Genomes of two new ammonia-oxidizing archaea enriched from deep marine sediments.

Soo-Je Park,Francisco Rodríguez-Valera,Won-Hyong Chung,Jung-Hyun Lee,Kaekyoung Kwon,Rohit Ghai,Sung-Keun Rhee,Ana-Belén Martín-Cuadrado,Eugene L Madsen,Celine Brochier-Armanet

doi:10.1371/journal.pone.0096449

Abstract

Ammonia-oxidizing archaea (AOA) are ubiquitous and abundant and contribute significantly to the carbon and nitrogen cycles in the ocean. In this study, we assembled AOA draft genomes from two deep marine sediments from Donghae, South Korea, and Svalbard, Arctic region, by sequencing the enriched metagenomes. Three major microorganism clusters belonging to Thaumarchaeota, Epsilonproteobacteria, and Gammaproteobacteria were deduced from their 16S rRNA genes, GC contents, and oligonucleotide frequencies. Three archaeal genomes were identified, two of which were distinct and were designated Ca. “Nitrosopumilus koreensis” AR1 and “Nitrosopumilus sediminis” AR2. AR1 and AR2 exhibited average nucleotide identities of 85.2% and 79.5% to N. maritimus, respectively. The AR1 and AR2 genomes contained genes pertaining to energy metabolism and carbon fixation as conserved in other AOA, but, conversely, had fewer heme-containing proteins and more copper-containing proteins than other AOA. Most of the distinctive AR1 and AR2 genes were located in genomic islands (GIs) that were not present in other AOA genomes or in a reference water-column metagenome from the Sargasso Sea. A putative gene cluster involved in urea utilization was found in the AR2 genome, but not the AR1 genome, suggesting niche specialization in marine AOA. Co-cultured bacterial genome analysis suggested that bacterial sulfur and nitrogen metabolism could be involved in interactions with AOA. Our results provide fundamental information concerning the metabolic potential of deep marine sedimentary AOA.

Highlights

Aerobic nitrification is a key process in the nitrogen cycle that converts ammonia to nitrate via nitrite and is catalyzed by aerobic autotrophic ammonia-oxidizing and nitrite-oxidizing microorganisms
Single reads of 16S rRNA genes recovered from the metagenome dataset (n = 1,100 in AR and n = 908 in SJ cultures) were used to analyze the compositions of the microbial communities that were enriched in the two cultures (Figure S2)
The most frequently recovered 16S rRNA gene sequences were affiliated to Epsilonproteobacteria (60–62%), Thaumarchaeota (13–17%), and Gammaproteobacteria (10–18%), with the proportions of these three taxa being similar in the two cultures (Figure S2)

Summary

Introduction

Aerobic nitrification is a key process in the nitrogen cycle that converts ammonia to nitrate via nitrite and is catalyzed by aerobic autotrophic ammonia-oxidizing and nitrite-oxidizing microorganisms. Critical evidence for the existence of autotrophic ammoniaoxidizing archaea (AOA) was obtained through characterization of the first ammonia-oxidizing archaeon, Nitrosopumilus maritimus SCM1, which was isolated from a marine aquarium [4]. This discovery was followed by the successful cultivation of diverse AOA of Thaumarchaeota [5,6] from marine (group I.1a) [4,7,8] and soil (group I.1a and I.1b) [9,10,11] environments. Investigations into the metabolic properties and nitrification potential of sedimentary AOA are necessary to understand the nitrogen cycle in marine environments

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