Cultivation of Autotrophic Ammonia-Oxidizing Archaea from Marine Sediments in Coculture with Sulfur-Oxidizing Bacteria
Open Access
- 15 November 2010
- journal article
- Published by American Society for Microbiology in Applied and Environmental Microbiology
- Vol. 76 (22), 7575-7587
- https://doi.org/10.1128/aem.01478-10
Abstract
The role of ammonia-oxidizing archaea (AOA) in nitrogen cycling in marine sediments remains poorly characterized. In this study, we enriched and characterized AOA from marine sediments. Group I.1a crenarchaea closely related to those identified in marine sediments and “ Candidatus Nitrosopumilus maritimus” (99.1 and 94.9% 16S rRNA and amoA gene sequence identities to the latter, respectively) were substantially enriched by coculture with sulfur-oxidizing bacteria (SOB). The selective enrichment of AOA over ammonia-oxidizing bacteria (AOB) is likely due to the reduced oxygen levels caused by the rapid initial growth of SOB. After biweekly transfers for ca. 20 months, archaeal cells became the dominant prokaryotes (>80%), based on quantitative PCR and fluorescence in situ hybridization analysis. The increase of archaeal 16S rRNA gene copy numbers was coincident with the amount of ammonia oxidized, and expression of the archaeal amoA gene was observed during ammonia oxidation. Bacterial amoA genes were not detected in the enrichment culture. The affinities of these AOA to oxygen and ammonia were substantially higher than those of AOB. [ 13 C]bicarbonate incorporation and the presence and activation of genes of the 3-hydroxypropionate/4-hydroxybutyrate cycle indicated autotrophy during ammonia oxidation. In the enrichment culture, ammonium was oxidized to nitrite by the AOA and subsequently to nitrate by Nitrospina -like bacteria. Our experiments suggest that AOA may be important nitrifiers in low-oxygen environments, such as oxygen-minimum zones and marine sediments.Keywords
This publication has 87 references indexed in Scilit:
- Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaeaProceedings of the National Academy of Sciences of the United States of America, 2010
- Comparative Metagenomic Analysis of a Microbial Community Residing at a Depth of 4,000 Meters at Station ALOHA in the North Pacific Subtropical GyreApplied and Environmental Microbiology, 2009
- Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environmentProceedings of the National Academy of Sciences of the United States of America, 2008
- A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot springProceedings of the National Academy of Sciences of the United States of America, 2008
- A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and EucaryaBiology Direct, 2008
- Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L'Atalante, Eastern Mediterranean SeaThe ISME Journal, 2007
- Linking crenarchaeal and bacterial nitrification to anammox in the Black SeaProceedings of the National Academy of Sciences of the United States of America, 2007
- Diversity of Ammonia-Oxidizing Archaea and Bacteria in the Sediments of a Hypernutrified Subtropical Estuary: Bahía del Tóbari, MexicoApplied and Environmental Microbiology, 2006
- Archaeal nitrification in the oceanProceedings of the National Academy of Sciences of the United States of America, 2006
- Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbonProceedings of the National Academy of Sciences of the United States of America, 2006