Temporal, environmental, and biological drivers of the mucosal microbiome in a wild marine fish, Scomber japonicus

AbstractChanging ocean conditions driven by anthropogenic activity may have a negative impact on fisheries by increasing stress and disease with the mucosal microbiome as a potentially important intermediate role. To understand how environment and host biology drives mucosal microbiomes in a marine fish, we surveyed five body sites (gill, skin, digesta, GI, and pyloric caeca) from 229 Pacific chub mackerel, Scomber japonicus, collected across 38 time points spanning one year from the Scripps Institution of Oceanography Pier, making this the largest and longest wild marine fish microbiome survey. Mucosal sites had unique communities significantly different from the surrounding sea water and sediment communities with over 10 times more diversity than sea water alone. Although, external surfaces such as skin and gill were more similar to sea water, digesta was similar to sediment. Both alpha and beta diversity of the skin and gill was explained by environmental and biological factors, especially sea surface temperature, chlorophyll a, and fish age, consistent with an exposure gradient relationship. We verified that seasonal microbial changes were not confounded by migrations of chub mackerel sub-populations by nanopore sequencing a 14 769 bp region of the 16 568 bp mitochondria. 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. Our study evaluates the extent which the environment and host biology drives mucosal microbial ecology, establishing a baseline for long term monitoring surveys for linking environment stressors to mucosal health of wild marine fish.

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

mSphere ◽

10.1128/msphere.00401-20 ◽

2020 ◽

Vol 5 (3) ◽

Author(s):

Jeremiah J. Minich ◽

Semar Petrus ◽

Julius D. Michael ◽

Todd P. Michael ◽

Rob Knight ◽

...

Keyword(s):

Microbial Communities ◽

Marine Fish ◽

Negative Impact ◽

Anthropogenic Activities ◽

Environmental Drivers ◽

Human Consumption ◽

Scomber Japonicus ◽

Chub Mackerel ◽

Content Type ◽

Ocean Conditions

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.

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Molecular characterization of muscle-parasitizing didymozoid from a chub mackerel, Scomber japonicus

Acta Parasitologica ◽

10.1515/ap-2015-0080 ◽

2015 ◽

Vol 60 (3) ◽

Cited By ~ 2

Author(s):

Niichiro Abe ◽

Mitsuru Okamoto

Keyword(s):

Marine Fish ◽

Phylogenetic Analyses ◽

Trunk Muscles ◽

Sea Bream ◽

Morphological Identification ◽

Scomber Japonicus ◽

Chub Mackerel ◽

Sequencing Analysis ◽

Atlantic Mackerel ◽

Flying Fish

AbstractDidymozoids found in the muscles of marine fish are almost always damaged because they are usually found after being sliced. Therefore, identifying muscle-parasitizing didymozoids is difficult because of the difficulty in collecting non-damaged worms and observing their organs as key points for morphological identification. Moreover, muscle-parasitizing didymozoids are not easily found because they parasitize at the trunk muscles. Therefore, muscle-parasitizing didymozoid classification has not progressed because there are few opportunities to detect them. Our recent report was the first to describe the usefulness of sequencing analysis for discrimination among muscle-parasitizing didymozoids. Recently, we found a didymozoid in the trunk muscle of a chub mackerel Scomber japonicus. The present study genetically compares the present isolate with other muscle-parasitizing didymozoids. The present isolate differs markedly from the previously unidentified didymozoid from an Atlantic mackerel S. scombrus by phylogenetic analysis of 18S rDNA. It also differs from other muscle-parasitizing didymozoids from other host species based on phylogenetic analyses of 18S, 28S rDNAs, and coxI loci. These results suggest that sequencing analysis is useful for the discrimination of muscle-parasitizing didymozoids. Combining the present data with earlier data for sequencing analysis, muscle-parasitizing didymozoids from seven marine fish species were classified as seven species. We proposed appellations for six distinct muscle-parasitizing didymozoids for future analysis: sweetlips fish type from Diagramma pictum and Plectorhinchus cinctus, red sea bream type from Pagrus major, flying fish type from Cypselurus heterurus, Atlantic mackerel type from Scomber scombrus, chub mackerel type from S. japonicus, and purple rockcod type from Epinephelus cyanopodus.

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