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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.


Distribution of components of Fe-metabolism systems in (A) marine microbial taxa and (B) Temperature groupings of metagenomes. For detailed description of the components of each system see Table 1.
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Figure 1: Distribution of components of Fe-metabolism systems in (A) marine microbial taxa and (B) Temperature groupings of metagenomes. For detailed description of the components of each system see Table 1.

Mentions: A set of proteins involved in iron metabolism (Table 1) was recovered from 164 marine microbial genomes belonging to Cyanobacteria, eukaryotic phytoplankton, Alphaproteobacteria, Gammaproteobacteria, and Flavobacteria (Figure 1A) using HMMs with optimized thresholds and modified emission probabilities as described earlier (Srivastava et al., 2007). The heme biosynthesis system, the TonB/ExbB/ExbD system, ferredoxin, and the iron-sulfur cluster assembly protein Isca1 (Table 1) were present in almost all prokaryotic genomes and therefore removed from further analysis. The observed abundances of TBD Fe-siderophore uptake systems, components of Fe2+ or divalent cation uptake and Fe3+ transporters were in agreement with previous reports (Hopkinson and Barbeau, 2012). The TBD uptake systems for catecholate, hydroxamate, and citrate siderophores were more widespread in Gammaproteobacteria (60, 55, and 37% of the genomes, respectively) as compared to Alphaproteobacteria (24, 16, and 13%, respectively), Flavobacteria (13, 8, and 30%, respectively), and Cyanobacteria (2, 19, and 19%, respectively). Fe2+ or divalent cation transporters were abundant in all the taxa but were most abundant in the eukaryotic phytoplankton genomes (39%). Ferric reductase was characteristic of the eukaryotic phytoplankton group (71%), but was also present in Cyanobacteria (2%), Alphaproteobacteria (16%), and Gammaproteobacteria (10%). Fe3+ transporters occurred in Cyanobacteria (37%), Alphaproteobacteria (33%), and Gammaproteobacteria (27%), but were uncommon in Flavobacteria (2%) and absent from eukaryotic phytoplankton. NRPS and NIS components involved in siderophore biosynthesis were present in Alphaproteobacteria (14 and 16%), Gammaproteobacteria (14 and 39%), Flavobacteria (14 and 22%), Cyanobacteria (32 and 11%), and also in eukaryotic phytoplankton (24 and 11% respectively).


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

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

Distribution of components of Fe-metabolism systems in (A) marine microbial taxa and (B) Temperature groupings of metagenomes. For detailed description of the components of each system see Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Distribution of components of Fe-metabolism systems in (A) marine microbial taxa and (B) Temperature groupings of metagenomes. For detailed description of the components of each system see Table 1.
Mentions: A set of proteins involved in iron metabolism (Table 1) was recovered from 164 marine microbial genomes belonging to Cyanobacteria, eukaryotic phytoplankton, Alphaproteobacteria, Gammaproteobacteria, and Flavobacteria (Figure 1A) using HMMs with optimized thresholds and modified emission probabilities as described earlier (Srivastava et al., 2007). The heme biosynthesis system, the TonB/ExbB/ExbD system, ferredoxin, and the iron-sulfur cluster assembly protein Isca1 (Table 1) were present in almost all prokaryotic genomes and therefore removed from further analysis. The observed abundances of TBD Fe-siderophore uptake systems, components of Fe2+ or divalent cation uptake and Fe3+ transporters were in agreement with previous reports (Hopkinson and Barbeau, 2012). The TBD uptake systems for catecholate, hydroxamate, and citrate siderophores were more widespread in Gammaproteobacteria (60, 55, and 37% of the genomes, respectively) as compared to Alphaproteobacteria (24, 16, and 13%, respectively), Flavobacteria (13, 8, and 30%, respectively), and Cyanobacteria (2, 19, and 19%, respectively). Fe2+ or divalent cation transporters were abundant in all the taxa but were most abundant in the eukaryotic phytoplankton genomes (39%). Ferric reductase was characteristic of the eukaryotic phytoplankton group (71%), but was also present in Cyanobacteria (2%), Alphaproteobacteria (16%), and Gammaproteobacteria (10%). Fe3+ transporters occurred in Cyanobacteria (37%), Alphaproteobacteria (33%), and Gammaproteobacteria (27%), but were uncommon in Flavobacteria (2%) and absent from eukaryotic phytoplankton. NRPS and NIS components involved in siderophore biosynthesis were present in Alphaproteobacteria (14 and 16%), Gammaproteobacteria (14 and 39%), Flavobacteria (14 and 22%), Cyanobacteria (32 and 11%), and also in eukaryotic phytoplankton (24 and 11% respectively).

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.