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Hollibaugh, J. T.

Publications and source records attributed to Hollibaugh, J. T..

3 recordsLinked to original sources

Contribution of Urea to Nitrite Production in Southern Ocean Waters with Contrasting Nitrifying Communities

We compared the contribution of ammonia and urea to nitrite production in >100 samples of Southern Ocean waters with abundant and diverse ammonia-oxidizing archaeal (AOA) communities. Ammonia (AO) and urea (UO) oxidation rates were distributed uniformly within a water mass across coastal and slope waters west of the Antarctic Peninsula; however, rates and AOA community composition displayed strong vertical gradients. Rates in most samples from Antarctic surface and slope water were at or below the limit of detection. Highest mean rates of both processes were in the Winter Water (WW, epipelagic, 21.2 and 1.6 nmol N L-1 d-1), and the Circumpolar Deep Water (CDW, mesopelagic, 7.9 and 2.5 nmol N L-1 d-1), for AO and UO, respectively. However, we also found that the response of AO and UO to substrate amendments varied by water mass. AO rates in WW samples increased by [~]200% with 44 vs 6 nM amendments, but decreased (down to 7%) in CDW samples. UO rates responded similarly, but to a lesser degree. This response suggests that even low NH4+ amendments may inhibit AO by mesopelagic Thaumarchaeota populations. AO and UO rates were not correlated, nor were they correlated with the abundance or ratios of abundance of marker genes, or with the concentrations of ammonium or urea. Our data suggest that while ammonium is the primary substrate, urea-N is responsible for a significant fraction ([~]25% of that from AO alone) of nitrite production in the Southern Ocean, comparable to its contribution at lower latitudes. IMPORTANCESouthern Ocean nitrification fuels denitrification in oxygen depleted zones at higher latitudes, one of the controls of N:P ratios in the global ocean. N2O, a powerful greenhouse gas, is by-product of nitrification. We contrast the contributions of ammonium and urea-N to nitrification in the Southern Ocean. Our work constrains rates and demonstrates that the contribution of urea-N to nitrite production in polar waters is comparable to that in temperate oceans. Correlations between activity and the abundance or ratios of Thaumarchaeota marker genes were weak, questioning their use as indicators of activity. We document differential responses of activity to substrate amendments by water mass: enhanced in epipelagic but inhibited in mesopelagic samples. We interpret this difference in the context of community composition and the production of reactive oxygen species. Our insights into environmental controls of nitrification are relevant to microbial ecologists studying Thaumarchaeota and to modeling the global nitrogen cycle.

microbiology↗

Limited accessibility of nitrogen supplied as amino acids, amides, and amines as energy sources for marine Thaumarchaeota

Genomic and physiological evidence from some strains of ammonia-oxidizing Thaumarchaeota demonstrate their additional ability to oxidize nitrogen (N) supplied as urea or cyanate, fueling conjecture about their ability to conserve energy by directly oxidizing reduced N from other dissolved organic nitrogen (DON) compounds. Similarly, field studies have shown rapid oxidation of polyamine-N in the ocean, but it is unclear whether Thaumarchaeota oxidize polyamine-N directly or whether heterotrophic DON remineralization is required. We tested growth of two marine Nitrosopumilus isolates on DON compounds including polyamines, amino acids, primary amines, and amides as their sole energy source. Though axenic cultures only consumed N supplied as ammonium or urea, there was rapid but inconsistent oxidation of N from the polyamine putrescine when cultures included a heterotrophic bacterium. Surprisingly, axenic cultures oxidized 15N-putrescine during growth on ammonia, suggesting co-metabolism or accelerated breakdown of putrescine by reactive metabolic byproducts. Nitric oxide, hydrogen peroxide, or peroxynitrite did not oxidize putrescine in sterile seawater. These data suggest that the N in common DON molecules is not directly accessible to marine Thaumarchaeota, with thaumarchaeal oxidation (and presumably assimilation) of DON-N requiring initial heterotrophic remineralization. However, reactive byproducts or enzymatic co-metabolism may facilitate limited thaumarchaeal DON-N oxidation.

microbiology↗

Transcriptional activity differentiates families of Marine Group II Euryarchaeota in the coastal ocean

Marine Group II Euryarchaeota (Candidatus Poseidoniales), abundant but yet-uncultivated members of marine microbial communities, are thought to be (photo)heterotrophs that metabolize dissolved organic matter (DOM) such as lipids and peptides. However, little is known about their transcriptional activity. We mapped reads from a metatranscriptomic time series collected at Sapelo Island (GA, USA) to metagenome-assembled genomes to determine the diversity of transcriptionally-active Ca. Poseidoniales. Summer metatranscriptomes had the highest abundance of Ca. Poseidoniales transcripts, mostly from the O1 and O3 genera within Ca. Thalassarchaeaceae (MGIIb). In contrast, transcripts from fall and winter samples were predominantly from Ca. Poseidoniaceae (MGIIa). Genes encoding proteorhodopsin, membrane-bound pyrophosphatase, peptidase/proteases, and part of the {beta}-oxidation pathway were highly transcribed across abundant genera. Highly transcribed genes specific to Ca. Thalassarchaeaceae included xanthine/uracil permease and receptors for amino acid transporters. Enrichment of Ca. Thalassarchaeaceae transcript reads related to protein/peptide, nucleic acid, and amino acid transport and metabolism, as well as transcript depletion during dark incubations, provided further evidence of heterotrophic metabolism. Quantitative PCR analysis of South Atlantic Bight samples indicated consistently abundant Ca. Poseidoniales in nearshore and inshore waters. Together, our data suggest Ca. Thalassarchaeaceae are important photoheterotrophs potentially linking DOM and nitrogen cycling in coastal waters.

microbiology↗