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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

Membrane lipid composition of “Ca. Nitrosotalea devanaterra.” Base peak chromatograms of core glycerol dibiphytanyl glycerol tetraether lipids (GDGTs) (A) and GDGT-based intact polar lipids (B) are shown. Cren′ refers to a regioisomer of crenarchaeol. Percentages below “4+Crenarchaeol” indicate the relative contributions of GDGT-4 and crenarchaeol to the peak, respectively. Peaks belong to various core GDGTs from 0 to 4, including GDGTs with hydroxy cores.
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Figure 3: Membrane lipid composition of “Ca. Nitrosotalea devanaterra.” Base peak chromatograms of core glycerol dibiphytanyl glycerol tetraether lipids (GDGTs) (A) and GDGT-based intact polar lipids (B) are shown. Cren′ refers to a regioisomer of crenarchaeol. Percentages below “4+Crenarchaeol” indicate the relative contributions of GDGT-4 and crenarchaeol to the peak, respectively. Peaks belong to various core GDGTs from 0 to 4, including GDGTs with hydroxy cores.

Mentions: The membrane lipid composition of “Ca. Nitrosotalea devanaterra” was investigated to determine whether it was distinct from that of neutrophilic AOA and therefore a potential adaptation to low pH. Thaumarchaea have glycerol dibiphytanyl glycerol tetraether lipids (GDGTs), with crenarchaeol typically the dominant GDGT in AOA (accounting for >30% of all lipids [24, 59–61]), but its proportion is much lower (11%) in “Ca. Nitrosotalea devanaterra.” Instead, GDGT-4 was the dominant membrane lipid in “Ca. Nitrosotalea devanaterra” (Fig. 3). The dominance of GDGT-4 over GDGT-0 to -3 in “Ca. Nitrosotalea devanaterra” compared to other AOA is in agreement with culture studies of acidophilic archaea which show an increase in the number of cyclopentane moieties in GDGTs with decreasing pH (62, 63). Furthermore, the increase in rings is thought to increase the packing density of the lipid membrane (64), which may reduce membrane permeability. The head groups of the “Ca. Nitrosotalea devanaterra” GDGTs are dominated by sugar moieties (glycolipids), in agreement with previous reports on acidophilic archaea which showed an increase in glycolipids versus phospholipids with decreasing pH (16). An increase in sugar units on the outside cell wall has been suggested to provide protection against proton entry (65). Hydroxylated GDGTs were also detected as cores, as in group 1.1a AOA (60), consistent with the 16S rRNA and amoA gene phylogenetic placement of Nitrosotalea (6).


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)

Membrane lipid composition of “Ca. Nitrosotalea devanaterra.” Base peak chromatograms of core glycerol dibiphytanyl glycerol tetraether lipids (GDGTs) (A) and GDGT-based intact polar lipids (B) are shown. Cren′ refers to a regioisomer of crenarchaeol. Percentages below “4+Crenarchaeol” indicate the relative contributions of GDGT-4 and crenarchaeol to the peak, respectively. Peaks belong to various core GDGTs from 0 to 4, including GDGTs with hydroxy cores.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Membrane lipid composition of “Ca. Nitrosotalea devanaterra.” Base peak chromatograms of core glycerol dibiphytanyl glycerol tetraether lipids (GDGTs) (A) and GDGT-based intact polar lipids (B) are shown. Cren′ refers to a regioisomer of crenarchaeol. Percentages below “4+Crenarchaeol” indicate the relative contributions of GDGT-4 and crenarchaeol to the peak, respectively. Peaks belong to various core GDGTs from 0 to 4, including GDGTs with hydroxy cores.
Mentions: The membrane lipid composition of “Ca. Nitrosotalea devanaterra” was investigated to determine whether it was distinct from that of neutrophilic AOA and therefore a potential adaptation to low pH. Thaumarchaea have glycerol dibiphytanyl glycerol tetraether lipids (GDGTs), with crenarchaeol typically the dominant GDGT in AOA (accounting for >30% of all lipids [24, 59–61]), but its proportion is much lower (11%) in “Ca. Nitrosotalea devanaterra.” Instead, GDGT-4 was the dominant membrane lipid in “Ca. Nitrosotalea devanaterra” (Fig. 3). The dominance of GDGT-4 over GDGT-0 to -3 in “Ca. Nitrosotalea devanaterra” compared to other AOA is in agreement with culture studies of acidophilic archaea which show an increase in the number of cyclopentane moieties in GDGTs with decreasing pH (62, 63). Furthermore, the increase in rings is thought to increase the packing density of the lipid membrane (64), which may reduce membrane permeability. The head groups of the “Ca. Nitrosotalea devanaterra” GDGTs are dominated by sugar moieties (glycolipids), in agreement with previous reports on acidophilic archaea which showed an increase in glycolipids versus phospholipids with decreasing pH (16). An increase in sugar units on the outside cell wall has been suggested to provide protection against proton entry (65). Hydroxylated GDGTs were also detected as cores, as in group 1.1a AOA (60), consistent with the 16S rRNA and amoA gene phylogenetic placement of Nitrosotalea (6).

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