Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation

Abstract

Ammonia-oxidizing archaea (AOA) are now implicated in exerting significant control over the form and availability of reactive nitrogen species in marine environments. Detailed studies of specific metabolic traits and physicochemical factors controlling their activities and distribution have not been well constrained in part due to the scarcity of isolated AOA strains. Here, we report the isolation of two new coastal marine AOA, strains PS0 and HCA1. Comparison of the new strains to Nitrosopumilus maritimus strain SCM1, the only marine AOA in pure culture thus far, demonstrated distinct adaptations to pH, salinity, organic carbon, temperature, and light. Strain PS0 sustained nearly 80% of ammonia oxidation activity at a pH as low as 5.9, indicating that coastal strains may be less sensitive to the ongoing reduction in ocean pH. Notably, the two novel isolates are obligate mixotrophs that rely on uptake and assimilation of organic carbon compounds, suggesting a direct coupling between chemolithotrophy and organic matter assimilation in marine food webs. All three isolates showed only minor photoinhibition at 15 μE·m −2 ·s −1 and rapid recovery of ammonia oxidation in the dark, consistent with an AOA contribution to the primary nitrite maximum and the plausibility of a diurnal cycle of archaeal ammonia oxidation activity in the euphotic zone. Together, these findings highlight an unexpected adaptive capacity within closely related marine group I Archaea and provide new understanding of the physiological basis of the remarkable ecological success reflected by their generally high abundance in marine environments.marine ammonia-oxidizing archaea | ecophysiology | urea utilization

Genomic and proteomic characterization of “ Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean

“…N. brevis genome vs. 31 in N. maritimus) and holds even when these estimates are normalized to genome size (14.6 vs. 18.9 ABC transporters per millions of base pairs genome). The identification and expression of two Amt-type ammonium transporters (T478_1378, T478_1350) gives further support for the hypothesis that ammonia-oxidizing archaea actively transport ammonium (NH 4 + ) into the cell (13,20) and is consistent with detection of these genes in environmental metatranscriptomes (8,57).…”

“…For example, putative transport proteins for the import of lipoproteins, glycerol, and glycine betaine were all identified in the genome, with several present in the proteome, suggestive of potential alternative substrate use. Similarly, the persistence of a small percentage (<10% of total cells) of putatively heterotrophic bacterial cells in the enrichment culture and reports of reliance on organic compounds in other marine Thaumarchaeota (13) leave open the potential that Ca. N. brevis may benefit from organic compounds produced by the bacteria or in the natural seawater medium for growth.…”

“…At present there are six pure cultures of Thaumarchaeota: one from a marine aquarium [Nitrosopumilus maritimus SCM1 (11,12)], two from an estuary in the northeast Pacific [PS0 and HCA1 (13)], and three from soil [Nitrosphaera viennensis (14) and Nitrosotalea devanaterra strains Nd1 and Nd2 (15)]. Of these isolates, N. maritimus, N. viennensis, and N. devanaterra are able to grow as chemolithoautotrophic ammonia oxidizers.…”

“…In terms of physiology, N. maritimus grows chemolithoautotrophically, with ammonia as its sole energy source and bicarbonate as its sole carbon source. However, mixotrophy has been proposed for both N. viennensis and the marine isolates PS0 and HCA1 on the basis of growth stimulation when organic acids are added to the media (13,14). In terms of genome content, metagenomic recruitment to N. maritimus is poor relative to that of single-cell genomes obtained from the open ocean (21).…”

Glyphosate Use Predicts Healthcare Utilization for ADHD in the Healthcare Cost and Utilization Project net (HCUPnet): A Two-Way Fixed-Effects Analysis

“…Microbes, including the documented emergence of archaeal strains in 2007, have been shown to be integral decomposers of residual inputs and biosolids in corn agroecosystems [70][71][72]. In this process, these archaeal strains are also known to be potent contributors to soil N 2 O emissions and may be able to contribute even amid the presence of any nitrification inhibition [73], indicating a widespread genomic adaptability distinct from AOB populations, [74][75][76]. It has also been suggested that N 2 O is emitted as a spontaneous metabolic AO intermediate [73].…”