Novel insights into the Thaumarchaeota in the deepest oceans: their metabolism and potential adaptation mechanisms

Abstract

Background: Marine Group I (MGI) Thaumarchaeota, which play key roles in the global biogeochemical cycling of nitrogen and carbon (ammonia oxidizers), thrive in the aphotic deep sea with massive populations. Recent studies have revealed that MGI Thaumarchaeota were present in the deepest part of oceans-the hadal zone (depth > 6000 m, consisting almost entirely of trenches), with the predominant phylotype being distinct from that in the "shallower" deep sea. However, little is known about the metabolism and distribution of these ammonia oxidizers in the hadal water. Results: In this study, metagenomic data were obtained from 0-10,500 m deep seawater samples from the Mariana Trench. The distribution patterns of Thaumarchaeota derived from metagenomics and 16S rRNA gene sequencing were in line with that reported in previous studies: abundance of Thaumarchaeota peaked in bathypelagic zone (depth 1000-4000 m) and the predominant clade shifted in the hadal zone. Several metagenome-assembled thaumarchaeotal genomes were recovered, including a near-complete one representing the dominant hadal phylotype of MGI. Using comparative genomics, we predict that unexpected genes involved in bioenergetics, including two distinct ATP synthase genes (predicted to be coupled with H + and Na + respectively), and genes horizontally transferred from other extremophiles, such as those encoding putative di-myo-inositol-phosphate (DIP) synthases, might significantly contribute to the success of this hadal clade under the extreme condition. We also found that hadal MGI have the genetic potential to import a far higher range of organic compounds than their shallower water counterparts. Despite this trait, hadal MDI ammonia oxidation and carbon fixation genes are highly transcribed providing evidence they are likely autotrophic, contributing to the primary production in the aphotic deep sea. Conclusions: Our study reveals potentially novel adaptation mechanisms of deep-sea thaumarchaeotal clades and suggests key functions of deep-sea Thaumarchaeota in carbon and nitrogen cycling.

Shift and Metabolic Potentials of Microbial Eukaryotic Communities Across the Full Depths of the Mariana Trench

“…Despite these information, little is known about the microbial eukaryotic communities and metabolic potentials in the deeper seawaters (8,727–11,000 m) of the Mariana Trench, where unique microbial populations (e.g., increased amount of SAR406, hydrocarbon-degrading microbes) have been observed ( Ichino et al, 2015 ; Nunoura et al, 2015 ; Liu et al, 2018 , 2019b ; Gao et al, 2019 ). In addition, whether microbial eukaryotes exhibit unique high-pressure adaptation mechanisms as found in bacteria and archaea in our previous studies ( Zheng et al, 2020 ; Zhong et al, 2020 ) is still unknown. Thus, knowledge of microbial eukaryotes at the bottom of the Mariana Trench, the deepest ocean part on Earth, is necessary for a better understanding of their ecological roles and potential adaptability.…”

Microbial ecology of the newly discovered serpentinite-hosted Old City hydrothermal field (southwest Indian ridge)

“…However, although such metabolisms have been reported to be possible in other serpentinite-hosted ecosystems [55][56][57], a low concentration of nitrate is usually documented in such systems. OCT and ToMo are dominated by Thaumarchaeota, which are more likely to originate from deep seawater where they are widespread [71], than from hydrothermal fluids. The relative enrichment in ammonia monooxygenase-encoding genes (amoA) in OCT and ToMo suggests that Thaumarchaeota could be involved in aerobic ammonia oxidation.…”

Leave no stone unturned: The hidden potential of carbon and nitrogen cycling by novel, highly adapted Thaumarchaeota in the Atacama Desert hyperarid core

“…Multiple copies of aquaporin genes per genome as well as the divergent and truncated subset indicate possible genome specific adaptations to desiccation and osmotic stress. We also recovered two distinct types of ATP synthases (namely A-type and V-type (67,68)) from the eight ABT genomes. Three ABT genomes (ABT-LB2, ABT-LB3, ABT-YB1) contained only A-type ATP synthase, while the rest contained both the A-type and the V-type ATP synthases often in multiple copies.…”

“…Considering that Atacama Desert soils are slightly alkaline (average pH = 7.7 Figure S13), it is surprising that the V-type ATP synthase is found and conserved across five ABT genomes. Zhong et al (68) hypothesized that these V-type ATP synthases may be coupled with Na + motive force instead of proton pumping. Atacama Desert soils present high salt stress, and therefore the V-type ATP synthase could perform Na + pumping and provide protection against high sodium stress (Table S14).…”