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Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea.

ABSTRACT: The ammonia-oxidizing archaea have recently been recognized as a significant component of many microbial communities in the biosphere. Although the overall stoichiometry of archaeal chemoautotrophic growth via ammonia (NH(3)) oxidation to nitrite (NO(2)(-)) is superficially similar to the ammonia-oxidizing bacteria, genome sequence analyses point to a completely unique biochemistry. The only genomic signature linking the bacterial and archaeal biochemistries of NH(3) oxidation is a highly divergent homolog of the ammonia monooxygenase (AMO). Although the presumptive product of the putative AMO is hydroxylamine (NH(2)OH), the absence of genes encoding a recognizable ammonia-oxidizing bacteria-like hydroxylamine oxidoreductase complex necessitates either a novel enzyme for the oxidation of NH(2)OH or an initial oxidation product other than NH(2)OH. We now show through combined physiological and stable isotope tracer analyses that NH(2)OH is both produced and consumed during the oxidation of NH(3) to NO(2)(-) by Nitrosopumilus maritimus, that consumption is coupled to energy conversion, and that NH(2)OH is the most probable product of the archaeal AMO homolog. Thus, despite their deep phylogenetic divergence, initial oxidation of NH(3) by bacteria and archaea appears mechanistically similar. They however diverge biochemically at the point of oxidation of NH(2)OH, the archaea possibly catalyzing NH(2)OH oxidation using a novel enzyme complex.

SUBMITTER: Vajrala N

PROVIDER: S-EPMC3549078 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

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Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea.

Vajrala Neeraja N Martens-Habbena Willm W Sayavedra-Soto Luis A LA Schauer Andrew A Bottomley Peter J PJ Stahl David A DA Arp Daniel J DJ

Proceedings of the National Academy of Sciences of the United States of America 20121231 3

The ammonia-oxidizing archaea have recently been recognized as a significant component of many microbial communities in the biosphere. Although the overall stoichiometry of archaeal chemoautotrophic growth via ammonia (NH(3)) oxidation to nitrite (NO(2)(-)) is superficially similar to the ammonia-oxidizing bacteria, genome sequence analyses point to a completely unique biochemistry. The only genomic signature linking the bacterial and archaeal biochemistries of NH(3) oxidation is a highly diverg ...[more]

PMID: 23277575

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Project description:Marine Group II (MGII) archaea represent the most abundant planktonic archaeal group in ocean surface waters, but our understanding of the group has been limited by a lack of cultured representatives and few sequenced genomes. Here, we conducted a comparative phylogenomic analysis of 270 recently available MGII metagenome-assembled genomes (MAGs) to investigate their evolution and ecology. Based on a rank-normalised genome phylogeny, we propose that MGII is an order-level lineage for which we propose the name Candidatus Poseidoniales (after Gr. n. Poseidon, God of the sea), comprising the families Candidatus Poseidonaceae fam. nov. (formerly subgroup MGIIa) and Candidatus Thalassarchaeaceae fam. nov. (formerly subgroup MGIIb). Within these families, 21 genera could be resolved, many of which had distinct biogeographic ranges and inferred nutrient preferences. Phylogenetic analyses of key metabolic functions suggest that the ancestor of Ca. Poseidoniales was a surface water-dwelling photoheterotroph that evolved to occupy multiple related ecological niches based primarily on spectral tuning of proteorhodopsin genes. Interestingly, this adaptation appears to involve an overwrite mechanism whereby an existing single copy of the proteorhodopsin gene is replaced by a horizontally transferred copy, which in many instances should allow an abrupt change in light absorption capacity. Phototrophy was lost entirely from five Ca. Poseidoniales genera coinciding with their adaptation to deeper aphotic waters. We also report the first instances of nitrate reductase in two genera acquired via horizontal gene transfer (HGT), which was a potential adaptation to oxygen limitation. Additional metabolic traits differentiating families and genera include flagellar-based adhesion, transporters, and sugar, amino acid, and peptide degradation. Our results suggest that HGT has shaped the evolution of Ca. Poseidoniales to occupy a variety of ecological niches and to become the most successful archaeal lineage in ocean surface waters.

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Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea.

Publications

Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea.

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