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      Drivers of archaeal ammonia-oxidizing communities in soil

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          Abstract

          Soil ammonia-oxidizing archaea (AOA) are highly abundant and play an important role in the nitrogen cycle. In addition, AOA have a significant impact on soil quality. Nitrite produced by AOA and further oxidized to nitrate can cause nitrogen loss from soils, surface and groundwater contamination, and water eutrophication. The AOA discovered to date are classified in the phylum Thaumarchaeota. Only a few archaeal genomes are available in databases. As a result, AOA genes are not well annotated, and it is difficult to mine and identify archaeal genes within metagenomic libraries. Nevertheless, 16S rRNA and comparative analysis of ammonia monooxygenase sequences show that soils can vary greatly in the relative abundance of AOA. In some soils, AOA can comprise more than 10% of the total prokaryotic community. In other soils, AOA comprise less than 0.5% of the community. Many approaches have been used to measure the abundance and diversity of this group including DGGE, T-RFLP, q-PCR, and DNA sequencing. AOA have been studied across different soil types and various ecosystems from the Antarctic dry valleys to the tropical forests of South America to the soils near Mount Everest. Different studies have identified multiple soil factors that trigger the abundance of AOA. These factors include pH, concentration of available ammonia, organic matter content, moisture content, nitrogen content, clay content, as well as other triggers. Land use management appears to have a major effect on the abundance of AOA in soil, which may be the result of nitrogen fertilizer used in agricultural soils. This review summarizes the published results on this topic and suggests future work that will increase our understanding of how soil management and edaphoclimatic factors influence AOA.

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          Examining the global distribution of dominant archaeal populations in soil.

          Archaea, primarily Crenarchaeota, are common in soil; however, the structure of soil archaeal communities and the factors regulating their diversity and abundance remain poorly understood. Here, we used barcoded pyrosequencing to comprehensively survey archaeal and bacterial communities in 146 soils, representing a multitude of soil and ecosystem types from across the globe. Relative archaeal abundance, the percentage of all 16S rRNA gene sequences recovered that were archaeal, averaged 2% across all soils and ranged from 0% to >10% in individual soils. Soil C:N ratio was the only factor consistently correlated with archaeal relative abundances, being higher in soils with lower C:N ratios. Soil archaea communities were dominated by just two phylotypes from a constrained clade within the Crenarchaeota, which together accounted for >70% of all archaeal sequences obtained in the survey. As one of these phylotypes was closely related to a previously identified putative ammonia oxidizer, we sampled from two long-term nitrogen (N) addition experiments to determine if this taxon responds to experimental manipulations of N availability. Contrary to expectations, the abundance of this dominant taxon, as well as archaea overall, tended to decline with increasing N. This trend was coupled with a concurrent increase in known N-oxidizing bacteria, suggesting competitive interactions between these groups.
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            Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota.

            The archaeal domain is currently divided into two major phyla, the Euryarchaeota and Crenarchaeota. During the past few years, diverse groups of uncultivated mesophilic archaea have been discovered and affiliated with the Crenarchaeota. It was recently recognized that these archaea have a major role in geochemical cycles. Based on the first genome sequence of a crenarchaeote, Cenarchaeum symbiosum, we show that these mesophilic archaea are different from hyperthermophilic Crenarchaeota and branch deeper than was previously assumed. Our results indicate that C. symbiosum and its relatives are not Crenarchaeota, but should be considered as a third archaeal phylum, which we propose to name Thaumarchaeota (from the Greek 'thaumas', meaning wonder).
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              The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria.

              Autotrophic ammonia oxidation occurs in acid soils, even though laboratory cultures of isolated ammonia oxidizing bacteria fail to grow below neutral pH. To investigate whether archaea possessing ammonia monooxygenase genes were responsible for autotrophic nitrification in acid soils, the community structure and phylogeny of ammonia oxidizing bacteria and archaea were determined across a soil pH gradient (4.9-7.5) by amplifying 16S rRNA and amoA genes followed by denaturing gradient gel electrophoresis (DGGE) and sequence analysis. The structure of both communities changed with soil pH, with distinct populations in acid and neutral soils. Phylogenetic reconstructions of crenarchaeal 16S rRNA and amoA genes confirmed selection of distinct lineages within the pH gradient and high similarity in phylogenies indicated a high level of congruence between 16S rRNA and amoA genes. The abundance of archaeal and bacterial amoA gene copies and mRNA transcripts contrasted across the pH gradient. Archaeal amoA gene and transcript abundance decreased with increasing soil pH, while bacterial amoA gene abundance was generally lower and transcripts increased with increasing pH. Short-term activity was investigated by DGGE analysis of gene transcripts in microcosms containing acidic or neutral soil or mixed soil with pH readjusted to that of native soils. Although mixed soil microcosms contained identical archaeal ammonia oxidizer communities, those adapted to acidic or neutral pH ranges showed greater relative activity at their native soil pH. Findings indicate that different bacterial and archaeal ammonia oxidizer phylotypes are selected in soils of different pH and that these differences in community structure and abundances are reflected in different contributions to ammonia oxidizer activity. They also suggest that both groups of ammonia oxidizers have distinct physiological characteristics and ecological niches, with consequences for nitrification in acid soils.
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                Author and article information

                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbio.
                Frontiers in Microbiology
                Frontiers Research Foundation
                1664-302X
                15 June 2012
                2012
                : 3
                : 210
                Affiliations
                [1] 1simpleMicrobiology and Cell Science Department, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL, USA
                [2] 2simpleSoil Science Department, Federal University of Rio Grande do Sul, Porto Alegre, Brazil
                Author notes

                Edited by: Rich Boden, University of Plymouth, USA

                Reviewed by: Jennifer F. Biddle, University of Delaware, USA J. Michael Beman, University of California, Merced, USA Nathan Basiliko, University of Toronto, Canada

                *Correspondence: Eric W. Triplett, Department of Microbiology and Cell Science, Institute of Food and Agricultural Sciences, University of Florida, 1052 Museum Road, Gainesville, FL 32611-0700, USA. e-mail: ewt@ 123456ufl.edu

                This article was submitted to Frontiers in Terrestrial Microbiology, a specialty of Frontiers in Microbiology.

                Article
                10.3389/fmicb.2012.00210
                3375578
                22715335
                3f796efa-e422-40d6-a60d-7e9a5bd23195
                Copyright © Zhalnina, Dörr de Quadros, Camargo and Triplett.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.

                History
                : 15 March 2012
                : 22 May 2012
                Page count
                Figures: 0, Tables: 1, Equations: 0, References: 93, Pages: 9, Words: 0
                Categories
                Microbiology
                Review Article

                Microbiology & Virology
                ammonia monooxygenase,ammonia-oxidizing archaea,soil
                Microbiology & Virology
                ammonia monooxygenase, ammonia-oxidizing archaea, soil

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