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

Smith, Sarah R.; Gillard, Jeroen T. F.; Kustka, Adam B.; McCrow, John P.; Badger, Jonathan H.; Zheng, Hong; New, Ashley M.; Dupont, Chris L.; Obata, Toshihiro; Fernie, Alisdair R.; Allen, Andrew E.; Richardson, ed., Paul M.

doi:10.1371/journal.pgen.1006490

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

Journal Article · Wed Dec 14 00:00:00 EST 2016 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1006490· OSTI ID:1335713

; Gillard, Jeroen T. F.;

; McCrow, John P.; Badger, Jonathan H.; Zheng, Hong; New, Ashley M.; Dupont, Chris L.; Obata, Toshihiro; Fernie, Alisdair R.; Allen, Andrew E.; Richardson, ed., Paul M.

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.

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Research Organization:: J. Craig Venter Inst., La Jolla, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Gordon and Betty Moore Foundation (United States)

Grant/Contract Number:: SC0006719; SC0008593; MCB-1024913; OCE-0727997; OCE-0727733; GBMF3828

OSTI ID:: 1335713

Alternate ID(s):: OSTI ID: 1423794

Journal Information:: PLoS Genetics, Journal Name: PLoS Genetics Vol. 12 Journal Issue: 12; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 69 works

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