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      Ubiquity and Diversity of Complete Ammonia Oxidizers (Comammox)

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      Applied and Environmental Microbiology
      American Society for Microbiology

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          ABSTRACT

          The discovery of complete ammonia oxidizers (comammox) refutes the century-old paradigm that nitrification requires the activity of two types of microbes. Determining the distribution and abundance of comammox in various environments is important for revealing the ecology of microbial nitrification within the global nitrogen cycle. In this study, the ubiquity and diversity of comammox were analyzed for samples from different types of environments, including soil, sediment, sludge, and water. The results of a two-step PCR using highly degenerate primers (THDP-PCR) and quantitative real-time PCR (qPCR) supported the relatively high abundance of comammox in nearly half of all samples tested, sometimes even outnumbering canonical ammonia-oxidizing bacteria (AOB). In addition, a relatively high proportion of comammox in tap and coastal water samples was confirmed via analysis of metagenomic data sets in public databases. The diversity of comammox was estimated by comammox-specific partial nested PCR amplification of the ammonia monooxygenase subunit A ( amoA) gene, and phylogenetic analysis of comammox AmoA clearly showed a split of clade A into clades A.1 and A.2, with the proportions of clades A.1, A.2, and B differing among the various environmental samples. Moreover, compared to the amoA genes of AOB and ammonia-oxidizing archaea (AOA), the comammox amoA gene exhibited higher diversity indices. The ubiquitous distribution and high diversity of comammox indicate that they are likely overlooked contributors to nitrification in various ecosystems.

          IMPORTANCE The discovery of complete ammonia oxidizers (comammox), which oxidize ammonia to nitrate via nitrite, refutes the century-old paradigm that nitrification requires the activity of two types of microbes and redefines a key process in the biogeochemical nitrogen cycle. Understanding the functional relationships between comammox and other nitrifiers is important for ecological studies on the nitrogen cycle. Therefore, the diversity and contribution of comammox should be considered during ecological analyses of nitrifying microorganisms. In this study, a ubiquitous and highly diverse distribution of comammox was observed in various environmental samples, similar to the distribution of canonical ammonia-oxidizing bacteria. The proportion of comammox was relatively high in coastal water and sediment samples, whereas it was nearly undetectable in open-ocean samples. The ubiquitous distribution and high diversity of comammox indicate that these microorganisms might be important contributors to nitrification.

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          An Earth-system perspective of the global nitrogen cycle.

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

            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.
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              Is Open Access

              FunGene: the functional gene pipeline and repository

              Ribosomal RNA genes have become the standard molecular markers for microbial community analysis for good reasons, including universal occurrence in cellular organisms, availability of large databases, and ease of rRNA gene region amplification and analysis. As markers, however, rRNA genes have some significant limitations. The rRNA genes are often present in multiple copies, unlike most protein-coding genes. The slow rate of change in rRNA genes means that multiple species sometimes share identical 16S rRNA gene sequences, while many more species share identical sequences in the short 16S rRNA regions commonly analyzed. In addition, the genes involved in many important processes are not distributed in a phylogenetically coherent manner, potentially due to gene loss or horizontal gene transfer. While rRNA genes remain the most commonly used markers, key genes in ecologically important pathways, e.g., those involved in carbon and nitrogen cycling, can provide important insights into community composition and function not obtainable through rRNA analysis. However, working with ecofunctional gene data requires some tools beyond those required for rRNA analysis. To address this, our Functional Gene Pipeline and Repository (FunGene; http://fungene.cme.msu.edu/) offers databases of many common ecofunctional genes and proteins, as well as integrated tools that allow researchers to browse these collections and choose subsets for further analysis, build phylogenetic trees, test primers and probes for coverage, and download aligned sequences. Additional FunGene tools are specialized to process coding gene amplicon data. For example, FrameBot produces frameshift-corrected protein and DNA sequences from raw reads while finding the most closely related protein reference sequence. These tools can help provide better insight into microbial communities by directly studying key genes involved in important ecological processes.
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                Author and article information

                Journal
                Applied and Environmental Microbiology
                Appl Environ Microbiol
                American Society for Microbiology
                0099-2240
                1098-5336
                December 15 2018
                November 30 2018
                October 12 2018
                : 84
                : 24
                Article
                10.1128/AEM.01390-18
                6275355
                30315079
                4cad8bd8-882a-4770-981f-999db6964f35
                © 2018
                History

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