An official website of the United States government
Abstract Urea is hypothesized to be an important source of nitrogen and chemical energy to microorganisms in the deep sea; however, direct evidence for urea use below the epipelagic ocean is lacking. Here, we explore urea utilization from 50 to 4000 meters depth in the northeastern Pacific Ocean using metagenomics, nitrification rates, and single-cell stable-isotope-uptake measurements with nanoscale secondary ion mass spectrometry. We find that on average 25% of deep-sea cells assimilated urea-derived N (60% of detectably active cells), and that cell-specific nitrogen-incorporation rates from urea were higher than that from ammonium. Both urea concentrations and assimilation rates relative to ammonium generally increased below the euphotic zone. We detected ammonia- and urea-based nitrification at all depths at one of two sites analyzed, demonstrating their potential to support chemoautotrophy in the mesopelagic and bathypelagic regions. Using newly generated metagenomes we find that the ureC gene, encoding the catalytic subunit of urease, is found within 39% of deep-sea cells in this region, including the Nitrososphaeria (syn., Thaumarchaeota; likely for nitrification) as well as members of thirteen other phyla such as Proteobacteria, Verrucomicrobia, Plantomycetota, Nitrospinota, and Chloroflexota (likely for assimilation). Analysis of public metagenomes estimated ureC within 10–46% of deep-sea cells around the world, with higher prevalence below the photic zone, suggesting urea is widely available to the deep-sea microbiome globally. Our results demonstrate that urea is a nitrogen source to abundant and diverse microorganisms in the dark ocean, as well as a significant contributor to deep-sea nitrification and therefore fuel for chemoautotrophy.
more »
« less
Substrate pulses as a selection factor for clades of marine Thaumarchaeota
ABSTRACT: Nitrification is a globally important biogeochemical process, helping to remove excess nitrogen from the biosphere. Thaumarchaeota are important contributors to ammonium oxidation, the first step in nitrification, especially in the ocean. A phylogenetic distinction between clades of marine Thaumarchaeota from shallow versus mesopelagic habitats emerged from the earliest analyses of sequence databases, yet the environmental factors driving these distributions, and their biogeochemical significance, are still debated. Steady-state ammonium concentrations are important determinants; however, environmental concentrations may fluctuate on short time scales, depending on localized coupling between production and consumption. Substrate pulses have been shown to inhibit the activity of Thaumarchaeota cultures via the accumulation of toxic intermediates. Evidence from experiments performed with samples from the Southern Ocean off the West Antarctic Peninsula show that ammonia oxidation can be strongly inhibited by ammonium amendments. We found greater inhibition with mesopelagic samples than with those from shallower water. Pulses of urea also inhibited the oxidation of urea-N, but to a lesser extent than ammonium pulses affected ammonia oxidation. The inhibition also affects carbon fixation, which may thus be greater in the dark ocean than currently believed. The differential response of meso- versus epipelagic Thaumarchaeota populations to pulses of ammonium potentially explains the evolutionary divergence of marine Thaumarchaeota into deep- and shallow-water clades. Measurements of ammonium oxidation rates needed for biogeochemical models are typically made with substrate amendments that may yield artificially low rates, to 25% of the uninhibited rate, in mesopelagic samples.
more »
« less
- Award ID(s):
- 1643466
- PAR ID:
- 10468103
- Publisher / Repository:
- American Geophysical Union
- Date Published:
- Subject(s) / Keyword(s):
- Thaumarchaeota nitrification ammonia-oxidation reactive-oxygen reactive-nitrogen Southern-Ocean Antarctica
- Format(s):
- Medium: X
- Location:
- AGU Meeting, San Francisco CA, 10-14 December 2023
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract. As a key biogeochemical pathway in the marine nitrogen cycle, nitrification (ammonia oxidation and nitrite oxidation) converts the most reduced form of nitrogen – ammonium–ammonia (NH4+–NH3) – into the oxidized species nitrite (NO2-) and nitrate (NO3-). In the ocean, these processes are mainly performed by ammonia-oxidizing archaea (AOA) and bacteria (AOB) and nitrite-oxidizing bacteria (NOB). By transforming nitrogen speciation and providing substrates for nitrogen removal, nitrification affects microbial community structure; marine productivity (including chemoautotrophic carbon fixation); and the production of a powerful greenhouse gas, nitrous oxide (N2O). Nitrification is hypothesized to be regulated by temperature, oxygen, light, substrate concentration, substrate flux, pH and other environmental factors. Although the number of field observations from various oceanic regions has increased considerably over the last few decades, a global synthesis is lacking, and understanding how environmental factors control nitrification remains elusive. Therefore, we have compiled a database of nitrification rates and nitrifier abundance in the global ocean from published literature and unpublished datasets. This database includes 2393 and 1006 measurements of ammonia oxidation and nitrite oxidation rates and 2242 and 631 quantifications of ammonia oxidizers and nitrite oxidizers, respectively. This community effort confirms and enhances our understanding of the spatial distribution of nitrification and nitrifiers and their corresponding drivers such as the important role of substrate concentration in controlling nitrification rates and nitrifier abundance. Some conundrums are also revealed, including the inconsistent observations of light limitation and high rates of nitrite oxidation reported from anoxic waters. This database can be used to constrain the distribution of marine nitrification, to evaluate and improve biogeochemical models of nitrification, and to quantify the impact of nitrification on ecosystem functions like marine productivity and N2O production. This database additionally sets a baseline for comparison with future observations and guides future exploration (e.g., measurements in the poorly sampled regions such as the Indian Ocean and method comparison and/or standardization). The database is publicly available at the Zenodo repository: https://doi.org/10.5281/zenodo.8355912 (Tang et al., 2023).more » « less
-
NOTE: THIS MS IS TO BE SUBMITTED FOLLOWING OUTCOME OF NATURE COMMUNICATIONS REVIEW OF A COMPANION MS. ABSTRACT (246 words, 1,457 characters including spaces) We measured the oxidation rates of N supplied as urea (UO) and ammonium (AO) in continental shelf and slope waters of the Southern Ocean west of the Antarctic Peninsula during the austral summer of 2018. The response of rates to substrate concentration varied by water mass. Rates increased moderately (up to 200%) with 440 vs 6 nM substrate amendments to samples from the Winter Water (WW, sampled at 35-100 m), but decreased (down to 7%) in samples from the Circumpolar Deep Water (CDW, 175-1000 m). AO rates decreased more than UO rates. This response suggests that CDW Thaumarchaeota are not well adapted to short-term variation in substrate concentrations and that even low amendments (we used 44 or 47 nM) may inhibit oxidation. Rates of AO and UO were not correlated; nor were they correlated with the abundance, or ratios of abundance, of marker genes; or with [NH4+]; or [urea]. UO and AO were distributed uniformly across the study area within a water mass; however, they displayed strong vertical gradients. Rates in most samples from Antarctic Surface Water (ASW, 10-15 m) were below the limit of detection. Highest rates of both processes were in samples from the WW (21.2 and 1.6 nmol L-1 d-1 for AO vs UO, respectively) and CDW (7.9 and 2.5 nmol L-1 d-1), comparable to rates from the study area reported previously. The contribution of UO to nitrite production was ~24% of that from AO alone, comparable to ratios measured at lower latitudes.more » « less
-
ABSTRACT The Thaumarchaeota is a diverse archaeal phylum comprising numerous lineages that play key roles in global biogeochemical cycling, particularly in the ocean. To date, all genomically characterized marine thaumarchaea are reported to be chemolithoautotrophic ammonia oxidizers. In this study, we report a group of putatively heterotrophic marine thaumarchaea (HMT) with small genome sizes that is globally abundant in the mesopelagic, apparently lacking the ability to oxidize ammonia. We assembled five HMT genomes from metagenomic data and show that they form a deeply branching sister lineage to the ammonia-oxidizing archaea (AOA). We identify this group in metagenomes from mesopelagic waters in all major ocean basins, with abundances reaching up to 6% of that of AOA. Surprisingly, we predict the HMT have small genomes of ∼1 Mbp, and our ancestral state reconstruction indicates this lineage has undergone substantial genome reduction compared to other related archaea. The genomic repertoire of HMT indicates a versatile metabolism for aerobic chemoorganoheterotrophy that includes a divergent form III-a RuBisCO, a 2M respiratory complex I that has been hypothesized to increase energetic efficiency, and a three-subunit heme-copper oxidase complex IV that is absent from AOA. We also identify 21 pyrroloquinoline quinone (PQQ)-dependent dehydrogenases that are predicted to supply reducing equivalents to the electron transport chain and are among the most highly expressed HMT genes, suggesting these enzymes play an important role in the physiology of this group. Our results suggest that heterotrophic members of the Thaumarchaeota are widespread in the ocean and potentially play key roles in global chemical transformations. IMPORTANCE It has been known for many years that marine Thaumarchaeota are abundant constituents of dark ocean microbial communities, where their ability to couple ammonia oxidation and carbon fixation plays a critical role in nutrient dynamics. In this study, we describe an abundant group of putatively heterotrophic marine Thaumarchaeota (HMT) in the ocean with physiology distinct from those of their ammonia-oxidizing relatives. HMT lack the ability to oxidize ammonia and fix carbon via the 3-hydroxypropionate/4-hydroxybutyrate pathway but instead encode a form III-a RuBisCO and diverse PQQ-dependent dehydrogenases that are likely used to conserve energy in the dark ocean. Our work expands the scope of known diversity of Thaumarchaeota in the ocean and provides important insight into a widespread marine lineage.more » « less
-
Weinert, Emily (Ed.)ABSTRACT When the oligotrophic microbial community was amended with Synechococcus -derived dissolved organic matter (SDOM) and incubated under the dark condition, archaea relative abundance was initially very low but made up more than 60% of the prokaryotic community on day 60, and remained dominant for at least 9 months. The archaeal sequences were dominated by Candidatus Nitrosopumilus , the Group I.1a Thaumarchaeota. The increase of Thaumarchaeota in the dark incubation corresponded to the period of delayed ammonium oxidation upon an initially steady increase in ammonia, supporting the remarkable competency of Thaumarchaeota in energy utilization and fixation of inorganic carbon in the ocean. IMPORTANCE Thaumarchaeota, which are ammonia-oxidizing archaea (AOA), are mainly chemolithoautotrophs that can fix inorganic carbon to produce organic matter in the dark. Their distinctive physiological traits and high abundance in the water column indicate the significant ecological roles they play in the open ocean. In our study, we found predominant Thaumarchaeota in the microbial community amended with cyanobacteria-derived lysate under the dark condition. Furthermore, Thaumarchaeota remained dominant in the microbial community even after 1 year of incubation. Through the ammonification process, dissolved organic matter (DOM) from cyanobacterial lysate was converted to ammonium which was used as an energy source for Thaumarchaeota to fix inorganic carbon into biomass. Our study further advocates the important roles of Thaumarchaeota in the ocean’s biogeochemical cycle.more » « less
