Despite the high abundance of Archaea in the global ocean, their metabolism and biogeochemical roles remain largely unresolved. We investigated the population dynamics and metabolic activity of Thaumarchaeota in polar environments, where these microorganisms are particularly abundant and exhibit seasonal growth. Thaumarchaeota were more abundant in deep Arctic and Antarctic waters and grew throughout the winter at surface and deeper Arctic halocline waters. However, in situ single-cell activity measurements revealed a low activity of this group in the uptake of both leucine and bicarbonate (<5% Thaumarchaeota cells active), which is inconsistent with known heterotrophic and autotrophic thaumarchaeal lifestyles. These results suggested the existence of alternative sources of carbon and energy. Our analysis of an environmental metagenome from the Arctic winter revealed that Thaumarchaeota had pathways for ammonia oxidation and, unexpectedly, an abundance of genes involved in urea transport and degradation. Quantitative PCR analysis confirmed that most polar Thaumarchaeota had the potential to oxidize ammonia, and a large fraction of them had urease genes, enabling the use of urea to fuel nitrification. Thaumarchaeota from Arctic deep waters had a higher abundance of urease genes than those near the surface suggesting genetic differences between closely related archaeal populations. In situ measurements of urea uptake and concentration in Arctic waters showed that small-sized prokaryotes incorporated the carbon from urea, and the availability of urea was often higher than that of ammonium. Therefore, the degradation of urea may be a relevant pathway for Thaumarchaeota and other microorganisms exposed to the low-energy conditions of dark polar waters.amoA | ureC | Beaufort Sea | Ross Sea | Amundsen Sea
Cyanobacteria are thought to be the main N2-fixing organisms (diazotrophs) in marine pelagic waters, but recent molecular analyses indicate that non-cyanobacterial diazotrophs are also present and active. Existing data are, however, restricted geographically and by limited sequencing depths. Our analysis of 79,090 nitrogenase (nifH) PCR amplicons encoding 7,468 unique proteins from surface samples (ten DNA samples and two RNA samples) collected at ten marine locations world-wide provides the first in-depth survey of a functional bacterial gene and yield insights into the composition and diversity of the nifH gene pool in marine waters. Great divergence in nifH composition was observed between sites. Cyanobacteria-like genes were most frequent among amplicons from the warmest waters, but overall the data set was dominated by nifH sequences most closely related to non-cyanobacteria. Clusters related to Alpha-, Beta-, Gamma-, and Delta-Proteobacteria were most common and showed distinct geographic distributions. Sequences related to anaerobic bacteria (nifH Cluster III) were generally rare, but preponderant in cold waters, especially in the Arctic. Although the two transcript samples were dominated by unicellular cyanobacteria, 42% of the identified non-cyanobacterial nifH clusters from the corresponding DNA samples were also detected in cDNA. The study indicates that non-cyanobacteria account for a substantial part of the nifH gene pool in marine surface waters and that these genes are at least occasionally expressed. The contribution of non-cyanobacterial diazotrophs to the global N2 fixation budget cannot be inferred from sequence data alone, but the prevalence of non-cyanobacterial nifH genes and transcripts suggest that these bacteria are ecologically significant.
Marine waters are generally considered to be nitrogen (N) limited and are therefore favourable environments for diazotrophs, i.e. organisms converting atmospheric N 2 into ammonium or nitrogen oxides available for growth. In some regions, this import of N supports up to half of the primary productivity. Diazotrophic Cyanobacteria appear to be the major contributors to marine N 2 fixation in surface waters, whereas the contribution of heterotrophic or chemoautotrophic diazotrophs to this process is usually regarded inconsequential. Culture-independent studies reveal that non-cyanobacterial diazotrophs are diverse, widely distributed, and actively expressing the nitrogenase gene in marine and estuarine environments. The detection of nifH genes and nifH transcripts, even in N-replete marine waters, suggests that N 2 fixation is an ecologically important process throughout the oceans. Because this process is highly sensitive to and inhibited by molecular oxygen (O 2 ), diazotrophy requires efficient scavenging of intracellular O 2 or growth in environments with low ambient O 2 concentration. Particles with interior low-O 2 micro-zones and oceanic oxygen minimum zones are just 2 potential habitats suitable for N 2 fixation by non-cyanobacterial diazotrophs. Our ignorance about the regulation of N 2 fixation by non-Cyanobacteria in their natural marine environments currently prevents an evaluation of their importance in marine N cycling and budgets. A review of the molecular data on distribution and expression of nifH genes in non-Cyanobacteria suggests that further study of the role of these Bacteria in N cycling at local, regional and global scales is needed.KEY WORDS: N 2 fixation · Nitrogen fixation · Non-Cyanobacteria · nifH · Nitrogenase Resale or republication not permitted without written consent of the publisher Contribution to AME Special 4 'Progress and perspectives in aquatic microbial ecology'OPEN PEN ACCESS CCESS
1 1 2 3 4 5 6 7 8 A recently described symbiosis between the metabolically streamlined nitrogen-fixing cyanobacterium UCYN-A and a single-celled eukaryote prymnesiophyte alga is widely distributed throughout tropical and subtropical marine waters, and is thought to contribute significantly to nitrogen fixation in these regions. Several UCYN-A sublineages have been defined based on UCYN-A nitrogenase (nifH) sequences. Due to the low abundances of UCYN-A in the global oceans, currently existing molecular techniques are limited for detecting and quantifying these organisms. A targeted approach is needed to adequately characterize the diversity of this important marine cyanobacterium, and to advance understanding of its ecological importance. We present findings on the distribution of UCYN-A sublineages based on high throughput sequencing of UCYN-A nifH PCR amplicons from 78 samples distributed throughout many major oceanic provinces. These UCYN-A nifH fragments were used to define oligotypes, alternative taxonomic units defined by nucleotide positions with high variability. The dataset was dominated by a single oligotype associated with the UCYN-A1 sublineage, consistent with previous observations of relatively high abundances in tropical and subtropical regions. However, this analysis also revealed for the first time the widespread distribution of the UCYN-A3 sublineage in oligotrophic waters. Furthermore, distinct assemblages of UCYN-A oligotypes were found in oligotrophic and coastally-influenced waters. This unique dataset provides a framework for determining the environmental controls on UCYN-A distributions and the ecological importance of the different sublineages.
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