Iron transporters in marine prokaryotic genomes and metagenomes

Abstract

In the pelagic environment, iron is a scarce but essential micronutrient. The iron acquisition capabilities of selected marine bacteria have been investigated, but the recent proliferation of marine prokaryotic genomes and metagenomes offers a more comprehensive picture of microbial iron uptake pathways in the ocean. Searching these data sets, we were able to identify uptake mechanisms for Fe(3+), Fe(2+) and iron chelates (e.g. siderophore and haem iron complexes). Transport of iron chelates is accomplished by TonB-dependent transporters (TBDTs). After clustering the TBDTs from marine prokaryotic genomes, we identified TBDT clusters for the transport of hydroxamate and catecholate siderophore iron complexes and haem using gene neighbourhood analysis and co-clustering of TBDTs of known function. The genomes also contained two classes of siderophore biosynthesis genes: NRPS (non-ribosomal peptide synthase) genes and NIS (NRPS Independent Siderophore) genes. The most common iron transporters, in both the genomes and metagenomes, were Fe(3+) ABC transporters. Iron uptake-related TBDTs and siderophore biosynthesis genes were less common in pelagic marine metagenomes relative to the genomic data set, in part because Pelagibacter ubique and Prochlorococcus species, which almost entirely lacked these Fe uptake systems, dominate the metagenomes. Our results are largely consistent with current knowledge of iron speciation in the ocean, but suggest that in certain niches the ability to acquire siderophores and/or haem iron chelates is beneficial.

Microbial iron uptake in the naturally fertilized waters in the vicinity of the Kerguelen Islands: phytoplankton–bacteria interactions

“…Southern Ocean phytoplankton species responded to Fe-light acclimation differently than temperate species (Sunda and Huntsman, 1997;Strzepek et al, 2012). In the case of heterotrophic bacteria, culture studies (Granger and Price, 1999;Armstrong et al, 2004;Fourquez et al, 2014) and metagenomic analysis (Hopkinson and Barbeau, 2012;Toulza et al, 2012) have also provided foundations for our understanding of the responses of bacteria to Fe limitation but extrapolation to field observations face the same constraints as mentioned for phytoplankton.…”

Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae

“…Both FeoA and FeoB proteins identified here are most similar to the MAI-containing magnetosome proteins Mad17 and Mad30 of Deltaproteobacteria MTB, respectively, (Lefèvre et al, 2013b), although they are outside of the MAI in Mcas. One gene belonging to the general metal 2 þ transporter NRAMP family was also found in the genome, which may provide an alternative mechanism for Fe 2 þ uptake (Forbes and Gros, 2001;Hopkinson and Barbeau, 2012). Although genes for Sfu/Fbp/Fut family of ferric iron transporters and siderophore biosynthesis were not found, we identified several putative genes for TonB-dependent transporters (catecholate and heme) and Fe 3 þ ABC ATPase, indicating that Mcas has the potential to acquire Fe 3 þ from the environments as well.…”

Coordinated transporter activity shapes high-affinity iron acquisition in cyanobacteria

“…The composition of Fe transporters analyzed here is not unique. Many microorganisms possess the genetic potential for multiple iron transporters (Rivers et al, 2009;Desai et al, 2012;Hopkinson and Barbeau, 2012;Morrissey and Bowler, 2012). Bioinformatic analyses of iron transport genes revealed that fut genes are common in cyanobacteria (Rivers et al, 2009;Hopkinson and Barbeau, 2012, with additional analysis included in Supplementary Figure S4).…”

“…Many microorganisms possess the genetic potential for multiple iron transporters (Rivers et al, 2009;Desai et al, 2012;Hopkinson and Barbeau, 2012;Morrissey and Bowler, 2012). Bioinformatic analyses of iron transport genes revealed that fut genes are common in cyanobacteria (Rivers et al, 2009;Hopkinson and Barbeau, 2012, with additional analysis included in Supplementary Figure S4). Feo genes were identified in freshwater and coastal cyanobacteria but were notably absent from marine picocyanobacteria (Palenik et al, 2006;Rivers et al, 2009;Desai et al, 2012;Hopkinson and Barbeau, 2012;Supplementary Figure S4).…”

“…Bioinformatic analyses of iron transport genes revealed that fut genes are common in cyanobacteria (Rivers et al, 2009;Hopkinson and Barbeau, 2012, with additional analysis included in Supplementary Figure S4). Feo genes were identified in freshwater and coastal cyanobacteria but were notably absent from marine picocyanobacteria (Palenik et al, 2006;Rivers et al, 2009;Desai et al, 2012;Hopkinson and Barbeau, 2012;Supplementary Figure S4). However, many of the marine picocyanobacteria strains did possess a broad-specificity divalent metal transporter, the natural resistance-associated macrophage protein (Hopkinson and Barbeau, 2012), suggesting the potential for Fe(II) transport.…”