The Sources of Organic Carbon in the Deepest Ocean: Implication From Bacterial Membrane Lipids in the Mariana Trench Zone

Abstract

Hadal trenches have higher microbial carbon turnover rates as compared to adjacent abyssal plains. However, the source of organic carbon in the trench remains enigmatic. In this study, we show that a fraction of organic carbon is possibly derived in situ and correlated with chemoautotrophic communities supported by the fluid discharge of water-rock interaction in the trench wall, based on analysis of glycerol dialkyl glycerol tetraether (GDGT) membrane lipids, including archaeal isoprenoid GDGTs (IsoGDGTs) and bacterial branched GDGTs (BrGDGTs), in sediments and rocks of the Mariana and Yap Trenches, northwest Pacific Ocean. These trench sediments contained relative higher BrGDGTs ratios, which was a rare observation in the open ocean. The BrGDGT-to-IsoGDGT ratios ranged in 0.02–0.88 (mean = 0.10 ± 0.11) in sediments and 0.09–0.38 (mean = 0.17 ± 0.13) in altered rocks. The calculated values of branched and isoprenoid tetraether (BIT) index ranged from 0.02–0.73 (mean = 0.18 ± 0.11) in sediments and from 0.16–0.9 in altered rocks (mean = 0.37 ± 0.27). Moreover, these GDGTs exhibited similar characteristics to those of altered basalt rocks, indicating inputs of organic carbon from the trench subsurface environment. Thus, in addition to organic-rich material settling, we propose chemoautotrophic activity in oceanic crust could be an additional source of organic carbon in the deepest part of the ocean, with an important role in deep-sea carbon cycles.

Chemolithotrophic biosynthesis of organic carbon associated with volcanic ash in the Mariana Trough, Pacific Ocean

“…To determine the origin of the brGDGTs, a ternary diagram of IIa + IIa', IIIa + IIIa' and Rings penta-hexa was used according to ref. 25 . The tuffs and background sediments have high ratio of acyclic hexamethylated brGDGTs versus pentamethylated brGDGTs abundance (i.e., ΣIIIa/ΣIIa > 0.92), quite different from global soil and peat analyses (Fig.…”

“…The brGDGTs share many characteristics with those of chemolithotrophic ecosystems, such as hydrothermal fields 28,36,[42][43][44][45] , cold seeps 27 , terrestrial serpentinites 37 , and altered rocks from the Mariana Trench 25,26 . Specifically, all tuffs have higher BIT values and lower R i/b ratios than normal marine sediments (see Fig.…”

“…The dark and light orange color represent tuffs and marine samples, respectively; while samples from chemolithotrophic systems and land are represented by yellow and gray, respectively. Data sources: tuffs and background sediments from this study, Mariana Trench sediments 32 , altered rocks and sediments 25,26,35 , hydrothermal deposits 28,[42][43][44][45] , cold seep carbonates 27 , serpentinites 37 , and the data source of global soil and peats datasets please see Supplementary References 9-24.…”

“…IsoGDGTs dominate the membrane lipids of marine Thaumarchaeota 21 , while brGDGTs can be produced by Acidobacteria which are living in terrestrial environments [22][23][24] . However, there are relatively high abundance of brGDGTs in typical chemolithotrophic systems, such as hydrothermal field, cold seeps and ocean crust rocks [25][26][27][28] . These environments are characterized by active geological processes that produce sufficient chemical sources for chemoautotrophs to be the primary producers in ecosystems [29][30][31] .…”

Macrofauna and Nematode Abundance in the Abyssal and Hadal Zones of Interconnected Deep-Sea Ecosystems in the Kuril Basin (Sea of Okhotsk) and the Kuril-Kamchatka Trench (Pacific Ocean)

“…For example, hadal cold seep communities in the Japan Trench were found to a depth of 7,326 m (Fujikura et al, 1999;Okutani et al, 1999;Sasaki et al, 2005). Also, Li et al (2021) suggest that the chemoautotrophic activity in the oceanic crust could be an additional source of organic carbon in trench sedimentary environments. Thus, our study confirms that abundant bottom communities, some of which supposedly utilize nutrients produced by chemosynthetic bacteria, are formed within the abyssal and hadal zones in the area of the Kuril-Kamchatka Trench, located in the eutrophic region of the Pacific Ocean.…”