The Genome of Nitrospina gracilis Illuminates the Metabolism and Evolution of the Major Marine Nitrite Oxidizer

Lücker, Sebastian; Nowka, Boris; Rattei, Thomas; Spieck, Eva; Daims, Holger

doi:10.3389/fmicb.2013.00027

Cited by 239 publications

(348 citation statements)

References 144 publications

(189 reference statements)

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“…This phylogenetic similarity suggests that our observed kinetic response could be consistent across low oxygen systems. Microaerobic adaptations have been identified in the genome of a marine Nitrospina gracilis strain, including the presence of a putatively high-affinity cbb 3 -type terminal oxidase (51). A K m value of 7 nmol·L −1 O 2 was previously determined for a cbb 3 -type oxidase (52) broadly consistent with the high-affinity component inferred here.…”

Section: Resultssupporting

confidence: 55%

Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters

Bristow

Dalsgaard

Tiano

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

207

209

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A major percentage of fixed nitrogen (N) loss in the oceans occurs within nitrite-rich oxygen minimum zones (OMZs) via denitrification and anammox. It remains unclear to what extent ammonium and nitrite oxidation co-occur, either supplying or competing for substrates involved in nitrogen loss in the OMZ core. Assessment of the oxygen (O 2 ) sensitivity of these processes down to the O 2 concentrations present in the OMZ core (<10 nmol·L −1 ) is therefore essential for understanding and modeling nitrogen loss in OMZs. We determined rates of ammonium and nitrite oxidation in the seasonal OMZ off Concepcion, Chile at manipulated O 2 levels between 5 nmol·L −1 and 20 μmol·L −1 . Rates of both processes were detectable in the low nanomolar range (5-33 nmol·L −1 O 2 ), but demonstrated a strong dependence on O 2 concentrations with apparent half-saturation constants (K m s) of 333 ± 130 nmol·L −1 O 2 for ammonium oxidation and 778 ± 168 nmol·L −1 O 2 for nitrite oxidation assuming one-component Michaelis-Menten kinetics. Nitrite oxidation rates, however, were better described with a two-component Michaelis-Menten model, indicating a high-affinity component with a K m of just a few nanomolar. As the communities of ammonium and nitrite oxidizers were similar to other OMZs, these kinetics should apply across OMZ systems. The high O 2 affinities imply that ammonium and nitrite oxidation can occur within the OMZ core whenever O 2 is supplied, for example, by episodic intrusions. These processes therefore compete with anammox and denitrification for ammonium and nitrite, thereby exerting an important control over nitrogen loss.is a key factor regulating biogeochemical cycling in the marine environment (1). Although the vast majority of the ocean remains well oxygenated, subsurface regions of extreme oxygen depletion can persist along eastern boundaries of the world's ocean basins. These regions are known as oxygen minimum zones (OMZs) and are located within the eastern tropical North and South Pacific, the Arabian Sea, and off the coast of Namibia, where oxygen depletion results from poor ventilation and a high export of organic matter from productive surface waters, generating high rates of subsurface oxygen consumption (2, 3).Oceanic waters characterized by oxygen-deficient conditions (<4.5 μmol·L −1 O 2 ) account for <0.1% of total ocean volume but for >30% of fixed nitrogen (N) loss (3-6) due to the onset of anaerobic processes, including denitrification and anammox (7-10). Both field and modeling observations point to the expansion of low oxygen regions as a result of global warming (11). Thus, to evaluate the biogeochemical impact of these regions, it is imperative to understand fully how oxygen controls the cycling of substrates involved in nitrogen loss pathways.Recent studies have quantified the oxygen sensitivity of anaerobic OMZ nitrogen transformations, finding that denitrification has relatively low oxygen tolerance with a half-inhibition concentration (IC 50 ) of 0.3 μmol·L −1 , compared with higher values for...

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Section: Resultssupporting

confidence: 55%

Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters

Bristow

Dalsgaard

Tiano

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

207

209

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“…Transcripts encoding nitrite oxidoreductase (nxrB) did not show a strong size fraction-specific enrichment, consistent with nxrB gene distributions in metagenomes from the Chilean OMZ (Ganesh et al, 2014). NxrB transcripts affiliated primarily with sequences from the genome of Nitrospina gracilis (Lücker et al, 2013), supporting reports of high Nitrospina activity in the ETNP region . Analysis of only N. gracilis-affiliated transcripts did not reveal any genes that were differentially expressed between FL and PA fractions (P40.05), although low N. gracilis read counts in PA data sets (5% those in FL data sets) likely confounded statistical detection.…”

Section: Size-fractionated Biochemical Rates and Gene Expressionsupporting

confidence: 51%

Size-fraction partitioning of community gene transcription and nitrogen metabolism in a marine oxygen minimum zone

et al. 2015

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The genetic composition of marine microbial communities varies at the microscale between particleassociated (PA; 41.6 μm) and free-living (FL; 0.2-1.6 μm) niches. It remains unclear, however, how metabolic activities differ between PA and FL fractions. We combined rate measurements with metatranscriptomics to quantify PA and FL microbial activity in the oxygen minimum zone (OMZ) of the Eastern Tropical North Pacific, focusing on dissimilatory processes of the nitrogen (N) cycle. Bacterial gene counts were 8-to 15-fold higher in the FL compared with the PA fraction. However, rates of all measured N cycle processes, excluding ammonia oxidation, declined significantly following particle (41.6 μm) removal. Without particles, rates of nitrate reduction to nitrite (1.5-9.4 nM N d − 1 ) fell to zero and N 2 production by denitrification (0.5-1.7 nM N d − 1 ) and anammox (0.3-1.9 nM N d − 1 ) declined by 53-85%. The proportional representation of major microbial taxa and N cycle gene transcripts in metatranscriptomes followed fraction-specific trends. Transcripts encoding nitrate reductase were uniform among PA and FL fractions, whereas anammox-associated transcripts were proportionately enriched up to 15-fold in the FL fraction. In contrast, transcripts encoding enzymes for N 2 O and N 2 production by denitrification were enriched up to 28-fold in PA samples. These patterns suggest that the majority of N cycle activity, excluding N 2 O and N 2 production by denitrification, is confined to a FL majority that is critically dependent on access to particles, likely as a source of organic carbon and inorganic N. Variable particle distributions may drive heterogeneity in N cycle activity and gene expression in OMZs.

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“…Nitrospina spp. are nitrite oxidizers and are proposed to have key roles in nitrogen fixing and cycling within the ascidian tunics Lucker et al, 2013). Another group that was slightly enriched in L. badium samples specifically in PNG_11062 (22%) is the Acidimicrobiales class of actinobacteria, a group that was previously described as a sponge-specific bacterial group (Simister et al, 2012).…”

Section: Bacterial Composition Of Ascidiansmentioning

confidence: 99%

Species specificity of symbiosis and secondary metabolism in ascidians

et al. 2014

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Ascidians contain abundant, diverse secondary metabolites, which are thought to serve a defensive role and which have been applied to drug discovery. It is known that bacteria in symbiosis with ascidians produce several of these metabolites, but very little is known about factors governing these 'chemical symbioses'. To examine this phenomenon across a wide geographical and species scale, we performed bacterial and chemical analyses of 32 different ascidians, mostly from the didemnid family from Florida, Southern California and a broad expanse of the tropical Pacific Ocean. Bacterial diversity analysis showed that ascidian microbiomes are highly diverse, and this diversity does not correlate with geographical location or latitude. Within a subset of species, ascidian microbiomes are also stable over time (R ¼ À 0.037, P-value ¼ 0.499). Ascidian microbiomes and metabolomes contain species-specific and location-specific components. Location-specific bacteria are found in low abundance in the ascidians and mostly represent strains that are widespread. Location-specific metabolites consist largely of lipids, which may reflect differences in water temperature. By contrast, species-specific bacteria are mostly abundant sequenced components of the microbiomes and include secondary metabolite producers as major components. Species-specific chemicals are dominated by secondary metabolites. Together with previous analyses that focused on single ascidian species or symbiont type, these results reveal fundamental properties of secondary metabolic symbiosis. Different ascidian species have established associations with many different bacterial symbionts, including those known to produce toxic chemicals. This implies a strong selection for this property and the independent origin of secondary metabolite-based associations in different ascidian species. The analysis here streamlines the connection of secondary metabolite to producing bacterium, enabling further biological and biotechnological studies.

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The Genome of Nitrospina gracilis Illuminates the Metabolism and Evolution of the Major Marine Nitrite Oxidizer

Cited by 239 publications

References 144 publications

Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters

Ammonium and nitrite oxidation at nanomolar oxygen concentrations in oxygen minimum zone waters

Size-fraction partitioning of community gene transcription and nitrogen metabolism in a marine oxygen minimum zone

Species specificity of symbiosis and secondary metabolism in ascidians

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