Natural marine prokaryote communities are mixtures of piezosensitive surface-derived organisms and piezotolerant or piezophilic deep-sea organisms, and the sinking of particles through the water column exposes these mixed assemblages to steadily increasing hydrostatic pressure. A 2013 review established that pressure effects on pure cultures are well studied while community-level impacts in the ocean were 'less well defined', and that routine measurements on decompressed samples at atmospheric pressure distort estimates of in situ activity. A decade of follow-up work — pressure-retaining samplers, high-pressure incubators, rotating pressure tanks, sinking simulators, isobaric enzyme assays, and basin-scale in situ incubations — has produced quantitative but directionally conflicting results, discovered new pressure-driven pathways such as pressure-induced leakage of dissolved organic matter from marine snow, and confirmed that conventional sampling artifacts are large and taxon-dependent. No quantitative, community-resolved general account of how prokaryote metabolism and organic-matter degradation track the pressure regime of particle descent exists, and no validated general correction for decompression artifacts in routine laboratory practice has been established: the problem remains open.

Background

About 70% of the ocean lies deeper than 1,000 m, where hydrostatic pressure increases by roughly 0.1 MPa (one atmosphere) per 10 m of depth, reaching beyond 100 MPa in the deepest trenches. Marine prokaryotes (bacteria and archaea) are classified by their growth response to pressure: piezosensitive organisms grow best at atmospheric pressure and are inhibited as pressure rises, piezotolerant organisms grow across a wide pressure range including atmospheric, and piezophilic organisms (obligate piezophiles in the deepest realms) require elevated pressure to grow. Most marine prokaryotes are thought to be piezotolerant or piezophilic, yet few have cultivated representatives, so their biochemistry and physiology remain largely unknown (Zhang et al. 2015, doi:10.1016/j.copbio.2015.02.013). This matters to the ocean carbon cycle because the biological carbon pump exports organic matter from the sunlit surface ocean mainly as sinking particles — 'marine snow' aggregates, plankton carcasses, and fecal pellets — and particle-attached and free-living prokaryotes remineralize that particulate organic carbon (POC) during its descent, attenuating the flux that reaches the seabed. The microbes riding a sinking particle experience a continuously changing pressure–temperature regime, and the attached community is itself a mixture: surface-origin piezosensitive taxa transported downward plus piezotolerant and piezophilic deep-water taxa. Community-level metabolism is usually assayed from water or particle samples recovered by Niskin bottles or traps, which decompress and often warm the sample before incubation at atmospheric pressure (~0.1 MPa); exoenzymatic hydrolysis (the extracellular enzymes that cleave particulate polymers into assimilable subunits) and bulk heterotrophic activity (community-level uptake/respiration of organic substrates) are typically measured only under these decompressed conditions. The anchor review of this problem (Tamburini et al. 2013, doi:10.1111/1462-2920.12084) synthesized experiments mimicking the pressure changes of particle descent and concluded that pure-culture pressure effects were well studied but community-level impacts in the ocean were 'less well defined'; that, under stratified conditions, deep-sea communities adapted to in situ high pressure, low temperature, and low organic matter mean decompressed atmospheric measurements underestimate in situ activity, with overestimating exceptions attributed to deep mixing, large surface-particle influxes, or excessive organic matter in experiments; and that the sediment–water interface hosts mixtures of piezosensitive, piezotolerant, and piezophilic prokaryotes whose pressure-dependence differs. Subsequent methodological work — pressure-retaining samplers and high-pressure incubation systems (Garel et al. 2019, doi:10.3389/fmicb.2019.00453), pilot systems measuring activity and composition simultaneously at high pressure (Wannicke et al. 2015, doi:10.1093/femsec/fiv036), rotating pressure tanks that keep aggregates in a sinking mode (Stief et al. 2021, doi:10.1002/lno.11791), and particle sinking simulators reproducing full water-column pressure–temperature trajectories (Tamburini et al. 2021, doi:10.3390/w13192616) — made the experiments possible, but the community-level answer remains contested.

Problem Statement

Determine, quantitatively and at the level of natural mixed communities, how the metabolic and organic-matter-degradation activity of marine prokaryotes — assemblages combining piezosensitive surface-origin organisms with piezotolerant and piezophilic deep-sea organisms — responds to the hydrostatic-pressure changes the communities actually experience as particles sink through the water column (and as mixing redistributes communities across depth), including how pressure alters community composition, bulk heterotrophic activity, extracellular enzymatic hydrolysis, and the partitioning of particulate organic carbon among respiration, transformation, and release as dissolved organic matter. The account must state, for each of these processes and at the level of natural mixed communities, the sign of the pressure effect and — where the evidence supports it — a quantitative pressure-response relationship with stated units, explicitly resolving its dependence on community composition and flagging where only a direction, not a magnitude, is supported; coverage across depth, taxon, particle type, and ocean basin may be representative rather than exhaustive, provided the dependence across those dimensions is mapped rather than inferred from a single case. From that account, establish what correction of routine laboratory practice — decompression during sample recovery and incubation at atmospheric pressure — is required (or show that no general correction applies) so that ex situ measurements recover in situ activity. These two deliverables serve one scientific objective: correct quantification of in situ prokaryotic organic-matter degradation in the ocean interior, since the community-level pressure response is what the measurement correction must encode. The question is stated at its natural generality — no specific depth range, taxon, particle type, method, or ocean basin is excluded — because the conflicting directional results now in the literature (inhibition, insensitivity, and pressure-induced DOM leakage across particle types and communities) show the answer depends on mapping the dependence across these dimensions rather than on any single case.

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