Life under pressure in prokaryotes and the impact on the biological carbon pump

The deep ocean, one of Earth's largest and least explored biomes, spans depths with extreme conditions, including high hydrostatic pressure, low temperatures, and minimal organic carbon. These characteristics significantly influence microbial life, requiring unique adaptations for survival and metabolic function. Prokaryotes thriving in high-pressure environments are known as piezophiles (Tamburini et al. 2013 and references therein). Those deep-sea micro-organisms adapt to high-pressure environments through cellular and genetic changes, constitute ‘bathytypes’  specific  to ocean depths (Oger and Jebbar 2010; Peoples and Bartlett 2017).

Due to technical challenges in sampling under in situ conditions, much of the data about deep-sea microbes has historically been gathered under decompressed conditions. This decompression can result in significant changes in community composition (La Cono et al. 2009; Edgcomb et al. 2016; Garel et al. 2019) and activity (Tamburini et al. 2013; Garel et al. 2019), which generally leads to underestimated assessments of their ecological roles. Innovations, such as pressure-retaining samplers (Peoples and Bartlett 2017; Garel et al. 2019) or in situ microbial incubator (Amano et al. 2022a), now allow for the collection or incubation of samples at in situ pressures, preserving the natural state of these microorganisms for more accurate study .

Deep-sea microbes play a critical role in the global carbon cycle, particularly through their participation in the biological carbon pump, which involves the decomposition and mineralization of organic material as it sinks through the water column (Arıstegui et al. 2009). Research suggests that deep-sea microbes are dynamically responsive to organic matter input, with a substantial portion of global heterotrophic production occurring below the photic zone. According to Aristegui et al. (2009) the integrated prokaryotic heterotrophic production (PHP) in the dark ocean represents around 50% of the total water column. Understanding the pressure effect on prokaryotic activities is crucial to better estimate their role in the remineralization in the dark ocean. However, to date, the effect of decompression is controversial, depending on the methodology used and the authors (Amano et al. 2022b versus Tamburini et al. 2013 and reference therein). 

Continued advancements in sampling technology and high-throughput sequencing will likely reveal more about these resilient organisms' ecological roles and physiological capacities, enhancing our comprehension of the deep ocean's contributions to Earth's biogeochemical processes​.

Over the last few years, pressure-retaining samplers were deployed during different oceanographic cruises in North Atlantic Ocean and in the Mediterranean Sea, allowing the constitution of a unique dataset of PHP rates (using 3H-Leucine) and MICROFISH, under in situ conditions. Among this cruise, a specific one dedicated to the study of deep convection and re-stratification phenomena brings new insights in the biological and physical coupling of this study area, and the necessity to well understand this context when talking about organisms adapted to pressure or not. Pressure effects on other activities (dark dissolved inorganic carbon fixation, ectoenzymatic activities, and high molecular organic compounds' degradation) will also be presented. Finally, we will also show how surface prokaryotes attached to gravitationally sinking particles cope with the increase in pressure with depth.