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Identifying Potential Mechanisms Enabling Acidophily in the Ammonia-Oxidizing Archaeon "Candidatus Nitrosotalea devanaterra".

Lehtovirta-Morley LE, Sayavedra-Soto LA, Gallois N, Schouten S, Stein LY, Prosser JI, Nicol GW - Appl. Environ. Microbiol. (2016)

Bottom Line: Instead, the genome indicates that "Ca Nitrosotalea devanaterra" contains genes encoding both a predicted high-affinity substrate acquisition system and potential pH homeostasis mechanisms absent in neutrophilic AOA.Analysis of mRNA revealed that candidate genes encoding the proposed homeostasis mechanisms were all expressed during acidophilic growth, and lipid profiling by high-performance liquid chromatography-mass spectrometry (HPLC-MS) demonstrated that the membrane lipids of "Ca Nitrosotalea devanaterra" were not dominated by crenarchaeol, as found in neutrophilic AOA.This study for the first time describes a genome of an obligately acidophilic ammonia oxidizer and identifies potential mechanisms enabling this unique phenotype for future biochemical characterization.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, United Kingdom l.lehtovirta@abdn.ac.uk.

No MeSH data available.


Related in: MedlinePlus

Ammonia oxidation machinery of “Ca. Nitrosotalea devanaterra.” (A and B) Conservation of the periplasmic active site in PmoB/AmoB (A) and PmoC/AmoC (B) sequences. (C) AMO gene cluster, Amt transporter, and PII gene arrangement. Longer alignments and protein topology predictions for AmoB and AmoC are in Fig. S3 and S4 in the supplemental material, respectively. Illustrated ORFs are drawn to scale, except for genes that are not involved in ammonia metabolism (truncated, white). The asterisks indicate that the “Candidatus Nitrosoarchaeum limnia” SFB1 and “Candidatus Nitrosotenuis uzonensis” genomes are not closed and distance cannot be estimated.
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Figure 4: Ammonia oxidation machinery of “Ca. Nitrosotalea devanaterra.” (A and B) Conservation of the periplasmic active site in PmoB/AmoB (A) and PmoC/AmoC (B) sequences. (C) AMO gene cluster, Amt transporter, and PII gene arrangement. Longer alignments and protein topology predictions for AmoB and AmoC are in Fig. S3 and S4 in the supplemental material, respectively. Illustrated ORFs are drawn to scale, except for genes that are not involved in ammonia metabolism (truncated, white). The asterisks indicate that the “Candidatus Nitrosoarchaeum limnia” SFB1 and “Candidatus Nitrosotenuis uzonensis” genomes are not closed and distance cannot be estimated.

Mentions: Since AOB cannot oxidize ammonia at low pH (8, 83), the substrate acquisition systems of “Ca. Nitrosotalea devanaterra,” AOA, and AOB were compared. The three histidine residues (His33, His137, and His139 in M. capsulatus Bath [37]) of AmoB/PmoB coordinating a periplasmic dicopper center are conserved in methanotrophs, AOB, and AOA (Fig. 4) but not in the acidophilic methane-oxidizing Verrucomicrobia (36, 37). In contrast, the variable metal binding site of AmoC is present in Verrucomicrobia, AOB, and AOA (38) (Fig. 4). In silico protein topology prediction for AmoB and AmoC favors an extracellular (outward-facing) location of the active site in “Ca. Nitrosotalea devanaterra” (see Fig. S3 and S4 in the supplemental material). The active site of AMO is conserved between “Ca. Nitrosotalea devanaterra,” AOA, and AOB and thus cannot explain the differences between these organisms.


Identifying Potential Mechanisms Enabling Acidophily in the Ammonia-Oxidizing Archaeon "Candidatus Nitrosotalea devanaterra".

Lehtovirta-Morley LE, Sayavedra-Soto LA, Gallois N, Schouten S, Stein LY, Prosser JI, Nicol GW - Appl. Environ. Microbiol. (2016)

Ammonia oxidation machinery of “Ca. Nitrosotalea devanaterra.” (A and B) Conservation of the periplasmic active site in PmoB/AmoB (A) and PmoC/AmoC (B) sequences. (C) AMO gene cluster, Amt transporter, and PII gene arrangement. Longer alignments and protein topology predictions for AmoB and AmoC are in Fig. S3 and S4 in the supplemental material, respectively. Illustrated ORFs are drawn to scale, except for genes that are not involved in ammonia metabolism (truncated, white). The asterisks indicate that the “Candidatus Nitrosoarchaeum limnia” SFB1 and “Candidatus Nitrosotenuis uzonensis” genomes are not closed and distance cannot be estimated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4836417&req=5

Figure 4: Ammonia oxidation machinery of “Ca. Nitrosotalea devanaterra.” (A and B) Conservation of the periplasmic active site in PmoB/AmoB (A) and PmoC/AmoC (B) sequences. (C) AMO gene cluster, Amt transporter, and PII gene arrangement. Longer alignments and protein topology predictions for AmoB and AmoC are in Fig. S3 and S4 in the supplemental material, respectively. Illustrated ORFs are drawn to scale, except for genes that are not involved in ammonia metabolism (truncated, white). The asterisks indicate that the “Candidatus Nitrosoarchaeum limnia” SFB1 and “Candidatus Nitrosotenuis uzonensis” genomes are not closed and distance cannot be estimated.
Mentions: Since AOB cannot oxidize ammonia at low pH (8, 83), the substrate acquisition systems of “Ca. Nitrosotalea devanaterra,” AOA, and AOB were compared. The three histidine residues (His33, His137, and His139 in M. capsulatus Bath [37]) of AmoB/PmoB coordinating a periplasmic dicopper center are conserved in methanotrophs, AOB, and AOA (Fig. 4) but not in the acidophilic methane-oxidizing Verrucomicrobia (36, 37). In contrast, the variable metal binding site of AmoC is present in Verrucomicrobia, AOB, and AOA (38) (Fig. 4). In silico protein topology prediction for AmoB and AmoC favors an extracellular (outward-facing) location of the active site in “Ca. Nitrosotalea devanaterra” (see Fig. S3 and S4 in the supplemental material). The active site of AMO is conserved between “Ca. Nitrosotalea devanaterra,” AOA, and AOB and thus cannot explain the differences between these organisms.

Bottom Line: Instead, the genome indicates that "Ca Nitrosotalea devanaterra" contains genes encoding both a predicted high-affinity substrate acquisition system and potential pH homeostasis mechanisms absent in neutrophilic AOA.Analysis of mRNA revealed that candidate genes encoding the proposed homeostasis mechanisms were all expressed during acidophilic growth, and lipid profiling by high-performance liquid chromatography-mass spectrometry (HPLC-MS) demonstrated that the membrane lipids of "Ca Nitrosotalea devanaterra" were not dominated by crenarchaeol, as found in neutrophilic AOA.This study for the first time describes a genome of an obligately acidophilic ammonia oxidizer and identifies potential mechanisms enabling this unique phenotype for future biochemical characterization.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, United Kingdom l.lehtovirta@abdn.ac.uk.

No MeSH data available.


Related in: MedlinePlus