skip to main content
Explore Scholarly Publications and Datasets in the NSF-PAR

Title: 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 more » 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. « less
Authors:
; ; ;
Award ID(s):
1851537 1851412 1737399 1737364
Publication Date:
NSF-PAR ID:
10287557
Journal Name:
ISME Communications
Volume:
1
Issue:
1
ISSN:
2730-6151
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ( , Molecular Ecology)
    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 tunicate Dolioletta gegenbauri as 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 genera Pseudoalteromomas and Shimia were the most abundant potential core microbiome taxa, similar tomore »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.« less
  2. ; ; ; ( , Frontiers in Microbiology)
    Persistent bacterial presence is believed to play an important role in host adaptation to specific niches that would otherwise be unavailable, including the exclusive consumption of blood by invertebrate parasites. Nearly all blood-feeding animals examined so far host internal bacterial symbionts that aid in some essential aspect of their nutrition. Obligate blood-feeding (OBF) invertebrates exist in the oceans, yet symbiotic associations between them and beneficial bacteria have not yet been explored. This study describes the microbiome of 6 phylogenetically-diverse species of marine obligate blood-feeders, including leeches (both fish and elasmobranch specialists; e.g., Pterobdella, Ostreobdella, and Branchellion ), isopods (e.g., Elthusa and Nerocila ), and a copepod (e.g., Lernanthropus ). Amplicon sequencing analysis revealed the blood-feeding invertebrate microbiomes to be low in diversity, compared to host fish skin surfaces, seawater, and non-blood-feeding relatives, and dominated by only a few bacterial genera, including Vibrio (100% prevalence and comprising 39%–81% of the average total recovered 16S rRNA gene sequences per OBF taxa). Vibrio cells were localized to the digestive lumen in and among the blood meal for all taxa examined via fluorescence microscopy. For Elthusa and Branchellion, Vibrio cells also appeared intracellularly within possible hemocytes, suggesting an interaction with the immune system. Additionally,more »Vibrio cultivated from four of the obligate blood-feeding marine taxa matched the dominant amplicons recovered, and all but one was able to effectively lyse vertebrate blood cells. Bacteria from 2 additional phyla and 3 families were also regularly recovered, albeit in much lower abundances, including members of the Oceanospirillaceae, Flavobacteriacea, Porticoccaceae, and unidentified members of the gamma-and betaproteobacteria, depending on the invertebrate host. For the leech Pterobdella , the Oceanospirillaceae were also detected in the esophageal diverticula. For two crustacean taxa, Elthusa and Lernanthropus , the microbial communities associated with brooded eggs were very similar to the adults, indicating possible direct transmission. Virtually nothing is known about the influence of internal bacteria on the success of marine blood-feeders, but this evidence suggests their regular presence in marine parasites from several prominent groups.« less
  3. ; ; ; ; ; ; ; ; ; ( , Proceedings of the National Academy of Sciences)

    Microbial eukaryotes (or protists) in marine ecosystems are a link between primary producers and all higher trophic levels, and the rate at which heterotrophic protistan grazers consume microbial prey is a key mechanism for carbon transport and recycling in microbial food webs. At deep-sea hydrothermal vents, chemosynthetic bacteria and archaea form the base of a food web that functions in the absence of sunlight, but the role of protistan grazers in these highly productive ecosystems is largely unexplored. Here, we pair grazing experiments with a molecular survey to quantify protistan grazing and to characterize the composition of vent-associated protists in low-temperature diffuse venting fluids from Gorda Ridge in the northeast Pacific Ocean. Results reveal protists exert higher predation pressure at vents compared to the surrounding deep seawater environment and may account for consuming 28 to 62% of the daily stock of prokaryotic biomass within discharging hydrothermal vent fluids. The vent-associated protistan community was more species rich relative to the background deep sea, and patterns in the distribution and co-occurrence of vent microbes provide additional insights into potential predator–prey interactions. Ciliates, followed by dinoflagellates, Syndiniales, rhizaria, and stramenopiles, dominated the vent protistan community and included bacterivorous species, species known to hostmore »symbionts, and parasites. Our findings provide an estimate of protistan grazing pressure within hydrothermal vent food webs, highlighting the important role that diverse protistan communities play in deep-sea carbon cycling.

    « less
  4. ; ; ; ; ; ; ; ( , The ISME Journal)
    Abstract Microbes transform aqueous mercury (Hg) into methylmercury (MeHg), a potent neurotoxin that accumulates in terrestrial and marine food webs, with potential impacts on human health. This process requires the gene pair hgcAB , which encodes for proteins that actuate Hg methylation, and has been well described for anoxic environments. However, recent studies report potential MeHg formation in suboxic seawater, although the microorganisms involved remain poorly understood. In this study, we conducted large-scale multi-omic analyses to search for putative microbial Hg methylators along defined redox gradients in Saanich Inlet, British Columbia, a model natural ecosystem with previously measured Hg and MeHg concentration profiles. Analysis of gene expression profiles along the redoxcline identified several putative Hg methylating microbial groups, including Calditrichaeota, SAR324 and Marinimicrobia, with the last the most active based on hgc transcription levels. Marinimicrobia hgc genes were identified from multiple publicly available marine metagenomes, consistent with a potential key role in marine Hg methylation. Computational homology modelling predicts that Marinimicrobia HgcAB proteins contain the highly conserved amino acid sites and folding structures required for functional Hg methylation. Furthermore, a number of terminal oxidases from aerobic respiratory chains were associated with several putative novel Hg methylators. Our findings thus revealmore »potential novel marine Hg-methylating microorganisms with a greater oxygen tolerance and broader habitat range than previously recognized.« less
  5. ; ; ( , Integrative and Comparative Biology)
    Abstract The chemical ecology and chemical defenses of sponges have been investigated for decades; consequently, sponges are among the best understood marine organisms in terms of their chemical ecology, from the level of molecules to ecosystems. Thousands of natural products have been isolated and characterized from sponges, and although relatively few of these compounds have been studied for their ecological functions, some are known to serve as chemical defenses against predators, microorganisms, fouling organisms, and other competitors. Sponges are hosts to an exceptional diversity of microorganisms, with almost 40 microbial phyla found in these associations to date. Microbial community composition and abundance are highly variable across host taxa, with a continuum from diverse assemblages of many microbial taxa to those that are dominated by a single microbial group. Microbial communities expand the nutritional repertoire of their hosts by providing access to inorganic and dissolved sources of nutrients. Not only does this continuum of microorganism–sponge associations lead to divergent nutritional characteristics in sponges, these associated microorganisms and symbionts have long been suspected, and are now known, to biosynthesize some of the natural products found in sponges. Modern “omics” tools provide ways to study these sponge–microbe associations that would have been difficultmore »even a decade ago. Metabolomics facilitate comparisons of sponge compounds produced within and among taxa, and metagenomics and metatranscriptomics provide tools to understand the biology of host–microbe associations and the biosynthesis of ecologically relevant natural products. These combinations of ecological, microbiological, metabolomic and genomics tools, and techniques provide unprecedented opportunities to advance sponge biology and chemical ecology across many marine ecosystems.« less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email