A 2021 coordinated survey of microbes, meiofauna and macrofauna inhabiting aggregations of the foundation tubeworm Ridgeia piscesae at the Endeavour and Middle Valley segments (Juan de Fuca Ridge) revealed two emergent cross-domain "core communities" separated by a basal-fluid temperature near 25 °C, inferred a web of covarying microbe-fauna associations, and flagged tubeworm-hosted assemblages as hotspots of novel, shallow-classified microbial taxa. The study left open whether temperature itself or covarying geochemical variables (sulphide, dissolved oxygen) drive the partition, whether the covariance-based associations are real ecological interactions, how the high-temperature sub-communities are further structured, and what functional roles the tubeworm-unique taxa play.

Background

Deep-sea hydrothermal vents along mid-ocean ridges discharge warm, chemically reduced diffuse fluid that mixes with cold oxygenated seawater, producing steep centimetre-scale gradients in temperature, sulphide (H2S, an energy source for chemosynthetic microbes but a toxin at high concentration) and dissolved oxygen. On the Juan de Fuca Ridge, the foundation species Ridgeia piscesae — a sessile vestimentiferan tubeworm hosting chemoautotrophic symbionts — forms long-lived aggregations (grabs) that create habitat for associated organisms across three size classes: microorganisms (<64 µm; bacteria, archaea and microbial eukaryotes, censused as OTUs, i.e. operational taxonomic units clustered from 16S/18S rRNA gene amplicons), meiofauna (metazoans in the 64 µm to 1 mm size fraction, e.g. nematodes, copepods, juvenile stages) and macrofauna (metazoans larger than 1 mm, such as polychaetes, limpets and snails). Murdock, Tunnicliffe, Boschen-Rose and Juniper (ISME Communications 1:27, 2021) co-sequenced all three size classes from tubeworm grabs spanning a basal-temperature gradient, plus venting diffuse fluids and background seawater, at the Endeavour and Middle Valley segments. They found that communities in grabs warmer than about 25 °C (highT) and cooler than about 25 °C (lowT) differ consistently in all size classes, defining two "core communities" of co-occurring, enriched taxa — an eight-species faunal core with Epsilonbacteraeota and Bacteroidetes microbes at highT, and a more meiofauna-weighted core at lowT. Crucially, they recognized that temperature is a proxy: sulphide concentration correlates positively with vent temperature and dissolved oxygen inversely, so the highT/lowT split may stand in for unmeasured geochemistry. All inferred species interactions (e.g. hydrogen-transfer mutualisms between breviate amoebae and Arcobacter-type epsilonbacteraeots, heterotrophic Bacteroidetes exploiting mucus from the polychaetes Depressigyra globulus and Paralvinella palmiformis, nematode mucus fueling aerobic heterotrophs, ciliates as meiofaunal prey) rest on covariance and enrichment, and the authors note the well-known caveat that co-occurrence is not evidence of interaction. Within the highT core, two faunal sub-clusters hinted at finer niche partitioning that the sampling did not resolve, and tubeworm grabs (relative to fluids) contained many OTUs classifiable only to phylum or domain — a reservoir of novelty whose functional roles were proposed as targets for future metagenomics. Comparable questions have been pursued in adjacent systems: Ladd et al. (Deep-Sea Research I 208:104314, 2024) used in-situ colonization surfaces at the East Pacific Rise to show that larval settlers, including the mussel Bathymodiolus thermophilus, prefer established microbial biofilms; Fullerton et al. (FEMS Microbiology Ecology 100:fiae001, 2024) deployed seafloor incubation chambers at Juan de Fuca/Ridge seamounts and found dissolved iron to be the strongest driver of nascent microbial community structure; and Alfaro-Lucas et al. (Scientific Reports 14:1940, 2024) exploited the chemically anomalous Capelinhos edifice at Lucky Strike to show that strongly contrasting fluid chemistry alters faunal trophodynamics but not faunal composition.

Problem Statement

For hydrothermal-vent communities associated with Ridgeia piscesae tubeworm aggregations (Endeavour and Middle Valley segments, Juan de Fuca Ridge), establish the causal and mechanistic basis of the emergent cross-domain core-community organization that Murdock et al. (2021) described structurally. Specifically: (1) determine the relative contributions of temperature per se versus covarying geochemical variables — sulphide concentration, dissolved oxygen, and other diffuse-fluid constituents — to the highT/lowT (~25 °C) partition of the microbial, meiofaunal and macrofaunal core communities; (2) test whether the specific covariance- and enrichment-based associations inferred within the core communities (e.g. breviate amoebae-Epsilonbacteraeota hydrogen-transfer mutualisms, Bacteroidetes associating with mucus-secreting polychaetes, nematode-mucus-fueled aerobic heterotrophy, ciliates as meiofaunal prey) reflect real ecological interactions; (3) resolve whether the sub-components detected within the high-temperature core community reflect finer niche partitioning by environmental conditions within tubeworm grabs; and (4) establish the functional roles of the numerous novel or weakly classified OTUs — particularly those found exclusively in tubeworm-hosted assemblages. These four deliverables jointly serve one objective: converting the described structure of these foundation-species-associated communities into a causal and functional understanding of their organization. Each deliverable is independently attackable and resolves its own facet of that objective, whereas resolving the objective as a whole requires progress on all four.

References

  1. Murdock, S. A., Tunnicliffe, V., Boschen-Rose, R. E., & Juniper, S. K. (2021). Emergent “core communities” of microbes, meiofauna and macrofauna at hydrothermal vents. ISME Communications 1, article 27. DOI 10.1038/s43705-021-00031-1. https://doi.org/10.1038/s43705-021-00031-1
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