The metagenomic basis of anammox metabolism in <i>Candidatus</i> ‘Brocadia fulgida’

Gori, Fabio; Tringe, Susannah G.; Kartal, Boran; Marchiori, Elena; Jetten, Mike S. M.

doi:10.1042/bst20110707

Cited by 100 publications

(49 citation statements)

References 21 publications

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“…In the present study, we showed the intracellular localization of the hydroxylamine oxidoreductase (HAO)-like protein kustc0457/58, hydrazine dehydrogenase (HDH), the NO-producing HAO-like protein HOX, nitrite oxidoreductase (NXR), and hydrazine synthase (HZS) within an anammox cell. All of these proteins are encoded in all presently available anammox genomes and play key roles in anammox catabolism (1,2,(9)(10)(11)(12)(13)(14). The fact that all studied protein complexes were exclusively immunolocalized to the anammoxosome in the present study supported the hypothesis that this cell compartment was a true prokaryotic organelle with a dedicated function.…”

Section: Discussionsupporting

confidence: 76%

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Immunogold Localization of Key Metabolic Enzymes in the Anammoxosome and on the Tubule-Like Structures of Kuenenia stuttgartiensis

et al. 2015

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Anaerobic ammonium-oxidizing (anammox) bacteria oxidize ammonium with nitrite as the terminal electron acceptor to form dinitrogen gas in the absence of oxygen. Anammox bacteria have a compartmentalized cell plan with a central membrane-bound "prokaryotic organelle" called the anammoxosome. The anammoxosome occupies most of the cell volume, has a curved membrane, and contains conspicuous tubule-like structures of unknown identity and function. It was suggested previously that the catalytic reactions of the anammox pathway occur in the anammoxosome, and that proton motive force was established across its membrane. Here, we used antibodies raised against five key enzymes of the anammox catabolism to determine their cellular location. The antibodies were raised against purified native hydroxylamine oxidoreductase-like protein kustc0458 with its redox partner kustc0457, hydrazine dehydrogenase (HDH; kustc0694), hydroxylamine oxidase (HOX; kustc1061), nitrite oxidoreductase (NXR; kustd1700/03/04), and hydrazine synthase (HZS; kuste2859-61) of the anammox bacterium Kuenenia stuttgartiensis. We determined that all five protein complexes were exclusively located inside the anammoxosome matrix. Four of the protein complexes did not appear to form higher-order protein organizations. However, the present data indicated for the first time that NXR is part of the tubule-like structures, which may stretch the whole length of the anammoxosome. These findings support the anammoxosome as the locus of catabolic reactions of the anammox pathway. IMPORTANCEAnammox bacteria are environmentally relevant microorganisms that contribute significantly to the release of fixed nitrogen in nature. Furthermore, the anammox process is applied for nitrogen removal from wastewater as an environment-friendly and cost-effective technology. These microorganisms feature a unique cellular organelle, the anammoxosome, which was proposed to contain the energy metabolism of the cell and tubule-like structures with hitherto unknown function. Here, we purified five native enzymes catalyzing key reactions in the anammox metabolism and raised antibodies against these in order to localize them within the cell. We showed that all enzymes were located within the anammoxosome, and nitrite oxidoreductase was located exclusively at the tubule-like structures, providing the first insights into the function of these subcellular structures.

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Section: Discussionsupporting

confidence: 76%

“…Apart from nitrite reductase, all currently available anammox genomes encode close homologs of the proteins described above (2,(9)(10)(11)(12)(13)(14), suggesting that they have the same energy metabolism as K. stuttgartiensis.…”

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confidence: 99%

Immunogold Localization of Key Metabolic Enzymes in the Anammoxosome and on the Tubule-Like Structures of Kuenenia stuttgartiensis

et al. 2015

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“…Our results showed that the most common anammox species in these soils were related to the genus "Candidatus Brocadia," which has been observed in other paddy soils (13,15). These results suggest that "Candidatus Brocadia" possess better adaptability in terrestrial ecosystems given that "Candidatus Brocadia" harbor diverse metabolism pathways (42); for example, they could use short-chain organic acids as alternative electron donors (43). Additionally, two novel clusters also were detected in our samples, suggesting that unknown anammox events are yet to be discovered and investigated.…”

Section: Figsupporting

confidence: 50%

Potential Contribution of Anammox to Nitrogen Loss from Paddy Soils in Southern China

Yang

Nie

et al. 2015

Appl Environ Microbiol

122

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eThe anaerobic oxidation of ammonium (anammox) process has been observed in diverse terrestrial ecosystems, while the contribution of anammox to N 2 production in paddy soils is not well documented. In this study, the anammox activity and the abundance and diversity of anammox bacteria were investigated to assess the anammox potential of 12 typical paddy soils collected in southern China. Anammox bacteria related to "Candidatus Brocadia" and "Candidatus Kuenenia" and two novel unidentified clusters were detected, with "Candidatus Brocadia" comprising 50% of the anammox population. The prevalence of the anammox was confirmed by the quantitative PCR results based on hydrazine synthase (hzsB) genes, which showed that the abundance ranged from 1.16 ؋ 10 4 to 9.65 ؋ 10 4 copies per gram of dry weight. The anammox rates measured by the isotope-pairing technique ranged from 0.27 to 5.25 nmol N per gram of soil per hour in these paddy soils, which contributed 0.6 to 15% to soil N 2 production. It is estimated that a total loss of 2.50 ؋ 10 6 Mg N per year is linked to anammox in the paddy fields in southern China, which implied that ca. 10% of the applied ammonia fertilizers is lost via the anammox process. Anammox activity was significantly correlated with the abundance of hzsB genes, soil nitrate concentration, and C/N ratio. Additionally, ammonia concentration and pH were found to be significantly correlated with the anammox bacterial structure.

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“…Kuenenia (Strous et al, 2006; Speth et al, 2012), Ca . Brocadia (Gori et al, 2011), Ca . Jettenia (Hu et al, 2012c), and Ca .…”

Section: Discussionmentioning

confidence: 99%

Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria

2014

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Anaerobic ammonia-oxidizing (anammox) bacteria are able to oxidize ammonia and reduce nitrite to produce N2 gas. After being discovered in a wastewater treatment plant (WWTP), anammox bacteria were subsequently characterized in natural environments, including marine, estuary, freshwater, and terrestrial habitats. Although anammox bacteria play an important role in removing fixed N from both engineered and natural ecosystems, broad scale anammox bacterial distributions have not yet been summarized. The objectives of this study were to explore global distributions and diversity of anammox bacteria and to identify factors that influence their biogeography. Over 6000 anammox 16S rRNA gene sequences from the public database were analyzed in this current study. Data ordinations indicated that salinity was an important factor governing anammox bacterial distributions, with distinct populations inhabiting natural and engineered ecosystems. Gene phylogenies and rarefaction analysis demonstrated that freshwater environments and the marine water column harbored the highest and the lowest diversity of anammox bacteria, respectively. Co-occurrence network analysis indicated that Ca. Scalindua strongly connected with other Ca. Scalindua taxa, whereas Ca. Brocadia co-occurred with taxa from both known and unknown anammox genera. Our survey provides a better understanding of ecological factors affecting anammox bacterial distributions and provides a comprehensive baseline for understanding the relationships among anammox communities in global environments.

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The metagenomic basis of anammox metabolism in Candidatus ‘Brocadia fulgida’

Cited by 100 publications

References 21 publications

Immunogold Localization of Key Metabolic Enzymes in the Anammoxosome and on the Tubule-Like Structures of Kuenenia stuttgartiensis

Immunogold Localization of Key Metabolic Enzymes in the Anammoxosome and on the Tubule-Like Structures of Kuenenia stuttgartiensis

Potential Contribution of Anammox to Nitrogen Loss from Paddy Soils in Southern China

Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria

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