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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.

 

The Laurentian Great Lakes provide economic support to millions of people, drive biogeochemical cycling, and are an important natural laboratory for characterizing the fundamental components of aquatic ecosystems. Small phytoplankton are important contributors to the food web in much of the Laurentian Great Lakes. Here, for the first time, we reveal and quantify eight phenotypically distinct picophytoplankton populations across the Lakes using a multilaser flow cytometry approach, which distinguishes cells based on their pigment phenotype. The distributions and diversity of picophytoplankton flow populations varied across lakes and depths, with Lake Erie standing out with the highest diversity. By sequencing sorted cells, we identified several distinct lineages ofSynechococcalesspanning Subclusters 5.2 and 5.3. Distinct genotypic clusters mapped to phenotypically similar flow populations, suggesting that there may not be a clear one‐to‐one mapping between genotypes and phenotypes. This suggests genome‐level differentiation between lakes but some degree of phenotypic convergence in pigment characteristics. Our results demonstrate that ecological selection for locally adapted populations may outpace homogenization by physical transport in this interconnected system. Given the reliance of the Lakes on in situ primary production as a source for organic carbon, this work sets the foundation to test how the community structure of small primary producers corresponds to biogeochemical and food web functions of the Great Lakes and other freshwater systems.

 

Microbial mortality impacts the structure of food webs, carbon flow, and the interactions that create dynamic patterns of abundance across gradients in space and time in diverse ecosystems. In the oceans, estimates of microbial mortality by viruses, protists, and small zooplankton do not account fully for observations of loss, suggesting the existence of underappreciated mortality sources. We examined how ubiquitous mucous mesh feeders (i.e. gelatinous zooplankton) could contribute to microbial mortality in the open ocean. We coupled capture of live animals by blue‐water diving to sequence‐based approaches to measure the enrichment and selectivity of feeding by two coexisting mucous grazer taxa (pteropods and salps) on numerically dominant marine prokaryotes. We show that mucous mesh grazers consume a variety of marine prokaryotes and select between coexisting lineages and similar cell sizes. We show thatProchlorococcusmay evade filtration more than other cells and that planktonic archaea are consumed by macrozooplanktonic grazers. Discovery of these feeding relationships identifies a new source of mortality for Earth's dominant marine microbes and alters our understanding of how top‐down processes shape microbial community and function.

 

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. 

Early evolution of mutualism is characterized by big and predictable adaptive changes, including the specialization of interacting partners, such as through deleterious mutations in genes not required for metabolic cross-feeding. We sought to investigate whether these early mutations improve cooperativity by manifesting in synergistic epistasis between genomes of the mutually interacting species. Specifically, we have characterized evolutionary trajectories of syntrophic interactions of Desulfovibrio vulgaris (Dv) with Methanococcus maripaludis (Mm) by longitudinally monitoring mutations accumulated over 1000 generations of nine independently evolved communities with analysis of the genotypic structure of one community down to the single-cell level. We discovered extensive parallelism across communities despite considerable variance in their evolutionary trajectories and the perseverance within many evolution lines of a rare lineage of Dv that retained sulfate-respiration (SR+) capability, which is not required for metabolic cross-feeding. An in-depth investigation revealed that synergistic epistasis across pairings of Dv and Mm genotypes had enhanced cooperativity within SR− and SR+ assemblages, enabling their coexistence within the same community. Thus, our findings demonstrate that cooperativity of a mutualism can improve through synergistic epistasis between genomes of the interacting species, enabling the coexistence of mutualistic assemblages of generalists and their specialized variants.