Abstract
BackgroundBiogeochemical elemental cycling is driven by primary production of biomass via phototrophic phytoplankton growth, with 40% of marine productivity being assigned to diatoms. Phytoplankton growth is widely limited by the availability of iron, an essential component of the photosynthetic apparatus. The oceanic diatom Thalassiosira oceanica shows a remarkable tolerance to low-iron conditions and was chosen as a model for deciphering the cellular response upon shortage of this essential micronutrient.ResultsThe combined efforts in genomics, transcriptomics and proteomics reveal an unexpected metabolic flexibility in response to iron availability for T. oceanica CCMP1005. The complex response comprises cellular retrenchment as well as remodeling of bioenergetic pathways, where the abundance of iron-rich photosynthetic proteins is lowered, whereas iron-rich mitochondrial proteins are preserved. As a consequence of iron deprivation, the photosynthetic machinery undergoes a remodeling to adjust the light energy utilization with the overall decrease in photosynthetic electron transfer complexes.ConclusionsBeneficial adaptations to low-iron environments include strategies to lower the cellular iron requirements and to enhance iron uptake. A novel contribution enhancing iron economy of phototrophic growth is observed with the iron-regulated substitution of three metal-containing fructose-bisphosphate aldolases involved in metabolic conversion of carbohydrates for enzymes that do not contain metals. Further, our data identify candidate components of a high-affinity iron-uptake system, with several of the involved genes and domains originating from duplication events. A high genomic plasticity, as seen from the fraction of genes acquired through horizontal gene transfer, provides the platform for these complex adaptations to a low-iron world.
Highlights
Biogeochemical elemental cycling is driven by primary production of biomass via phototrophic phytoplankton growth, with 40% of marine productivity being assigned to diatoms
Characteristics of the T. oceanica genome The genome of the centric diatom T. oceanica CCMP1005 (Figure 1) was de novo assembled from 725 Mb of Roche 454 sequence read information, generated using nuclear genomic DNA of an axenic clonal culture as substrate [14]
The gene finder tool AUGUSTUS [16] predicts 37,921 protein gene models that cluster into a non-redundant set of 29,306 models including pseudogenes and short open reading frame (ORF); 10,109 models have BLAST hits to the National Center for Biotechnology Information (NCBI) nr protein database at a conservative E-value cutoff of 1.0E-30 and are more indicative of the expected true protein-coding gene number
Summary
Biogeochemical elemental cycling is driven by primary production of biomass via phototrophic phytoplankton growth, with 40% of marine productivity being assigned to diatoms. Diatoms often dominate phytoplankton communities in nutrient-rich ecosystems, members of this diverse group are adapted to survive and persist in nutrient-limited conditions. Iron is an essential nutrient for all organisms and in particular for photoautotrophic organisms. Numerous large-scale iron fertilization experiments have confirmed that iron is the limiting nutrient in HNLC regions [3]. Phytoplankton blooms induced by iron fertilization were dominated by diatoms and carbon export to the deep-sea floor could be observed in some cases. The strong response of diatoms to the input of iron in HNLC regions has been a motivation for exploring large-scale iron fertilization as a possible bioengineering strategy to sequester CO2 into the ocean in HNLC regions, which are otherwise rich in macronutrients
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