Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea

Abstract

Ammonia-oxidizing archaea (AOA), that is, members of the Thaumarchaeota phylum, occur ubiquitously in the environment and are of major significance for global nitrogen cycling. However, controls on cell growth and organic carbon assimilation by AOA are poorly understood. We isolated an ammonia-oxidizing archaeon (designated strain DDS1) from seawater and used this organism to study the physiology of ammonia oxidation. These findings were confirmed using four additional Thaumarchaeota strains from both marine and terrestrial habitats. Ammonia oxidation by strain DDS1 was enhanced in coculture with other bacteria, as well as in artificial seawater media supplemented with α-keto acids (e.g., pyruvate, oxaloacetate). α-Keto acid-enhanced activity of AOA has previously been interpreted as evidence of mixotrophy. However, assays for heterotrophic growth indicated that incorporation of pyruvate into archaeal membrane lipids was negligible. Lipid carbon atoms were, instead, derived from dissolved inorganic carbon, indicating strict autotrophic growth. α-Keto acids spontaneously detoxify H 2 O 2 via a nonenzymatic decarboxylation reaction, suggesting a role of α-keto acids as H 2 O 2 scavengers. Indeed, agents that also scavenge H 2 O 2 , such as dimethylthiourea and catalase, replaced the α-keto acid requirement, enhancing growth of strain DDS1. In fact, in the absence of α-keto acids, strain DDS1 and other AOA isolates were shown to endogenously produce H 2 O 2 (up to ∼4.5 μM), which was inhibitory to growth. Genomic analyses indicated catalase genes are largely absent in the AOA. Our results indicate that AOA broadly feature strict autotrophic nutrition and implicate H 2 O 2 as an important factor determining the activity, evolution, and community ecology of AOA ecotypes.

Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers

“…However, despite the large amount of transporters encoded in the genome of N. viennensis (13), we have so far not been able to identify alternate energy or carbon sources in growth experiments. In addition, Kim et al (47) have convincingly shown that the dependency of N. viennensis and other strains on small amounts of organic acids (16,17,48) can be overcome by reducing reactive oxygen species in the medium. Consequently, based on growth experiments and genomic predictions, all AOA currently in pure culture can grow strictly autotrophically.…”

De novo acetate production is coupled to central carbon metabolism in mammals

“…Keto acids have been reported to be chemical scavengers in both bacterial culture and mammalian cells 25,26 . A plausible reaction pathway for the generation of acetate could involve the nucleophilic attack of pyruvate by the reactive oxygen species generated from hydrogen peroxide (H 2 O 2 ) (Fig.…”

Potential correlated environmental factors leading to the niche seg- regation of ammonia-oxidizing archaea and ammonia-oxidizing bac- teria: A review

“…For example, the very little dose of organic matters like 0.20 mg/L of yeast extract or 2 mM acetate inhibited the growth of Nitrosocaldus yellowstonii (De La Torre et al, 2008). Despite facts above, organic matters could sometimes stimulate the growth of AOA (Bayer et al, 2016;Kim et al, 2016;Lehtovirta-Morley et al, 2014;Sauder et al, 2017). The phenomenon that the growth rate of Nitrososphaera viennensis increased significantly and its cell generation got shortened by 11.5 times when 0.10 mM pyruvate was added, was misinterpreted as mixtrophy (Tourna et al, 2011), and was recently explained as a hydrogen peroxide detoxification mechanism .…”

“…As chemolithoautotrophic organisms, some AOA tend to be inhibited by organic matters Kim et al, 2016;Könneke et al, 2005;Lehtovirta-Morley et al, 2014). For example, the very little dose of organic matters like 0.20 mg/L of yeast extract or 2 mM acetate inhibited the growth of Nitrosocaldus yellowstonii (De La Torre et al, 2008).…”

“…This traditional viewpoint was thoroughly challenged and changed on the basis of the discovery of AOA. So far, more than 10 strains of AOA were already isolated, and more than 10 enrichments have been cultivated (Blainey et al, 2011;De La Torre et al, 2008;Elling et al, 2015;Hallam et al, 2006;Hatzenpichler et al, 2008;Jung et al, 2011;Jung et al, 2014;Kim et al, 2012;Kim et al, 2016;Könneke et al, 2005;Lehtovirta-Morley et al, 2011;Lehtovirta-Morley et al, 2016a;Mosier et al, 2012;Qin et al, 2014;Sauder et al, 2017). Yet more than 80% of the AOA were still undiscovered so far (Biller et al, 2012).…”