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Factors influencing the diversity of iron uptake systems in aquatic microorganisms.

Desai DK, Desai FD, Laroche J - Front Microbiol (2012)

Bottom Line: A multivariate statistical approach demonstrated that in phototrophic organisms, there is a clear influence of the ecological niche on the diversity of Fe uptake systems.Extending the analyses to the metagenome database from the Global Ocean Sampling expedition, we demonstrated that the Fe uptake and homeostasis mechanisms differed significantly across marine niches defined by temperatures and dFe concentrations, and that this difference was linked to the distribution of microbial taxa in these niches.Using the dN/dS ratios (which signify the rate of non-synonymous mutations) of the nucleotide sequences, we identified that genes encoding for TonB, Ferritin, Ferric reductase, IdiA, ZupT, and Fe(2+) transport proteins FeoA and FeoB were evolving at a faster rate (positive selection pressure) while genes encoding ferrisiderophore, heme and Vitamin B12 uptake systems, siderophore biosynthesis, and IsiA and IsiB were under purifying selection pressure (evolving slowly).

View Article: PubMed Central - PubMed

Affiliation: Biological Oceanography Division, Helmholtz-Zentrum für Ozeanforschung Kiel (GEOMAR) Kiel, Germany.

ABSTRACT
Iron (Fe) is an essential micronutrient for many processes in all living cells. Dissolved Fe (dFe) concentrations in the ocean are of the order of a few nM, and Fe is often a factor limiting primary production. Bioavailability of Fe in aquatic environments is believed to be primarily controlled through chelation by Fe-binding ligands. Marine microbes have evolved different mechanisms to cope with the scarcity of bioavailable dFe. Gradients in dFe concentrations and diversity of the Fe-ligand pool from coastal to open ocean waters have presumably imposed selection pressures that should be reflected in the genomes of microbial communities inhabiting the pelagic realm. We applied a hidden Markov model (HMM)-based search for proteins related to cellular iron metabolism, and in particular those involved in Fe uptake mechanisms in 164 microbial genomes belonging to diverse taxa and occupying different aquatic niches. A multivariate statistical approach demonstrated that in phototrophic organisms, there is a clear influence of the ecological niche on the diversity of Fe uptake systems. Extending the analyses to the metagenome database from the Global Ocean Sampling expedition, we demonstrated that the Fe uptake and homeostasis mechanisms differed significantly across marine niches defined by temperatures and dFe concentrations, and that this difference was linked to the distribution of microbial taxa in these niches. Using the dN/dS ratios (which signify the rate of non-synonymous mutations) of the nucleotide sequences, we identified that genes encoding for TonB, Ferritin, Ferric reductase, IdiA, ZupT, and Fe(2+) transport proteins FeoA and FeoB were evolving at a faster rate (positive selection pressure) while genes encoding ferrisiderophore, heme and Vitamin B12 uptake systems, siderophore biosynthesis, and IsiA and IsiB were under purifying selection pressure (evolving slowly).

No MeSH data available.


Non-parametric multidimensional scaling plots showing the clustering of genomes and metagenomes based on the similarities of occurrence patterns of Fe uptake systems. (A) Heterotrophic genomes labeled by taxa, (B) phototrophic genomes labeled by taxa, (C) phototrophic genomes labeled by niche, and (D) GOS metagenomes labeled by marine niche groups.
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Figure 3: Non-parametric multidimensional scaling plots showing the clustering of genomes and metagenomes based on the similarities of occurrence patterns of Fe uptake systems. (A) Heterotrophic genomes labeled by taxa, (B) phototrophic genomes labeled by taxa, (C) phototrophic genomes labeled by niche, and (D) GOS metagenomes labeled by marine niche groups.

Mentions: The NMDS plot of 110 heterotrophic genomes showed three distinct clusters corresponding to the three taxa (Figure 3A). The differences in Fe-metabolism systems among the three groups were statistically significant (Table 2). The greatest diversity of TBD hydroxamate/catecholate siderophore and heme uptake components, and occurrence frequency of bacterioferritin and NIS biosynthesis component RhbB, as identified by SIMPER, was seen in Gammaproteobacteria (Table 3). The Alphaproteobacteria genomes had the highest occurrence frequencies of Ferric reductase, the Zinc uptake protein ZupT (free Fe2+and other divalent cations), and FbpA (Fe3+ transporter component) as well as regulatory elements Fur and RirA. The ferric citrate uptake protein FecA, the FeoAB proteins (Fe2+ uptake), and Ferritin were amongst the most abundant in Flavobacteria and infrequent in the other two groups of heterotrophic bacteria. The regulatory element DtxR was only present in Flavobacteria and absent in Alphaproteobacteria and Gammaproteobacteria.


Factors influencing the diversity of iron uptake systems in aquatic microorganisms.

Desai DK, Desai FD, Laroche J - Front Microbiol (2012)

Non-parametric multidimensional scaling plots showing the clustering of genomes and metagenomes based on the similarities of occurrence patterns of Fe uptake systems. (A) Heterotrophic genomes labeled by taxa, (B) phototrophic genomes labeled by taxa, (C) phototrophic genomes labeled by niche, and (D) GOS metagenomes labeled by marine niche groups.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3475125&req=5

Figure 3: Non-parametric multidimensional scaling plots showing the clustering of genomes and metagenomes based on the similarities of occurrence patterns of Fe uptake systems. (A) Heterotrophic genomes labeled by taxa, (B) phototrophic genomes labeled by taxa, (C) phototrophic genomes labeled by niche, and (D) GOS metagenomes labeled by marine niche groups.
Mentions: The NMDS plot of 110 heterotrophic genomes showed three distinct clusters corresponding to the three taxa (Figure 3A). The differences in Fe-metabolism systems among the three groups were statistically significant (Table 2). The greatest diversity of TBD hydroxamate/catecholate siderophore and heme uptake components, and occurrence frequency of bacterioferritin and NIS biosynthesis component RhbB, as identified by SIMPER, was seen in Gammaproteobacteria (Table 3). The Alphaproteobacteria genomes had the highest occurrence frequencies of Ferric reductase, the Zinc uptake protein ZupT (free Fe2+and other divalent cations), and FbpA (Fe3+ transporter component) as well as regulatory elements Fur and RirA. The ferric citrate uptake protein FecA, the FeoAB proteins (Fe2+ uptake), and Ferritin were amongst the most abundant in Flavobacteria and infrequent in the other two groups of heterotrophic bacteria. The regulatory element DtxR was only present in Flavobacteria and absent in Alphaproteobacteria and Gammaproteobacteria.

Bottom Line: A multivariate statistical approach demonstrated that in phototrophic organisms, there is a clear influence of the ecological niche on the diversity of Fe uptake systems.Extending the analyses to the metagenome database from the Global Ocean Sampling expedition, we demonstrated that the Fe uptake and homeostasis mechanisms differed significantly across marine niches defined by temperatures and dFe concentrations, and that this difference was linked to the distribution of microbial taxa in these niches.Using the dN/dS ratios (which signify the rate of non-synonymous mutations) of the nucleotide sequences, we identified that genes encoding for TonB, Ferritin, Ferric reductase, IdiA, ZupT, and Fe(2+) transport proteins FeoA and FeoB were evolving at a faster rate (positive selection pressure) while genes encoding ferrisiderophore, heme and Vitamin B12 uptake systems, siderophore biosynthesis, and IsiA and IsiB were under purifying selection pressure (evolving slowly).

View Article: PubMed Central - PubMed

Affiliation: Biological Oceanography Division, Helmholtz-Zentrum für Ozeanforschung Kiel (GEOMAR) Kiel, Germany.

ABSTRACT
Iron (Fe) is an essential micronutrient for many processes in all living cells. Dissolved Fe (dFe) concentrations in the ocean are of the order of a few nM, and Fe is often a factor limiting primary production. Bioavailability of Fe in aquatic environments is believed to be primarily controlled through chelation by Fe-binding ligands. Marine microbes have evolved different mechanisms to cope with the scarcity of bioavailable dFe. Gradients in dFe concentrations and diversity of the Fe-ligand pool from coastal to open ocean waters have presumably imposed selection pressures that should be reflected in the genomes of microbial communities inhabiting the pelagic realm. We applied a hidden Markov model (HMM)-based search for proteins related to cellular iron metabolism, and in particular those involved in Fe uptake mechanisms in 164 microbial genomes belonging to diverse taxa and occupying different aquatic niches. A multivariate statistical approach demonstrated that in phototrophic organisms, there is a clear influence of the ecological niche on the diversity of Fe uptake systems. Extending the analyses to the metagenome database from the Global Ocean Sampling expedition, we demonstrated that the Fe uptake and homeostasis mechanisms differed significantly across marine niches defined by temperatures and dFe concentrations, and that this difference was linked to the distribution of microbial taxa in these niches. Using the dN/dS ratios (which signify the rate of non-synonymous mutations) of the nucleotide sequences, we identified that genes encoding for TonB, Ferritin, Ferric reductase, IdiA, ZupT, and Fe(2+) transport proteins FeoA and FeoB were evolving at a faster rate (positive selection pressure) while genes encoding ferrisiderophore, heme and Vitamin B12 uptake systems, siderophore biosynthesis, and IsiA and IsiB were under purifying selection pressure (evolving slowly).

No MeSH data available.