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

Haohui Zhong,Delei Song,Heyu Lin,Xiao-Hua Zhang,Jonathan D Todd,Jiwei Tian,Jiwen Liu,Laura Lehtovirta-Morley,Yanfen Zheng

doi:10.1186/s40168-020-00849-2

Abstract

BackgroundMarine 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.ResultsIn 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.ConclusionsOur study reveals potentially novel adaptation mechanisms of deep-sea thaumarchaeotal clades and suggests key functions of deep-sea Thaumarchaeota in carbon and nitrogen cycling.En6fqpb_2L47ybAR2Rb-e_Video

Highlights

Concepts of the carbon cycle in deep sea have been challenged due to recent re-evaluation of the imbalance between the quantity of sinking organic carbon from surface and the consumption by deep-sea heterotrophic microorganisms
Evidence of autotrophy in MTA1 Considering the presence of both the inorganic carbon fixation pathway and the large complement of predicted transporters for organic compounds in the MTA1 metagenomeassembled genomes (MAGs), we further investigated whether the lifestyle of archaea in the hadal zone is autotrophic
We postulate that genes involved in bioenergetics and osmoprotectant biosynthesis are important in the adaptation of ammonia-oxidizing archaea to the high hydrostatic pressure in the deep sea and we further demonstrated the transcriptional activity of the myo-inositol production pathway in these archaea

Summary

Introduction

Concepts of the carbon cycle in deep sea (depth > 200 m) have been challenged due to recent re-evaluation of the imbalance between the quantity of sinking organic carbon from surface and the consumption by deep-sea heterotrophic microorganisms. Marine Thaumarchaeota are chemolithoautotrophs and considered to be important participants in this dark primary production process [4]. Thaumarchaeota were initially known as mesophilic Crenarchaeota [5] and most studied members of this phylum are ammonia-oxidizing archaea (AOA) [6, 7]. Studies of the piezotolerant and abundant ammonia oxidizers could significantly advance our understanding of global nitrogen and carbon cycles. 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. Little is known about the metabolism and distribution of these ammonia oxidizers in the hadal water

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