Limited carbon cycling due to high-pressure effects on the deep-sea microbiome

Abstract

Deep-sea microbial communities are exposed to high-pressure conditions, which has a variable impact on prokaryotes depending on whether they are piezophilic (that is, pressure-loving), piezotolerant or piezosensitive. While it has been suggested that elevated pressures lead to higher community-level metabolic rates, the response of these deep-sea microbial communities to the high-pressure conditions of the deep sea is poorly understood. Based on microbial activity measurements in the major oceanic basins using an in situ microbial incubator, we show that the bulk heterotrophic activity of prokaryotic communities becomes increasingly inhibited at higher hydrostatic pressure. At 4,000 m depth, the bulk heterotrophic prokaryotic activity under in situ hydrostatic pressure was about one-third of that measured in the same community at atmospheric pressure conditions. In the bathypelagic zone—between 1,000 and 4,000 m depth—~85% of the prokaryotic community was piezotolerant and ~5% of the prokaryotic community was piezophilic. Despite piezosensitive-like prokaryotes comprising only ~10% (mainly members of Bacteroidetes, Alteromonas) of the deep-sea prokaryotic community, the more than 100-fold metabolic activity increase of these piezosensitive prokaryotes upon depressurization leads to high apparent bulk metabolic activity. Overall, the heterotrophic prokaryotic activity in the deep sea is likely to be substantially lower than hitherto assumed, with major impacts on the oceanic carbon cycling.

A device for assessing microbial activity under ambient hydrostatic pressure: The in situ microbial incubator (ISMI)

“…6b; Table S3). These rates were 67-83% of that measured under atmospheric pressure conditions on samples collected by Niskin bottles (Christaki et al 2021;Amano et al 2022). In the North Atlantic, leucine incorporation rates under in situ pressure conditions were 0.24 AE 0.01 pmol leu L À1 h À1 in the mesopelagic and 0.003 AE 0.000 pmol leu L À1 h À1 in the bathypelagic layers (Fig.…”

“…In the North Atlantic, leucine incorporation rates under in situ pressure conditions were 0.24 AE 0.01 pmol leu L À1 h À1 in the mesopelagic and 0.003 AE 0.000 pmol leu L À1 h À1 in the bathypelagic layers (Fig. 6b; Table S3), 51-57% of that measured under atmospheric pressure conditions (Amano et al 2022). Hence, our results indicate substantially lower bulk heterotrophic activity under in situ hydrostatic pressure than under depressurized conditions.…”

“…The dark ocean, making up in terms of volume > 90% of the world's living space, is a key ecosystem in biodiversity and functioning of the ocean (Robison 2009;Levin and Le Bris 2015). However, estimates on the metabolic activity of the most abundant living entity in the oceans, the prokaryotes, at depth below 200 m are still relatively rare compared to the data available for epipelagic waters (Herndl et al 2022). In addition, below those epipelagic waters almost all metabolic activity measurements taken were carried out using decompressed samples.…”

“…Garcin 1994; Tholosan et al 1999;Tamburini et al 2002Tamburini et al , 2003Tamburini et al , 2009Garel et al 2019). The vast majority of studies measuring deep-sea microbial activity, however, have been performed under atmospheric pressure conditions (Aristegui et al 2009;Herndl et al 2022).…”

Cultivation of SAR202 Bacteria from the Ocean

“…In the dark ocean, where polysaccharides are depleted, however, paralogous gene expansions may provide group I with a competitive advantage by allowing them to use a diverse range of sugars, sugar acids, and related compounds, leading to the observed increase in relative abundance. Piezotolerance of SAR202 cells would also give them a competitive advantage in the dark ocean 61 .…”