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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.
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Urea assimilation and oxidation support activity of phylogenetically diverse microbial communities of the dark ocean
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.
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- Award ID(s):
- 2143035
- PAR ID:
- 10564734
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 18
- Issue:
- 1
- ISSN:
- 1751-7362
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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