194 / 2024-09-11 10:06:34

Exploring incorporation of DIC by heterotrophic prokaryotes: a key process in deep/dark ocean microbial carbon cycling

dark carbon fixation,heterotrophic prokaryotes,Dissolved organic carbon,stable isotopic probing,Microbial carbon cycling

The dark ocean, accounting for ~70% of the global ocean volume, plays a significant role in the global carbon cycle. Heterotrophic microorganisms in the dark ocean primarily rely on particulate organic carbon (POC) sinking from the euphotic zone for respiration, contributing to the long-term storage of dissolved inorganic carbon (DIC) and recalcitrant dissolved organic carbon (RDOC) through the biological and microbial carbon pumps. However, there exists a discrepancy between the carbon demand of heterotrophic microorganisms and the supply of POC, which can be compensated by dark carbon fixation—a process that includes both chemolithoautotrophic carbon fixation and incorporation of DIC by heterotrophic prokaryotes. This study aims to explore the underappreciated role of heterotrophic carbon fixation in deep ocean microbial carbon cycling. We conducted small-volume incubation experiments using seawater from the Aquatron tower, a large volume (117,000 L) incubation facility at Dalhousie University, simulating deep-sea conditions. Using ¹³C-labeled DIC and various organic or oxidizable inorganic nitrogen compounds, dark carbon fixation was examined through short-term (3-7 days) DNA-based stable isotope probing and long-term (104 days) biogeochemical analyses. Our results reveal that the assimilation of DIC by heterotrophic prokaryotes significantly contributes to total dark carbon fixation, with distinct interactions between dark carbon fixation, degradation of external organic carbon, and nutrient cycles. The addition of DOC stimulated dark carbon fixation rates, reaching values 10 to 30 times higher than in-situ rates and comparable to surface primary production levels. We observed that D-Leucine, L-Leucine, and Methanol stimulated dark carbon fixation, accounting for up to 20% of the added DOC content and about 40% of remaining POC. The dark fixed carbon could accumulate in POC for a long time (at least 104 days). The dark carbon fixation was mainly contributed by heterotrophic Alphaproteobacteria, Gammaproteobacteria, Dadabacteria, as well as other diverse heterotrophs. Our findings highlight the substantial role of heterotrophic carbon fixation in deep ocean carbon cycling, suggesting that it could exceed autotrophic processes due to the higher abundance of heterotrophic prokaryotes. This study emphasizes the need to consider heterotrophic pathways in global carbon models, as they may play a critical role in carbon storage and transformation in the dark ocean, thereby influencing long-term carbon sequestration.