Dataset Information

Diversity and Evolutionary History of Iron Metabolism Genes in Diatoms.

ABSTRACT: Ferroproteins arose early in Earth's history, prior to the emergence of oxygenic photosynthesis and the subsequent reduction of bioavailable iron. Today, iron availability limits primary productivity in about 30% of the world's oceans. Diatoms, responsible for nearly half of oceanic primary production, have evolved molecular strategies for coping with variable iron concentrations. Our understanding of the evolutionary breadth of these strategies has been restricted by the limited number of species for which molecular sequence data is available. To uncover the diversity of strategies marine diatoms employ to meet cellular iron demands, we analyzed 367 newly released marine microbial eukaryotic transcriptomes, which include 47 diatom species. We focused on genes encoding proteins previously identified as having a role in iron management: iron uptake (high-affinity ferric reductase, multi-copper oxidase, and Fe(III) permease); iron storage (ferritin); iron-induced protein substitutions (flavodoxin/ferredoxin, and plastocyanin/cytochrome c6) and defense against reactive oxygen species (superoxide dismutases). Homologs encoding the high-affinity iron uptake system components were detected across the four diatom Classes suggesting an ancient origin for this pathway. Ferritin transcripts were also detected in all Classes, revealing a more widespread utilization of ferritin throughout diatoms than previously recognized. Flavodoxin and plastocyanin transcripts indicate possible alternative redox metal strategies. Predicted localization signals for ferredoxin identify multiple examples of gene transfer from the plastid to the nuclear genome. Transcripts encoding four superoxide dismutase metalloforms were detected, including a putative nickel-coordinating isozyme. Taken together, our results suggest that the majority of iron metabolism genes in diatoms appear to be vertically inherited with functional diversity achieved via possible neofunctionalization of paralogs. This refined view of iron use strategies in diatoms elucidates the history of these adaptations, and provides potential molecular markers for determining the iron nutritional status of different diatom species in environmental samples.

SUBMITTER: Groussman RD

PROVIDER: S-EPMC4460010 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Diversity and Evolutionary History of Iron Metabolism Genes in Diatoms.

Groussman Ryan D RD Parker Micaela S MS Armbrust E Virginia EV

PloS one 20150608 6

Ferroproteins arose early in Earth's history, prior to the emergence of oxygenic photosynthesis and the subsequent reduction of bioavailable iron. Today, iron availability limits primary productivity in about 30% of the world's oceans. Diatoms, responsible for nearly half of oceanic primary production, have evolved molecular strategies for coping with variable iron concentrations. Our understanding of the evolutionary breadth of these strategies has been restricted by the limited number of speci ...[more]

PMID: 26052941

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Project description:Iron (Fe) availability restricts diatom growth and primary production in large areas of the oceans. It is a challenge to assess the bulk Fe nutritional health of natural diatom populations, since species can differ in their physiological and molecular responses to Fe limitation. We assayed expression of selected genes in diatoms from the Thalassiosira genus to assess their potential utility as species-specific molecular markers to indicate Fe status in natural diatom assemblages. In this study, we compared the expression of the photosynthetic genes encoding ferredoxin (a Fe-requiring protein) and flavodoxin (a Fe-free protein) in culture experiments with Fe replete and Fe stressed Thalassiosira pseudonana (CCMP 1335) isolated from coastal waters and Thalassiosira weissflogii (CCMP 1010) isolated from the open ocean. In T. pseudonana, expression of flavodoxin and ferredoxin genes were not sensitive to Fe status but were found to display diel periodicities. In T. weissflogii, expression of flavodoxin was highly responsive to iron levels and was only detectable when cultures were Fe limited. Flavodoxin genes have been duplicated in most diatoms with available genome data and we show that T. pseudonana has lost its copy related to the Fe-responsive copy in T. weissflogii. We also examined the expression of genes for a putative high affinity, copper (Cu)-dependent Fe uptake system in T. pseudonana. Our results indicate that genes encoding putative Cu transporters, a multi-Cu oxidase, and a Fe reductase are not linked to Fe status. The expression of a second putative Fe reductase increased in Fe limited cultures, but this gene was also highly expressed in Fe replete cultures, indicating it may not be a useful marker in the field. Our findings highlight that Fe metabolism may differ among diatoms even within a genus and show a need to validate responses in different species as part of the development pipeline for genetic markers of Fe status in field populations.

Project description:The generation of large immune gene families is often driven by evolutionary pressure exerted on host genomes by their pathogens, which has been described as the immunological arms race. The SpTransformer (SpTrf) gene family from the California purple sea urchin, Strongylocentrotus purpuratus, is upregulated upon immune challenge and encodes the SpTrf proteins that interact with pathogens during an immune response. Native SpTrf proteins bind both bacteria and yeast, and augment phagocytosis of a marine Vibrio, while a recombinant SpTrf protein (rSpTrf-E1) binds a subset of pathogens and a range of pathogen associated molecular patterns. In the sequenced sea urchin genome, there are four SpTrf gene clusters for a total of 17 genes. Here, we report an in-depth analysis of these genes to understand the sequence complexities of this family, its genomic structure, and to derive a putative evolutionary history for the formation of the gene clusters. We report a detailed characterization of gene structure including the intron type and UTRs with conserved transcriptional start sites, the start codon and multiple stop codons, and locations of polyadenylation signals. Phylogenetic and percent mismatch analyses of the genes and the intergenic regions allowed us to predict the last common ancestral SpTrf gene and a theoretical evolutionary history of the gene family. The appearance of the gene clusters from the theoretical ancestral gene may have been driven by multiple duplication and deletion events of regions containing SpTrf genes. Duplications and ectopic insertion events, indels, and point mutations in the exons likely resulted in the extant genes and family structure. This theoretical evolutionary history is consistent with the involvement of these genes in the arms race in responses to pathogens and suggests that the diversification of these genes and their encoded proteins have been selected for based on the survival benefits of pathogen binding and host protection.

Dataset Information

Diversity and Evolutionary History of Iron Metabolism Genes in Diatoms.

Publications

Diversity and Evolutionary History of Iron Metabolism Genes in Diatoms.

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