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Abstract Bloom‐forming gelatinous zooplankton occur circumglobally and significantly influence the structure of pelagic marine food webs and biogeochemical cycling through interactions with microbial communities. During bloom conditions especially, gelatinous zooplankton are keystone taxa that help determine the fate of primary production, nutrient remineralization, and carbon export. Using the pelagic tunicateDolioletta gegenbaurias a model system for gelatinous zooplankton, we carried out a laboratory‐based feeding experiment to investigate the potential ecosystem impacts of doliolid gut microbiomes and microbial communities associated with doliolid faecal pellets and the surrounding seawater. Metabarcoding targeting Bacteria and Archaea 16S rRNA genes/Archaea) and qPCR approaches were used to characterize microbiome assemblages. Comparison between sample types revealed distinct patterns in microbial diversity and biomass that were replicable across experiments. These observations support the hypothesis that through their presence and trophic activity, doliolids influence the structure of pelagic food webs and biogeochemical cycling in subtropical continental shelf systems where tunicate blooms are common. Bacteria associated with starved doliolids (representative of the resident gut microbiome) possessed distinct low‐biomass and low‐diversity microbial assemblages, suggesting that the doliolid microbiome is optimized to support a detrital trophic mode. Bacterial generaPseudoalteromomasandShimiawere the most abundant potential core microbiome taxa, similar to patterns observed in other marine invertebrates. Exploratory bioinformatic analyses of predicted functional genes suggest that doliolids, via their interactions with bacterial communities, may affect important biogeochemical processes including nitrogen, sulphur, and organic matter cycling.
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Host-specific symbioses and the microbial prey of a pelagic tunicate (Pyrosoma atlanticum)
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.
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- PAR ID:
- 10287557
- Date Published:
- Journal Name:
- ISME Communications
- Volume:
- 1
- Issue:
- 1
- ISSN:
- 2730-6151
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Abstract Gelatinous zooplankton play a crucial role in pelagic marine food webs, however, due to methodological challenges and persistent misconceptions of their importance, the trophic role of gelatinous zooplankton remains poorly investigated. This is particularly true for small gelatinous zooplankton including the marine pelagic tunicate,Dolioletta gegenbauri.D. gegenbauriand other doliolid species occur persistently on wide subtropical shelves where they often produce massive blooms in association with shelf upwelling conditions. As efficient filter feeders and prodigious producers of relatively low‐density organic‐rich aggregates, doliolids are understood to contribute significantly to shelf production, pelagic ecology, and pelagic–benthic coupling. Utilizing molecular gut content analysis and stable isotope analysis approaches, the trophic interactions of doliolids were explored during bloom and non‐bloom conditions on the South Atlantic Bight continental shelf in the Western North Atlantic. Based on molecular gut content analysis, relative ingestion selectivity varied withD. gegenbaurilife stage. At all life stages, doliolids ingested a wide range of prey types and sizes, but exhibited selectivity for larger prey types including diatoms, ciliates, and metazoans. Experimental growth studies confirmed that metazoan prey were ingested, but indicated that they were not digested and assimilated. Stable isotopic composition (δ13C and δ15N) of wild‐caught doliolids, during bloom and non‐bloom conditions, were most consistent with a detrital‐supplemented diet. These observations suggest that the feeding ecology ofD. gegenbauriis more complex than previously reported, and have strong and unusual linkages to the microbial food web.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s43705-021-00007-1
