Abstract
Thaumarchaeota have been detected in several industrial and municipal wastewater treatment plants (WWTPs), despite the fact that ammonia-oxidizing archaea (AOA) are thought to be adapted to low ammonia environments. However, the activity, physiology and metabolism of WWTP-associated AOA remain poorly understood. We report the cultivation and complete genome sequence of Candidatus Nitrosocosmicus exaquare, a novel AOA representative from a municipal WWTP in Guelph, Ontario (Canada). In enrichment culture, Ca. N. exaquare oxidizes ammonia to nitrite stoichiometrically, is mesophilic, and tolerates at least 15 mm of ammonium chloride or sodium nitrite. Microautoradiography (MAR) for enrichment cultures demonstrates that Ca. N. exaquare assimilates bicarbonate in association with ammonia oxidation. However, despite using inorganic carbon, the ammonia-oxidizing activity of Ca. N. exaquare is greatly stimulated in enrichment culture by the addition of organic compounds, especially malate and succinate. Ca. N. exaquare cells are coccoid with a diameter of ~1–2 μm. Phylogenetically, Ca. N. exaquare belongs to the Nitrososphaera sister cluster within the Group I.1b Thaumarchaeota, a lineage which includes most other reported AOA sequences from municipal and industrial WWTPs. The 2.99 Mbp genome of Ca. N. exaquare encodes pathways for ammonia oxidation, bicarbonate fixation, and urea transport and breakdown. In addition, this genome encodes several key genes for dealing with oxidative stress, including peroxidase and catalase. Incubations of WWTP biofilm demonstrate partial inhibition of ammonia-oxidizing activity by 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl 3-oxide (PTIO), suggesting that Ca. N. exaquare-like AOA may contribute to nitrification in situ. However, CARD-FISH-MAR showed no incorporation of bicarbonate by detected Thaumarchaeaota, suggesting that detected AOA may incorporate non-bicarbonate carbon sources or rely on an alternative and yet unknown metabolism.
Highlights
Nitrification is an important process for municipal and industrial wastewater treatment plants (WWTPs) because it prevents the negative impacts of releasing ammonia to receiving waters, including toxicity to fish, eutrophication and increased oxygen demand
We report the cultivation of a Thaumarchaeota representative originating from a municipal WWTP, which oxidizes ammonia, fixes inorganic carbon, and possesses a genomic repertoire consistent with chemolithoautotrophy
N. exaquare produces nitrite from ammonia at near-stoichiometric values (Figure 1a), and thaumarchaeotal cell numbers follow nitrite production closely, providing evidence that energy for cell growth is derived from the oxidation of ammonia to nitrite
Summary
Nitrification is an important process for municipal and industrial wastewater treatment plants (WWTPs) because it prevents the negative impacts of releasing ammonia to receiving waters, including toxicity to fish, eutrophication and increased oxygen demand. Ca. N. exaquare has several genes related to ammonia oxidation, including amoA, amoB, and three copies of amoC, in an arrangement that differs from both AOB and other AOA representatives (Supplementary Figure S6).
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