Hadal trenches are dynamic hotspots for early diagenesis in the deep sea

Hadal trenches, extending from 6,000 to 11,000 meters deep, are located along tectonic subduction zones and represent the deepest parts of the global ocean. While conditions like temperature, oxygen availability, and current velocities resemble those in other deep-sea environments, the extreme hydrostatic pressure and geographic isolation lead to lower biodiversity and endemism among the piezophilic communities. Seismic activity, downslope funneling, and fluid dynamics enhance local deposition, making hadal trenches significant depocenters for organic matter. Previous research has shown elevated abundance of prokaryotes, infauna, and scavenging fauna in the deepest parts of trenches compared to adjacent abyssal plains, suggesting that enhanced organic matter deposition supports higher biological activity despite the extreme conditions. However, the technical challenges of sampling at hadal depths and potential artifacts from pressure and temperature changes during sample recovery have limited our understanding. In-situ measurements of benthic oxygen uptake offer a robust proxy for biological activity and carbon mineralization in deep-sea settings. Studies measuring benthic oxygen uptake have shown a decrease in mineralization rates from coastal oceans to abyssal plains (6000m). Recent in-situ measurements in the deepest parts of trenches suggest this pattern reverses in the hadal realm, implying that intensified organic matter deposition enhances biological activity and carbon mineralization. However, these studies focused primarily on the deepest points of trenches, neglecting the within-trench variability that likely influences seafloor conditions across depths and along the trench axis. Therefore, understanding within-trench variability is crucial for comprehending element cycling and early diagenesis in these unique environments. This study aims to investigate the availability and mineralization of organic carbon in two contrasting hadal systems: the Kermadec and Atacama trenches, to better understand the processes driving the observed high levels of biological activity.

Numerous studies have explored the unique characteristics of hadal trenches and their role as organic matter depocenters. Early research by Jumars & Hessler (1976) and Tietjen et al. (1989) highlighted the distribution and abundance of meiobenthos and macrofauna in hadal environments, noting elevated levels in comparison to abyssal plains. Studies following major seismic events, such as the Tohoku-Oki Earthquake (Oguri et al., 2013), demonstrated the significant impact of such events on sediment deposition and organic carbon influx into hadal trenches. The work of Bao et al. (2018) and Kioka et al. (2019) further emphasized the link between tectonic activity and carbon export to these deep-sea environments. However, prior research has often been limited by sampling difficulties and potential artifacts in sample recovery from these extreme depths. In-situ measurements provide a superior method to understand benthic oxygen consumption and consequently, biological activity, as presented in work by Glud et al (2013), Wenzhöfer et al. (2016), and Luo et al. (2018). These studies have suggested a link between surface ocean productivity and hadal benthic oxygen uptake, but lacked comprehensive investigation of within-trench variability. Understanding the complex interplay between surface primary production, sediment deposition dynamics, and benthic activity within hadal trenches remains a significant challenge requiring further research.

This study investigated the Kermadec and Atacama trenches during two separate research cruises in 2017 and 2018. A total of 14 hadal sites across the two trenches were selected, along with abyssal reference sites for comparison. The Kermadec sites covered a 483 km transect (9300–10,010 m depth), while the Atacama sites covered a 445 km transect (7720-8085 m). Surface primary production estimates for each region were obtained from a model using remote sensing data. At each site, two autonomous instruments were deployed: a Reiver for sediment surface probing and imaging, and a Hadal-Profiler Lander for measuring benthic oxygen distribution. The Reiver helped assess seafloor suitability before lander deployment. The Hadal-Profiler Lander used an array of oxygen microsensors to measure multiple oxygen microprofiles during 15-24-hour deployments. These profiles were used to calculate diffusive oxygen uptake (DOU), a robust proxy for sediment community respiration at deep-sea settings. Intact sediment cores were recovered using various methods (multi-corer, autonomous coring lander, box-corer) and analyzed for porosity, total organic carbon (TOC), and phytodetrital pigment concentrations. A total of 206 microprofiles were obtained and analyzed, excluding those disturbed by infauna or other sediment features. Statistical analysis, linear regression, and comparison with previous findings were conducted to correlate oxygen uptake rates with organic matter content, Chlorophyll a levels, and surface primary production.

The study revealed significant variations in benthic oxygen consumption rates between and within the two trench systems. The lowest oxygen uptake was recorded at an abyssal site off the Kermadec trench axis (152 ± 22 µmol m⁻²d⁻¹), while the highest rates were observed in the Atacama trench (up to 1793 ± 77 µmol m⁻²d⁻¹). All hadal sites exhibited higher oxygen uptake than adjacent abyssal plains. In both trenches, oxygen consumption rates were highest near the sediment surface and also showed a secondary peak near the oxic-anoxic interface. This pattern suggests that both labile organic carbon at the surface and oxidation of reduced inorganic constituents at the interface contribute significantly to overall aerobic activity. There was a strong correlation between diffusive oxygen uptake (DOU) and both total organic carbon (TOC) content and Chlorophyll a concentration in surface sediments. This suggests that the input and lability of organic matter are key factors influencing benthic activity. Higher surface primary production in the Atacama region corresponded to higher benthic oxygen consumption compared to Kermadec. However, the within-trench variability in Kermadec highlighted the importance of local deposition dynamics in modulating benthic activity. Analysis revealed that hadal benthic mineralization corresponds to 1.6% of the overlying surface production, approximately 1.5-2.0 times higher than the vertical depositional flux. While oxygen microprofiles showed some inorganic reoxidation at the oxic-anoxic interface, significant reduced equivalents (inorganic sulfur and ferrous iron) were detected in the Atacama Trench sediments, suggesting that the measured oxygen consumption may underestimate total carbon mineralization. These findings confirm that hadal trenches function as hotspots of deep-sea early diagenesis, despite the significant variability in benthic activity.

The findings address the research question by demonstrating that hadal trenches are indeed significant sites of intensified early diagenesis, driven by a complex interplay of factors. The strong correlation between benthic oxygen consumption and organic matter content highlights the critical role of organic matter deposition in fueling this activity. The significant variability observed within and between trenches underscores the importance of local depositional processes, including mass-wasting events, fluid dynamics, and the transport of labile organic carbon from shallower regions, in shaping benthic metabolism. The higher-than-expected carbon mineralization rates in hadal settings relative to depositional fluxes suggest that lateral inputs of reactive organic matter are a key factor. The observed connection between surface primary productivity and benthic activity, modulated by local deposition, highlights the integration of large-scale oceanographic processes and small-scale sedimentary dynamics in these deep-sea environments. These findings provide new insights into the biogeochemical functioning of hadal trenches, advancing our understanding of deep-sea ecosystems and their role in global carbon cycling. The observed variability emphasizes the need for future research considering temporal changes and local influences on hadal ecosystems.

This study demonstrates that hadal trenches are dynamic hotspots for early diagenesis in the deep sea, exhibiting higher rates of carbon mineralization than adjacent abyssal plains. The observed high variability in benthic activity highlights the importance of local depositional processes and complex interactions between surface ocean productivity and bottom water conditions in shaping these unique environments. Future studies should focus on further quantifying the role of anaerobic processes, improving our understanding of organic matter lability, and investigating temporal variability to fully characterize the function of hadal trenches in the global carbon cycle. Further exploration of the diversity and interactions of the benthic community is needed to fully understand the deep-sea biogeochemical cycling.

The study acknowledges that recovering intact sediment cores from hadal depths is challenging, and some key findings are based on a subset of successfully retrieved cores. Furthermore, the assumption of a respiratory quotient of 1.0 may not fully capture the complex redox processes occurring in hadal sediments, potentially underestimating the total carbon mineralization rates. Finally, the study focused primarily on two trenches in the Pacific Ocean, and further investigations are needed across diverse hadal environments to broaden the scope and generalizability of these findings.