The Importance of Protein Phosphorylation for Signaling and Metabolism in Response to Diel Light Cycling and Nutrient Availability in a Marine Diatom
Abstract
Diatoms are major contributors to global primary production and their populations in the modern oceans are affected by availability of iron, nitrogen, phosphate, silica, and other trace metals, vitamins, and infochemicals. However, little is known about the role of phosphorylation in diatoms and its role in regulation and signaling. We report a total of 2759 phosphorylation sites on 1502 proteins detected in Phaeodactylum tricornutum. Conditionally phosphorylated peptides were detected at low iron (n = 108), during the diel cycle (n = 149), and due to nitrogen availability (n = 137). Through a multi-omic comparison of transcript, protein, phosphorylation, and protein homology, we identify numerous proteins and key cellular processes that are likely under control of phospho-regulation. We show that phosphorylation regulates: (1) carbon retrenchment and reallocation during growth under low iron, (2) carbon flux towards lipid biosynthesis after the lights turn on, (3) coordination of transcription and translation over the diel cycle and (4) in response to nitrogen depletion. We also uncover phosphorylation sites for proteins that play major roles in diatom Fe sensing and utilization, including flavodoxin and phytotransferrin (ISIP2A), as well as identify phospho-regulated stress proteins and kinases. These findings provide much needed insight into the roles ofmore »
- Authors:
-
[1];
[2];
[4];
[6]
- Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography
- J. Craig Venter Inst., Inc., La Jolla, CA (United States). Microbial and Environmental Genomics
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab.
- Univ. of California, San Diego, CA (United States). Dept. of Bioengineering
- Rutgers Univ., New Brunswick, NJ (United States). Dept. of Earth and Environmental Sciences
- Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography; J. Craig Venter Inst., Inc., La Jolla, CA (United States). Microbial and Environmental Genomics
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Gordon and Betty Moore Foundation
- OSTI Identifier:
- 1673586
- Report Number(s):
- PNNL-SA-153917
Journal ID: ISSN 2079-7737
- Grant/Contract Number:
- AC05-76RL01830; SC0006719; SC0008593; MCB-1024913; MCB-1818390; OCE-0727997; OCE-1756884; GBMF3828
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biology
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 7; Journal ID: ISSN 2079-7737
- Publisher:
- MDPI
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; phosphoproteome; nitrogen stress; iron; diel; diatom; signaling
Citation Formats
Tan, Maxine H., Smith, Sarah R., Hixson, Kim K., Tan, Justin, McCarthy, James K., Kustka, Adam B., and Allen, Andrew E. The Importance of Protein Phosphorylation for Signaling and Metabolism in Response to Diel Light Cycling and Nutrient Availability in a Marine Diatom. United States: N. p., 2020.
Web. doi:10.3390/biology9070155.
Tan, Maxine H., Smith, Sarah R., Hixson, Kim K., Tan, Justin, McCarthy, James K., Kustka, Adam B., & Allen, Andrew E. The Importance of Protein Phosphorylation for Signaling and Metabolism in Response to Diel Light Cycling and Nutrient Availability in a Marine Diatom. United States. https://doi.org/10.3390/biology9070155
Tan, Maxine H., Smith, Sarah R., Hixson, Kim K., Tan, Justin, McCarthy, James K., Kustka, Adam B., and Allen, Andrew E. Mon .
"The Importance of Protein Phosphorylation for Signaling and Metabolism in Response to Diel Light Cycling and Nutrient Availability in a Marine Diatom". United States. https://doi.org/10.3390/biology9070155. https://www.osti.gov/servlets/purl/1673586.
@article{osti_1673586,
title = {The Importance of Protein Phosphorylation for Signaling and Metabolism in Response to Diel Light Cycling and Nutrient Availability in a Marine Diatom},
author = {Tan, Maxine H. and Smith, Sarah R. and Hixson, Kim K. and Tan, Justin and McCarthy, James K. and Kustka, Adam B. and Allen, Andrew E.},
abstractNote = {Diatoms are major contributors to global primary production and their populations in the modern oceans are affected by availability of iron, nitrogen, phosphate, silica, and other trace metals, vitamins, and infochemicals. However, little is known about the role of phosphorylation in diatoms and its role in regulation and signaling. We report a total of 2759 phosphorylation sites on 1502 proteins detected in Phaeodactylum tricornutum. Conditionally phosphorylated peptides were detected at low iron (n = 108), during the diel cycle (n = 149), and due to nitrogen availability (n = 137). Through a multi-omic comparison of transcript, protein, phosphorylation, and protein homology, we identify numerous proteins and key cellular processes that are likely under control of phospho-regulation. We show that phosphorylation regulates: (1) carbon retrenchment and reallocation during growth under low iron, (2) carbon flux towards lipid biosynthesis after the lights turn on, (3) coordination of transcription and translation over the diel cycle and (4) in response to nitrogen depletion. We also uncover phosphorylation sites for proteins that play major roles in diatom Fe sensing and utilization, including flavodoxin and phytotransferrin (ISIP2A), as well as identify phospho-regulated stress proteins and kinases. These findings provide much needed insight into the roles of protein phosphorylation in diel cycling and nutrient sensing in diatoms.},
doi = {10.3390/biology9070155},
journal = {Biology},
number = 7,
volume = 9,
place = {United States},
year = {Mon Jul 06 00:00:00 EDT 2020},
month = {Mon Jul 06 00:00:00 EDT 2020}
}
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Figure 1: Summary of the phosphoproteome of P. tricornutum. (a) Proportions of detected phosphoproteins in each KOG class (* indicate significantly enriched groups, ˆ indicate significantly depleted groups). Proteins related to signal transduction mechanisms and RNA processing/modification were significantly enriched for phosphorylation. (b) The majority of phosphoproteins (76%) had onemore »
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