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Eastern Boundary Systems support major fisheries whose early life stages depend on upwelling production. Upwelling can be highly variable at the regional scale, with substantial repercussions for new productivity and microbial loop activity. Studies that integrate the classic trophic web based on new production with the microbial loop are rare due to the range in body forms and sizes of the taxa. Underwater imaging can overcome this limitation, and with machine learning, enables fine resolution studies spanning large spatial scales. We used theIn-situIchthyoplankton Imaging System (ISIIS) to investigate the drivers of plankton community structure in the northern California Current, sampled along the Newport Hydrographic (NH) and Trinidad Head (TR) lines, in OR and CA, respectively. The non-invasive imaging of particles and plankton over 1644km in the winters and summers of 2018 and 2019 yielded 1.194 billion classified plankton images. Combining nutrient analysis, flow cytometry, and 16S rRNA gene sequencing of the microbial community with mesoplankton underwater imaging enabled us to study taxa from 0.2µm to 15cm, including prokaryotes, copepods, ichthyoplankton, and gelatinous forms. To assess community structure, >2000 single-taxon distribution profiles were analyzed using high resolution spatial correlations. Co-occurrences on the NH line were consistently significantly higher off-shelf while those at TR were highest on-shelf. Random Forests models identified the concentrations of microbial loop associated taxa such as protists,Oithonacopepods, and appendicularians as important drivers of co-occurrences at NH line, while at TR, cumulative upwelling and chlorophyllawere of the highest importance. Our results indicate that the microbial loop is driving plankton community structure in intermittent upwelling systems such as the NH line and supports temporal stability, and further, that taxa such as protists,Oithonacopepods, and appendicularians connect a diverse and functionally redundant microbial community to stable plankton community structure. Where upwelling is more continuous such as at TR, primary production may dominate patterns of community structure, obscuring the underlying role of the microbial loop. Future changes in upwelling strength are likely to disproportionately affect plankton community structure in continuous upwelling regions, while high microbial loop activity enhances community structure resilience.

 

Abstract Pyrosomes are widely distributed pelagic tunicates that have the potential to reshape marine food webs when they bloom. However, their grazing preferences and interactions with the background microbial community are poorly understood. This is the first study of the marine microorganisms associated with pyrosomes undertaken to improve the understanding of pyrosome biology, the impact of pyrosome blooms on marine microbial systems, and microbial symbioses with marine animals. The diversity, relative abundance, and taxonomy of pyrosome-associated microorganisms were compared to seawater during a Pyrosoma atlanticum bloom in the Northern California Current System using high-throughput sequencing of the 16S rRNA gene, microscopy, and flow cytometry. We found that pyrosomes harbor a microbiome distinct from the surrounding seawater, which was dominated by a few novel taxa. In addition to the dominant taxa, numerous more rare pyrosome-specific microbial taxa were recovered. Multiple bioluminescent taxa were present in pyrosomes, which may be a source of the iconic pyrosome luminescence. We also discovered free-living marine microorganisms in association with pyrosomes, suggesting that pyrosome feeding impacts all microbial size classes but preferentially removes larger eukaryotic taxa. This study demonstrates that microbial symbionts and microbial prey are central to pyrosome biology. In addition to pyrosome impacts on higher trophic level marine food webs, the work suggests that pyrosomes also alter marine food webs at the microbial level through feeding and seeding of the marine microbial communities with their symbionts. Future efforts to predict pyrosome blooms, and account for their ecosystem impacts, should consider pyrosome interactions with marine microbial communities.