Respiratory quotients of particle-associated microbes track carbon flux attenuation in the mesopelagic Southern Ocean

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Mesopelagic microbes and zooplankton, degrade and attenuate >90% of the 10 billion tonnes of Particulate Organic Carbon (POC) that sinks into the oceans’ interior annually. Approaches such as particle interceptors/incubators (called C-RESPIRE) can isolate the microbial assemblage attached to particles from that of zooplankton, enabling quantification of microbially-mediated POC flux attenuation. This metric yields patterns of POC degradation by microbes through the upper mesopelagic (200-500 m depth). Here, we investigate the temporal sequence of POC degradation in two steps. First, we intercept sinking particle assemblages from different depths (180-300 m) and hence with varying degrees of exposure to microbial activity. Second, we incubate these intercepted particles shipboard for 12h (short-term) and track degradation using Apparent Respiratory Quotients (ARQ, dDIC/dDO2). We also incubate shipboard (12h) a particle assemblage previously incubated (36h) in situ using C-RESPIRE (long-term). At a subantarctic and two polar sites, ARQs from short-term incubations exhibited a significant decrease with depth, consistent with particles deeper in the upper mesopelagic being exposed to a longer period of degradation and flux attenuation (as they settle). ARQs from all long-term incubations had significantly lower ARQs, and smaller depth-dependent gradients, than the short-term incubations. We interpret these trends as being driven in part by sequential changes in the stoichiometry of the microbially-altered POC substrates. Several ARQs of <0.5 (less than the theoretical minimum) were observed in long-term incubations suggesting a role for incomplete oxidation of substrates. This temporal sequence is used to conceptually explore what sets the limits on microbially-mediated degradation of POC.

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Statement: Samples were obtained during the SOLACE (Southern Ocean Large Area Carbon Export) voyage from 4 December 2020 to 15 January 2021. Surface-tethered free-drifting particle interceptor traps (PITs) and C-RESPIRE dual particle interceptor/incubators (Fig. 1) were deployed repeatedly at three depths in the upper mesopelagic (S-Table 1) at one subantarctic (SOTS, Southern Ocean Time Series, Erikson et al., 2018) and two polar sites (Fig. 2A). All sites were located in low advective regimes based on satellite maps of sea surface height anomaly (Boyd et al., 2024). Deployment depths differed slightly between sites to accommodate varying mixed layer depths (50 m SOTS, 65 m PF1, 75 m, PF2). Therefore, in the Results the trap deployments are referred to as depth 1 (shallowest), 2 (intermediate) and 3 (deepest). Profiling robotic floats (https://biogeochemical-argo.org/) were deployed during SOLACE at SOTS and PF1 and provided ancillary data on particle dynamics (see Supplementary Materials). Trap deployments At each site, due to mooring design constraints, PIT and C-RESPIRE traps were deployed ~20 m apart (S-Table 1), on the same array for in situ particle interception (Supplementary Fig. S2) prior to incubation. Three types of PIT tubes were prepared: a) used a preservative (buffered-formalin brine) for analyses of POC, Particulate Organic Nitrogen (PON), Biogenic Silica (BSi), and chlorophyll a (Petiteau et al. accepted); b) had polyacrylamide gel in the base of the trap to observe particle characteristics using microscopy; c) had no preservative to obtain 'fresh' sinking particles to subsequently determine ARQ shipboard. Upon recovery, PIT tubes with preservatives or gels were processed (See Supplementary Materials). A subsample of particles from PIT tubes with no preservatives were incubated to measure ARQs. For the C-RESPIRE traps, a subsample of the post-incubation particle assemblage was further incubated onboard to estimate the ARQ (Supplementary Fig. S1 and S2). Subsamples of the seawater from C-RESPIRE were analyzed to estimate nitrification rates (S-Table 2) and DOC accumulation (Supplementary Materials). Sample analysis and ARQ determination PIT tube C and subsamples of C-RESPIRE particles were transferred to a temperature-controlled lab (S-Table 3). Each tube was placed upright in darkness for one hour for disturbed particles to re-settle (following transit to the lab). Then the overlying water was gently siphoned off. Particles were harvested and placed in 4 mL glass sample vials each containing a PreSens O2 and CO2 sensor, and filled with 0.2 µm filtered sea water from the depth of deployment (Supplementary Fig. S3). A subsequent lab-based experiment to map ARQs on a krill pellet (presented in Fig. 4) employed a modified optode system in conjunction with a flow chamber

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Credit
This research was supported by the Australian Research Council Special Research Initiative, Australian Centre for Excellence in Antarctic Science (ACEAS) (Project Number SR200100008).