Scomber japonicus is an economically important fishery, and is an emerging aquaculture species in Asia. Mackerel, crucial to marine ecosystems as forage fish and prey, are highly nutritious due to their rich omega-3 content and can be caught year-round in San Diego (wide temperature range 10-29 oC); thus, it is an ideal fish to study the impacts of seasonal variation on the microbiome. Here, we evaluated the extent to which the microbiome varied seasonally by sampling at least four fish per month for three years (2017-2019) from a fixed location (Scripps Institution of Oceanography Pier, La Jolla, CA). We hypothesized that the gut microbiome would be the most impacted as prey items are known to differ seasonally and that temperature would be the strongest environmental driver with winter and summer months varying the most. Microbiome samples from the gill, skin, and hindgut were processed from a total of 230 fish individuals using the EMP pipeline. Seasonal effects were greatest in the gill microbiome followed by skin, but absent in the gut. The gill and skin microbiomes varied most between spring (high diversity) and fall (low diversity) which may be driven by upwelling and general nutrient availability rather than the hypothesized summer-winter extremes driven by temperature. A single, highly abundant, Shewanella ASV was found in every gill sample, and was negatively associated with microbial diversity and Vibrio abundance. In a comparison to 101 other coastal marine fish species, Shewanella enrichment in the gill is unique to mackerel. We isolated and sequenced two Shewanella isolates with Oxford Nanopore, and performed a pangenome analysis with all 153 complete Shewanella genomes in NCBI which suggested our isolates are a new genus with the metabolic capacity for utilzing urea waste from fish gills and a type III secretion system. We next generated a chromosomal-level reference genome of mackerel (788 Mbp, scaffold N50 33.19 Mbp, BUSCO 96.9%) and resequenced 22 mackerel genomes spanning the three years to verify there was no population structure of the fish confounding seasonal variation in microbiome. We assessed whether gill microbiome biofouling negatively impacted fish respiration. Older fish had higher microbial biomass, which was linked to declining respiration efficiency, suggesting a role for the gill microbiome in aging. Our study shows how seasonal effects primarily impact the external mucosal surfaces of the gill and skin of a coastal marine forage fish while identifying a previously undescribed gill symbiont, Shewanella.