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

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.

Taxonomic and Functional Characteristics of the Gill and Gastrointestinal Microbiota and Its Correlation with Intestinal Metabolites in NEW GIFT Strain of Farmed Adult Nile Tilapia (Oreochromis niloticus)

“…The gill and stomach mucosae shared the core bacterial genera, including Sphingomonas, Ralstonia, unclassified Comamonadaceae, and Pelomonas, all of which were aerobic microorganisms [49][50][51][52]. This finding suggested that both the gill and stomach mucosae had high oxygen levels, which was consistent with adequate exposure to the environment at the two sites [10]. However, further study is required to explain the similarity between the gill and stomach mucosal microbiota observed in the present study.…”

“…Such significant differences in microbial structure led to significant differences in microbial function, which could be attributed to the functional heterogeneity of the gastrointestinal tract, because the stomach is the main site of diet fermentation and the hindgut plays an important role in nutrient absorption [ 38 ]. No significant differences were found in the bacterial community structure and composition between the stomach and gill mucosae, which might have been due to the similarity of mucosal niches between these two sites [ 10 ]. In addition, three mucosa sites had no significant differences in terms of microbial diversity and displayed a lower microbial diversity compared with the digesta.…”

“…The evaluation of the bacterial community attached to the gills, which is the respiratory organ, has a long history [ 5 ]. However, except for several recent studies [ 6 , 7 , 8 , 9 , 10 ], this topic has received little attention. The gastrointestinal tract is a complex ecosystem that harbors diverse microbial communities that can increase digestion efficiency and the use of nutrients, boost the immune system, and prevent the attachment and proliferation of opportunistic pathogens [ 11 ].…”

The Southern Bluefin Tuna Mucosal Microbiome Is Influenced by Husbandry Method, Net Pen Location, and Anti-parasite Treatment

“…Presence of adult flukes in heart and egg densities within the gill were measured per fish as previously described ( Aiken et al, 2006 ; Power et al, 2019 ). Comparison of the SBT microbiome to other fish samples, including Pacific chub mackerel (MKL) ( Minich et al, 2020b ) and yellowtail kingfish (YTK), was performed computationally within Qiita ( Gonzalez et al, 2018 ). All MKL samples were collected from the wild while the YTK were farmed.…”

Fishing for the Bacteriome of Tropical Tuna

“…Mammals, corals and, to a lesser extent, fish have been primarily targeted by marine microbiologists in microbiome studies, and we now have a body of evidence that these diverse and abundant microbes play a vital role in the health and fitness of their hosts, participating in functions as important as digestion, defence, and nutrition, among others [1][2][3]. Most such studies show that the composition of these microbial communities remains highly variable and multifactorial and is subject, in a still unclear way, to the influence of different parameters associated with the host, including species [4], age [5], sex [6], and diet [7], as well as external environmental conditions such as salinity [8], seasonality [9], geographical location [10], temperature [11], and chlorophyll a concentration [12]. However, these commensal microbes are not evenly distributed throughout the body of their marine hosts, where similar to those in humans, they form complex bacterial consortia mainly in the digestive tract [13], skin [14], and respiratory system [15].…”