStr	Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, <named-content content-type="genus-species">Scomber japonicus</named-content>
title_full_unstemmed	Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, <named-content content-type="genus-species">Scomber japonicus</named-content>
title_sort	temporal, environmental, and biological drivers of the mucosal microbiome in a wild marine fish, <named-content content-type="genus-species">scomber japonicus</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/2c65ababfd8141b1b1188ea52dbb657d
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Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, <named-content content-type="genus-species">Scomber japonicus</named-content>

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