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

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 relativelymore » 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.« less

Authors:
ORCiD logo [1];  [2]; ORCiD logo [3];  [4];  [4];  [4];  [3];  [4];  [5];  [5];  [1]
  1. Univ. of California, San Diego, CA (United States). Integrative Oceanography Division. Scripps Inst. of Oceanography; J. Craig Venter Inst., La Jolla, CA (United States)
  2. J. Craig Venter Inst., La Jolla, CA (United States); California State Univ., Bakersfield, CA (United States). Dept. of Biology
  3. Rutgers Univ., Newark, NJ (United States). Dept. of Earth and Environmental Sciences
  4. J. Craig Venter Inst., La Jolla, CA (United States)
  5. Max Planck Inst. of Molecular Plant Physiology, Potsdam (Germany)
Publication Date:
Research Org.:
J. Craig Venter Inst., La Jolla, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF); Gordon and Betty Moore Foundation (United States)
OSTI Identifier:
1335713
Alternate Identifier(s):
OSTI ID: 1423794
Grant/Contract Number:  
SC0008593; SC0006719; MCB-1024913; OCE-0727997; OCE-0727733; GBMF3828
Resource Type:
Journal Article: Published Article
Journal Name:
PLoS Genetics
Additional Journal Information:
Journal Volume: 12; Journal Issue: 12; Journal ID: ISSN 1553-7404
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; diatoms; mitochondria; cell cycle and cell division; gene expression; biosynthesis; chloroplasts; urea; metabolic pathways

Citation Formats

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., and Allen, Andrew E. Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation. United States: N. p., 2016. Web. doi:10.1371/journal.pgen.1006490.
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. Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation. United States. doi:10.1371/journal.pgen.1006490.
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., and Allen, Andrew E. Wed . "Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation". United States. doi:10.1371/journal.pgen.1006490.
@article{osti_1335713,
title = {Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation},
author = {Smith, Sarah R. and Gillard, Jeroen T. F. and Kustka, Adam B. and McCrow, John P. and Badger, Jonathan H. and Zheng, Hong and New, Ashley M. and Dupont, Chris L. and Obata, Toshihiro and Fernie, Alisdair R. and Allen, Andrew E.},
abstractNote = {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.},
doi = {10.1371/journal.pgen.1006490},
journal = {PLoS Genetics},
number = 12,
volume = 12,
place = {United States},
year = {Wed Dec 14 00:00:00 EST 2016},
month = {Wed Dec 14 00:00:00 EST 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1371/journal.pgen.1006490

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Cited by: 7 works
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Works referenced in this record:

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