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Competition between ammonia-oxidizing bacteria and benthic microalgae.

ABSTRACT: The abundance, activity, and diversity of ammonia-oxidizing bacteria (AOB) were studied in prepared microcosms with and without microphytobenthic activity. In the microcosm without alga activity, both AOB abundance, estimated by real-time PCR, and potential nitrification increased during the course of the experiment. AOB present in the oxic zone of these sediments were able to fully exploit their nitrification potential because NH(4)(+) did not limit growth. In contrast, AOB in the alga-colonized sediments reached less than 20% of their potential activity, suggesting starvation of cells. Starvation resulted in a decrease with time in the abundance of AOB as well as in nitrification potential. This decrease was correlated with an increase in alga biomass, suggesting competitive exclusion of AOB by microalgae. Induction of N limitation in the oxic zone of the alga-colonized sediments and O(2) limitation of the majority of AOB in darkness were major mechanisms by which microalgae suppressed the growth and survival of AOB. The competition pressure from the algae seemed to act on the entire population of AOB, as no differences were observed by denaturing gradient gel electrophoresis of amoA fragments during the course of the experiment. Enumeration of bacteria based on 16S rRNA gene copies and d-amino acids suggested that the algae also affected other bacterial groups negatively. Our data indicate that direct competitive interaction takes place between algae and AOB and that benthic algae are superior competitors because they have higher N uptake rates and grow faster than AOB.

SUBMITTER: Risgaard-Petersen N

PROVIDER: S-EPMC520845 | biostudies-literature | 2004 Sep

REPOSITORIES: biostudies-literature

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Competition between ammonia-oxidizing bacteria and benthic microalgae.

Risgaard-Petersen Nils N Nicolaisen Mette H MH Revsbech Niels Peter NP Lomstein Bente Aa BA

Applied and environmental microbiology 20040901 9

The abundance, activity, and diversity of ammonia-oxidizing bacteria (AOB) were studied in prepared microcosms with and without microphytobenthic activity. In the microcosm without alga activity, both AOB abundance, estimated by real-time PCR, and potential nitrification increased during the course of the experiment. AOB present in the oxic zone of these sediments were able to fully exploit their nitrification potential because NH(4)(+) did not limit growth. In contrast, AOB in the alga-colonize ...[more]

PMID: 15345441

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Project description:Aerobic ammonia oxidizers (AOs) are prokaryotic microorganisms that contribute to the global nitrogen cycle by performing the first step of nitrification, the oxidation of ammonium to nitrite and nitrate. While aerobic AOs are found ubiquitously, their distribution is controlled by key environmental conditions such as substrate (ammonium) availability. Ammonia-oxidizing archaea (AOA) and complete ammonia oxidizers (comammox) are generally found in oligotrophic environments with low ammonium availability. However, whether AOA and comammox share these habitats or outcompete each other is not well understood. We assessed the competition for ammonium between an AOA and comammox enriched from the freshwater Lake Burr Oak. The AOA enrichment culture (AOA-BO1) contained Nitrosarchaeum sp. BO1 as the ammonia oxidizer and Nitrospira sp. BO1 as the nitrite oxidizer. The comammox enrichment BO4 (cmx-BO4) contained the comammox strain Nitrospira sp. BO4. The competition experiments were performed either in continuous cultivation with ammonium as a growth-limiting substrate or in batch cultivation with initial ammonium concentrations of 50 and 500 µM. Regardless of the ammonium concentration, Nitrospira sp. BO4 outcompeted Nitrosarchaeum sp. BO1 under all tested conditions. The dominance of Nitrospira sp. BO4 could be explained by the ability of comammox to generate more energy through the complete oxidation of ammonia to nitrate and their more efficient carbon fixation pathway-the reductive tricarboxylic acid cycle. Our results are supported by the higher abundance of comammox compared to AOA in the sediment of Lake Burr Oak.ImportanceNitrification is a key process in the global nitrogen cycle. Aerobic ammonia oxidizers play a central role in the nitrogen cycle by performing the first step of nitrification. Ammonia-oxidizing archaea (AOA) and complete ammonia oxidizers (comammox) are the dominant nitrifiers in environments with low ammonium availability. While AOA have been studied for almost 20 years, comammox were only discovered 8 years ago. Until now, there has been a gap in our understanding of whether AOA and comammox can co-exist or if one strain would be dominant under ammonium-limiting conditions. Here, we present the first study characterizing the competition between freshwater AOA and comammox under varying substrate concentrations. Our results will help in elucidating the niches of two key nitrifiers in freshwater lakes.

Project description:Many but not all ammonia-oxidizing bacteria (AOB) produce urease (urea amidohydrolase, EC 3.5.1.5) and are capable of using urea for chemolithotrophic growth. We sequenced the urease operons from two AOB, the beta-proteobacterium Nitrosospira sp. strain NpAV and the gamma-proteobacterium Nitrosococcus oceani. In both organisms, all seven urease genes were contiguous: the three structural urease genes ureABC were preceded and succeeded by the accessory genes ureD and ureEFG, respectively. Green fluorescent protein reporter gene fusions revealed that the ure genes were under control of a single operon promoter upstream of the ureD gene in Nitrosococcus oceani. Southern analyses revealed two copies of ureC in the Nitrosospira sp. strain NpAV genome, while a single copy of the ure operon was detected in the genome of Nitrosococcus oceani. The ureC gene encodes the alpha subunit protein containing the active site and conserved nickel binding ligands; these conserved regions were suitable primer targets for obtaining further ureC sequences from additional AOB. In order to develop molecular tools for detecting the ureolytic ecotype of AOB, ureC genes were sequenced from several beta-proteobacterial AOB. Pairwise identity values ranged from 80 to 90% for the UreC peptides of AOB within a subdivision. UreC sequences deduced from AOB urease genes and available UreC sequences in the public databases were used to construct alignments and make phylogenetic inferences. The UreC proteins from beta-proteobacterial AOB formed a distinct monophyletic group. Unexpectedly, the peptides from AOB did not group most closely with the UreC proteins from other beta-proteobacteria. Instead, it appears that urease in beta-proteobacterial autotrophic ammonia oxidizers is the product of divergent evolution in the common ancestor of gamma- and beta-proteobacteria that was initiated before their divergence during speciation. Sequence motifs conserved for the proteobacteria and variable regions possibly discriminatory for ureC from beta-proteobacterial AOB were identified for future use in environmental analysis of ureolytic AOB. These gene sequences are the first publicly available for ure genes from autotrophic AOB.

Dataset Information

Competition between ammonia-oxidizing bacteria and benthic microalgae.

Publications

Competition between ammonia-oxidizing bacteria and benthic microalgae.

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