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Abstract Cell surface properties can strongly mediate microbial interactions with predators in soil and host‐pathogen systems. Yet, the role of microbial surface properties in avoiding or enhancing predation in the ocean is less well known. Appendicularians are globally abundant marine suspension feeders that capture marine microorganisms in a complex mucous filtration system. We used artificial microspheres to test whether the surface properties of prey particles influenced selection by the appendicularian,Oikopleura dioica. We used a range of microsphere sizes (0.5, 1, 2, and 3 μm), concentrations (~ 10³–10⁶particles mL⁻¹), and two charges (amine‐modified, more positive vs. carboxylate‐modified, more negative) to represent open‐ocean microbial communities. We found that appendicularians selected between the particles of different charge. More negatively charged particles were enriched in the gut by up to 3.8‐fold, while more positive particles were enriched in the mucous filters by up to 4.7‐fold, leading to different particle fates. These results expand understanding of the mechanisms by which filter‐feeders select between prey and reveal a mechanism by which marine bacteria could rapidly alter their susceptibility to predation, either through adaption or acclimation. 

Abstract Doliolids have a unique ability to impact the marine microbial community through bloom events and filter feeding. Their predation on large eukaryotic microorganisms is established and evidence of predation on smaller prokaryotic microorganisms is beginning to emerge. We studied the association between microorganisms and wild‐caught doliolids in the Northern California Current system. Doliolids were collected during bloom events identified at three different shelf locations with variable upwelling intensity. We discovered doliolids were associated with a range of prokaryotic microbial functional groups, which included free‐living pelagic Archaea, SAR11, and picocyanobacteria. The results suggest the possibility that doliolids could feed on the smallest members of the microbial community, expanding our understanding of doliolid feeding and microbial mortality. Given the ability of doliolids to clear large portions of seawater by filtration and their high abundance in this system, we suggest that doliolids could be an important player in shaping the microbial community structure of the Northern California Current system. 

Abstract The mechanism of mortality plays a large role in how microorganisms in the open ocean contribute to global energy and nutrient cycling. Salps are ubiquitous pelagic tunicates that are a well-known mortality source for large phototrophic microorganisms in coastal and high-latitude systems, but their impact on the immense populations of smaller prokaryotes in the tropical and subtropical open ocean gyres is not well quantified. We used robustly quantitative techniques to measure salp clearance and enrichment of specific microbial functional groups in the North Pacific Subtropical Gyre, one of the largest ecosystems on Earth. We discovered that salps are a previously unknown predator of the globally abundant nitrogen fixer Crocosphaera; thus, salps restrain new nitrogen delivery to the marine ecosystem. We show that the ocean's two numerically dominant cells, Prochlorococcus and SAR11, are not consumed by salps, which offers a new explanation for the dominance of small cells in open ocean systems. We also identified a double bonus for Prochlorococcus, wherein it not only escapes salp predation but the salps also remove one of its major mixotrophic predators, the prymnesiophyte Chrysochromulina. When we modeled the interaction between salp mesh and particles, we found that cell size alone could not account for these prey selection patterns. Instead, the results suggest that alternative mechanisms, such as surface property, shape, nutritional quality, or even prey behavior, determine which microbial cells are consumed by salps. Together, these results identify salps as a major factor in shaping the structure, function, and ecology of open ocean microbial communities. 

Abstract 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 Blooms of the colonial pelagic tunicate Pyrosoma atlanticum in 2014–2018 followed a marine heatwave in the eastern Pacific Ocean. Pyrosome blooms could alter pelagic food webs of the northern California Current (NCC) by accelerating the biological pump via active transport, fecal pellet production and mortality events. Although aggregations of P. atlanticum have the potential to shape marine trophic dynamics via carbon export, little is known about pyrosome vertical distribution patterns. In this study, we estimated the distribution of P. atlanticum in the NCC along transects off of Oregon (45°N and 124°W) and northern California (41°N and 124°W), USA during February and July 2018. Depth-stratified plankton tows provided volume-normalized pyrosome abundance and biovolume estimates that complemented fine-scale counts by a vertically deployed camera system. Pyrosomes were numerous offshore during February, especially off Oregon. Colonies were distributed non-uniformly in the water column with peak numbers associated with vertical gradients in environmental parameters, notably density and chl-a. Vertical distributions shifted over the 24-h period, indicative of diel vertical migration. Understanding the vertical distribution of these gelatinous grazers in the NCC gives insight to their behavior and ecological role in biologically productive temperate ecosystems as conditions become more favorable for recurring blooms. 

Planktonic organisms feed while suspended in water using various hydrodynamic pumping strategies. Appendicularians are a unique group of plankton that use their tail to pump water over mucous mesh filters to concentrate food particles. As ubiquitous and often abundant members of planktonic ecosystems, they play a major role in oceanic food webs. Yet, we lack a complete understanding of the fluid flow that underpins their filtration. Using high-speed, high-resolution video and micro particle image velocimetry, we describe the kinematics and hydrodynamics of the tail inOikopleura dioicain filtering and free-swimming postures. We show that sinusoidal waves of the tail generate peristaltic pumping within the tail chamber with fluid moving parallel to the tail when filtering. We find that the tail contacts attachment points along the tail chamber during each beat cycle, serving to seal the tail chamber and drive pumping. When we tested how the pump performs across environmentally relevant temperatures, we found that the amplitude of the tail was invariant but tail beat frequency increased threefold across three temperature treatments (5°C, 15°C and 25°C). Investigation into this unique pumping mechanism gives insight into the ecological success of appendicularians and provides inspiration for novel pump designs. 

Appendicularians are abundant planktonic filter feeders that play a significant role in the pelagic food web due to their high clearance rates. Their diet and feeding rates have typically been measured as bulk chlorophyll or cell removal, with some attention given to prey size but no differentiation between the microbial phylotypes. Using a combination of in situ and laboratory incubations with flow cytometry and next-generation sequencing, we found species-specific differences in clearance rates and diet compositions of 4 common species: Oikopleura albicans , O. fusiformis , O. longicauda , and O. dioica . While O. albicans most efficiently removed nano-eukaryotic algae, the other smaller species preferentially removed micron-sized pico-eukaryotic algae. Pico- and nano-eukaryotic cells constituted the major food source of the studied appendicularians despite their occurrence in oligotrophic water dominated by prokaryotic cells. Across species, pico- and nano-planktonic microalgae biomass comprised 45 to 75% of the appendicularian diets. Although non-photosynthetic bacteria were removed at lower rates than all other prey groups, their total contribution to the appendicularian diet was not trivial, representing 5 to 19% of the planktonic carbon in the appendicularian diet; pico-cyanobacteria contributed an additional 9 to 18%. Removal rates and efficiencies of pico-eukaryotes were higher than those of prokaryotes of similar size. Strikingly different clearance rates were observed for different prokaryotic phylotypes, indicating that factors other than size are involved in determining the capturability of the cells. Collectively, our findings provide additional evidence for differential retention of microbial prey among mucous-mesh grazers and its substantial effect on the upper-ocean microbial community. 

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. 

Suspension feeders, including ascidians (Phylum Chordata, Class Ascidiacea), experience a dilute prey field composed of extremely small particles. The filtration apparatus of ascidians is based on a mucous-mesh that is continuously secreted and ingested. The rate and metabolic cost of this mesh secretion has not been quantified to date. We used video boroscopy to quantify the mucous-mesh production rate of the solitary ascidian Herdmania momus under different food and temperature treatments. H. momus individuals with an average (±95% CI) biomass of 30.7 ± 1.1 mg and a branchial sac area of 10.3 ± 1.2 cm 2 produced an average of 276 ± 33.5 cm 2 of mucous-mesh h -1 , corresponding to a median turnover rate of 625 ± 82 mesh d -1 . Since the mean mesh mass was 2.44 ± 0.58 mg, this production rate corresponds to roughly 50 ± 8 times the individual’s biomass per day. Food concentration had no detectable effect on mesh production rate, whereas a temperature difference of ~9°C (20 vs. 29°C) moderately increased mesh production by 30-50%. The current study reveals that the feeding process of H. momus involves a high expenditure on mucous-mesh synthesis that, combined with low food availability, may limit its growth in oligotrophic waters and under changing climate regimes.