Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation

PLoS Genet. 2016 Dec 14;12(12):e1006490. doi: 10.1371/journal.pgen.1006490. eCollection 2016 Dec.

Abstract

Environmental fluctuations affect distribution, growth and abundance of diatoms in nature, with iron (Fe) availability playing a central role. Studies on the response of diatoms to low Fe have either utilized continuous (24 hr) illumination or sampled a single time of day, missing any temporal dynamics. We profiled the physiology, metabolite composition, and global transcripts of the pennate diatom Phaeodactylum tricornutum during steady-state growth at low, intermediate, and high levels of dissolved Fe over light:dark cycles, to better understand fundamental aspects of genetic control of physiological acclimation to growth under Fe-limitation. We greatly expand the catalog of genes involved in the low Fe response, highlighting the importance of intracellular trafficking in Fe-limited diatoms. P. tricornutum exhibited transcriptomic hallmarks of slowed growth leading to prolonged periods of cell division/silica deposition, which could impact biogeochemical carbon sequestration in Fe-limited regions. Light harvesting and ribosome biogenesis transcripts were generally reduced under low Fe while transcript levels for genes putatively involved in the acquisition and recycling of Fe were increased. We also noted shifts in expression towards increased synthesis and catabolism of branched chain amino acids in P. tricornutum grown at low Fe whereas expression of genes involved in central core metabolism were relatively unaffected, indicating that essential cellular function is protected. Beyond the response of P. tricornutum to low Fe, we observed major coordinated shifts in transcript control of primary and intermediate metabolism over light:dark cycles which contribute to a new view of the significance of distinctive diatom pathways, such as mitochondrial glycolysis and the ornithine-urea cycle. This study provides new insight into transcriptional modulation of diatom physiology and metabolism across light:dark cycles in response to Fe availability, providing mechanistic understanding for the ability of diatoms to remain metabolically poised to respond quickly to Fe input and revealing strategies underlying their ecological success.

MeSH terms

  • Cell Cycle / drug effects
  • Cell Cycle / genetics
  • Cell Division / drug effects
  • Cell Division / genetics
  • Chloroplasts / genetics
  • Diatoms / drug effects
  • Diatoms / growth & development
  • Diatoms / metabolism*
  • Gene Expression
  • Iron / metabolism*
  • Iron / pharmacology
  • Metabolic Networks and Pathways / genetics
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Photoperiod*
  • Protein Biosynthesis / drug effects
  • Transcriptome / genetics*

Substances

  • Iron

Grant support

This work was supported by National Science Foundation (www.nsf.gov) grants MCB-1024913 (AEA and CLD) and OCE-0727997 and OCE-0727733 (AEA and ABK), United States Department of Energy Genomics Science program (http://genomicscience.energy.gov) grants (DE-SC00006719 and DE-SC0008593; AEA and CLD) and Gordon and Betty Moore Foundation (https://www.moore.org) grant GBMF3828 (AEA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.