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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.


Related in: MedlinePlus

(A) Average dN/dS ratios of selected genes. The genes are sorted by highest dN/dS value. (B) Phylogenetic spread as defined by maximum phylogenetic distance among the genomes possessing the gene. The black line marks the dN/dS value = 1. Genes with dN/dS >1 and a wide phylogenetic spread are marked with stars. Genes with dN/dS >1 and a narrow phylogenetic spread are marked by an arrow. Fe-red – Ferric reductase.
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Figure 7: (A) Average dN/dS ratios of selected genes. The genes are sorted by highest dN/dS value. (B) Phylogenetic spread as defined by maximum phylogenetic distance among the genomes possessing the gene. The black line marks the dN/dS value = 1. Genes with dN/dS >1 and a wide phylogenetic spread are marked with stars. Genes with dN/dS >1 and a narrow phylogenetic spread are marked by an arrow. Fe-red – Ferric reductase.

Mentions: The nucleotide sequences of some of the abundant genes, extracted from the genomes, were analyzed for the rate of non-synonymous mutations. Because non-synonymous mutations result in amino acid replacement, they are often eliminated by purifying selection, a form of natural selection that selectively removes deleterious mutations. Under certain selection pressures, non-synonymous mutations might be retained when they are advantageous (known as positive selection). The dN/dS ratio therefore provides a measure of the selection pressure operating on a gene. The dN/dS ratio for some of the genes was plotted (Figure 7) along with their average phylogenetic spread (the average phylogenetic distance among the genomes possessing the gene, calculated from a Maximum Likelihood tree of 16S rRNA gene sequences of the genomes). Ferric reductase, feoA, feoB, idiA, and the zinc uptake gene zupT, tonB, and ferritin genes all had a dN/dS value >1, indicating that non-synonymous mutations were possibly beneficial for these genes and that they were evolving rapidly under positive selection. With the exception of the idiA gene, all of these genes also had a wide phylogenetic spread indicating that they were present in a wide range of taxonomic groups (Figure 7). The remaining genes analyzed had a dN/dS ratio <1 (28 out of 35), indicating that they were under purifying selection pressure. All proteins involved in siderophore biosynthesis or high-affinity uptake systems for hydroxamate or catecholate siderophore/heme or vitamin B12 were undergoing purifying selection. The regulatory element fur, fbp-family gene fbpA, hitB, isiA, isiB, and the Mg2+ transporter mgtE were also included in the category of purifying selection and, with the exception of isiA, retained a wide phylogenetic spread among the marine genomes.


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

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

(A) Average dN/dS ratios of selected genes. The genes are sorted by highest dN/dS value. (B) Phylogenetic spread as defined by maximum phylogenetic distance among the genomes possessing the gene. The black line marks the dN/dS value = 1. Genes with dN/dS >1 and a wide phylogenetic spread are marked with stars. Genes with dN/dS >1 and a narrow phylogenetic spread are marked by an arrow. Fe-red – Ferric reductase.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: (A) Average dN/dS ratios of selected genes. The genes are sorted by highest dN/dS value. (B) Phylogenetic spread as defined by maximum phylogenetic distance among the genomes possessing the gene. The black line marks the dN/dS value = 1. Genes with dN/dS >1 and a wide phylogenetic spread are marked with stars. Genes with dN/dS >1 and a narrow phylogenetic spread are marked by an arrow. Fe-red – Ferric reductase.
Mentions: The nucleotide sequences of some of the abundant genes, extracted from the genomes, were analyzed for the rate of non-synonymous mutations. Because non-synonymous mutations result in amino acid replacement, they are often eliminated by purifying selection, a form of natural selection that selectively removes deleterious mutations. Under certain selection pressures, non-synonymous mutations might be retained when they are advantageous (known as positive selection). The dN/dS ratio therefore provides a measure of the selection pressure operating on a gene. The dN/dS ratio for some of the genes was plotted (Figure 7) along with their average phylogenetic spread (the average phylogenetic distance among the genomes possessing the gene, calculated from a Maximum Likelihood tree of 16S rRNA gene sequences of the genomes). Ferric reductase, feoA, feoB, idiA, and the zinc uptake gene zupT, tonB, and ferritin genes all had a dN/dS value >1, indicating that non-synonymous mutations were possibly beneficial for these genes and that they were evolving rapidly under positive selection. With the exception of the idiA gene, all of these genes also had a wide phylogenetic spread indicating that they were present in a wide range of taxonomic groups (Figure 7). The remaining genes analyzed had a dN/dS ratio <1 (28 out of 35), indicating that they were under purifying selection pressure. All proteins involved in siderophore biosynthesis or high-affinity uptake systems for hydroxamate or catecholate siderophore/heme or vitamin B12 were undergoing purifying selection. The regulatory element fur, fbp-family gene fbpA, hitB, isiA, isiB, and the Mg2+ transporter mgtE were also included in the category of purifying selection and, with the exception of isiA, retained a wide phylogenetic spread among the marine genomes.

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.


Related in: MedlinePlus