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Research Article | Ecological and Evolutionary Science

Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, Scomber japonicus

Jeremiah J. Minich, Semar Petrus, Julius D. Michael, Todd P. Michael, Rob Knight, Eric E. Allen
Katherine McMahon, Editor
Jeremiah J. Minich
aMarine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USA
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  • ORCID record for Jeremiah J. Minich
Semar Petrus
bJ. Craig Venter Institute, La Jolla, California, USA
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Julius D. Michael
bJ. Craig Venter Institute, La Jolla, California, USA
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Todd P. Michael
aMarine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USA
bJ. Craig Venter Institute, La Jolla, California, USA
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Rob Knight
cCenter for Microbiome Innovation, University of California San Diego, La Jolla, California, USA
dDepartment of Pediatrics, University of California San Diego, La Jolla, California, USA
eDepartment of Computer Science and Engineering, University of California San Diego, La Jolla, California, USA
fDepartment of Bioengineering, University of California San Diego, La Jolla, California, USA
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Eric E. Allen
aMarine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California, USA
cCenter for Microbiome Innovation, University of California San Diego, La Jolla, California, USA
gDivision of Biological Sciences, University of California, San Diego, La Jolla, California, USA
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Katherine McMahon
University of Wisconsin—Madison
Roles: Editor
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DOI: 10.1128/mSphere.00401-20
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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.

  • Copyright © 2020 Minich et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, Scomber japonicus
Jeremiah J. Minich, Semar Petrus, Julius D. Michael, Todd P. Michael, Rob Knight, Eric E. Allen
mSphere May 2020, 5 (3) e00401-20; DOI: 10.1128/mSphere.00401-20

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Temporal, Environmental, and Biological Drivers of the Mucosal Microbiome in a Wild Marine Fish, Scomber japonicus
Jeremiah J. Minich, Semar Petrus, Julius D. Michael, Todd P. Michael, Rob Knight, Eric E. Allen
mSphere May 2020, 5 (3) e00401-20; DOI: 10.1128/mSphere.00401-20
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KEYWORDS

fish microbiome
mackerel
microbial ecology
microbial biogeography
Scomber japonicus
marine microbiology
veterinary microbiology

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