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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.


Median and range of dissolved Fe concentrations (A) and Temperature (B) for the GOS metagenome sample groups used in the study. Numbers of samples in the groups are as follows: Atlantic (18), Pacific (12), Atlantic Open Ocean (9), Pacific Open Ocean (5), Pacific-Coastal (7), Tropical-Open Ocean (11), Tropical-Coastal (11), Temperate-Coastal (8), Open Ocean (14), Coastal (16).
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Figure 6: Median and range of dissolved Fe concentrations (A) and Temperature (B) for the GOS metagenome sample groups used in the study. Numbers of samples in the groups are as follows: Atlantic (18), Pacific (12), Atlantic Open Ocean (9), Pacific Open Ocean (5), Pacific-Coastal (7), Tropical-Open Ocean (11), Tropical-Coastal (11), Temperate-Coastal (8), Open Ocean (14), Coastal (16).

Mentions: To further understand the interaction between dFe and temperature and to define meaningful niche groups with contrasting parameters, we compared the median and range of the dFe concentrations as well as the temperatures (suitably transformed as described in the methods) for different group of GOS samples (Figures 6A,B respectively). There was a significant difference in dFe concentrations in the Pacific and Atlantic samples (single factor ANOVA, p value = 6.31E−09), and their median temperature difference was also significantly different (p value < 0.0005). The most noticeable difference of Fe concentrations was seen in the Atlantic Open Ocean samples and Pacific (Open Ocean and Coastal) samples (p value 1.3E−11) whereas the corresponding temperature difference between these groups was not significant (p value 0.27 at α = 0.01). Conversely, the Temperate, Coastal samples were primarily separated from the Tropical (Open Ocean and Coastal) samples by a temperature difference (p value 2.1E−07) with no difference in the corresponding average Fe concentrations (p value 0.3 at α = 0.01). Consequently, only these three pairs of groups (Atlantic Open Ocean vs. Pacific, Temperate vs. Tropical, and Open Ocean vs. Coastal) were further analyzed for the differences in their taxonomic profiles and their associated Fe-metabolism systems.


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

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

Median and range of dissolved Fe concentrations (A) and Temperature (B) for the GOS metagenome sample groups used in the study. Numbers of samples in the groups are as follows: Atlantic (18), Pacific (12), Atlantic Open Ocean (9), Pacific Open Ocean (5), Pacific-Coastal (7), Tropical-Open Ocean (11), Tropical-Coastal (11), Temperate-Coastal (8), Open Ocean (14), Coastal (16).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Median and range of dissolved Fe concentrations (A) and Temperature (B) for the GOS metagenome sample groups used in the study. Numbers of samples in the groups are as follows: Atlantic (18), Pacific (12), Atlantic Open Ocean (9), Pacific Open Ocean (5), Pacific-Coastal (7), Tropical-Open Ocean (11), Tropical-Coastal (11), Temperate-Coastal (8), Open Ocean (14), Coastal (16).
Mentions: To further understand the interaction between dFe and temperature and to define meaningful niche groups with contrasting parameters, we compared the median and range of the dFe concentrations as well as the temperatures (suitably transformed as described in the methods) for different group of GOS samples (Figures 6A,B respectively). There was a significant difference in dFe concentrations in the Pacific and Atlantic samples (single factor ANOVA, p value = 6.31E−09), and their median temperature difference was also significantly different (p value < 0.0005). The most noticeable difference of Fe concentrations was seen in the Atlantic Open Ocean samples and Pacific (Open Ocean and Coastal) samples (p value 1.3E−11) whereas the corresponding temperature difference between these groups was not significant (p value 0.27 at α = 0.01). Conversely, the Temperate, Coastal samples were primarily separated from the Tropical (Open Ocean and Coastal) samples by a temperature difference (p value 2.1E−07) with no difference in the corresponding average Fe concentrations (p value 0.3 at α = 0.01). Consequently, only these three pairs of groups (Atlantic Open Ocean vs. Pacific, Temperate vs. Tropical, and Open Ocean vs. Coastal) were further analyzed for the differences in their taxonomic profiles and their associated Fe-metabolism systems.

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.