Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean

Abstract

Nitrification, the microbial oxidation of ammonia to nitrite and nitrate, occurs in a wide variety of environments and plays a central role in the global nitrogen cycle. Catalyzed by the enzyme ammonia monooxygenase, the ability to oxidize ammonia was previously thought to be restricted to a few groups within the beta- and gamma-Proteobacteria. However, recent metagenomic studies have revealed the existence of unique ammonia monooxygenase alpha-subunit (amoA) genes derived from uncultivated, nonextremophilic Crenarchaeota. Here, we report molecular evidence for the widespread presence of ammonia-oxidizing archaea (AOA) in marine water columns and sediments. Using PCR primers designed to specifically target archaeal amoA, we find AOA to be pervasive in areas of the ocean that are critical for the global nitrogen cycle, including the base of the euphotic zone, suboxic water columns, and estuarine and coastal sediments. Diverse and distinct AOA communities are associated with each of these habitats, with little overlap between water columns and sediments. Within marine sediments, most AOA sequences are unique to individual sampling locations, whereas a small number of sequences are evidently cosmopolitan in distribution. Considering the abundance of nonextremophilic archaea in the ocean, our results suggest that AOA may play a significant, but previously unrecognized, role in the global nitrogen cycle.

Fig. 1.

Phylogenetic relationships among archaeal amoA sequences from water columns, sediments, and soil. Sequences are color-coded according to location; symbols are used to distinguish different sites or depths within a given location. One representative of sequence groups ≥99% identical is shown; additional symbols show the total number of clones represented by a sequence. Database sequences are shown in black. Bootstrap values (>50%) are indicated at branch points. Brackets highlight phylogenetic clusters referred to in the text. HI, Hummingbird Island; HL, Hudson's Landing; VM, Vierra Marsh.

Fig. 2.

Rarefaction curves indicating archaeal amoA richness within clone libraries derived from water columns (A) and sediments and soil (B). OTUs were defined as groups of sequences differing by ≤2% at the DNA level. Curves are color-coded as in Fig. 1. HI, Hummingbird Island; HL, Hudson's Landing; VM, Vierra Marsh.