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Title: Specialized proteomic responses and an ancient photoprotection mechanism sustain marine green algal growth during phosphate limitation

Abstract

Marine algae perform approximately half of global carbon fixation, but their growth is often limited by availability of phosphate or other nutrients1,2. As oceans warm, the area of phosphate-limited surface waters is predicted to increase, resulting in ocean desertification3,4. Understanding the responses of key eukaryotic phytoplankton to nutrient limitation is therefore critical5,6. We used advanced photo-bioreactors to investigate how the widespread green alga Micromonas commoda grows under transitions from replete nutrients to chronic phosphate limitation and subsequent relief, analyzing photosystem changes and broad cellular responses using proteomics, transcriptomics and biophysical measurements. We find that physiological and protein expression responses previously attributed to stress are critical to supporting stable exponential growth when phosphate is limiting. Unexpectedly, the abundance of most proteins involved in light-harvesting does not change, but an ancient light-harvesting related protein, LHCSR, is induced and dissipates damaging excess absorbed light as heat during P-limitation. Concurrently, a suite of uncharacterized proteins with narrow phylogenetic distributions increase multifold. Notably, of the proteins that exhibit significant changes, 70% are not differentially expressed at the mRNA transcript level, highlighting the importance of post-transcriptional processes in microbial eukaryotes. Nevertheless, transcript-protein pairs with concordant changes were identified that will enable more robust interpretation of eukaryoticmore » phytoplankton responses in the field from metatranscriptomic studies. Our results show P-limited Micromonas responds quickly to a fresh pulse of phosphate by rapidly increasing replication and that the protein network associated with this ability is composed of both conserved and phylogenetically recent proteome systems that promote dynamic phosphate homeostasis. That an ancient mechanism for mitigating light-stress is central to sustaining growth throughout extended periods of phosphate limitation highlights possible interactive effects, arising from multiple stressors under ocean change, which could reduce the efficacy of algal strategies for optimizing marine photosynthesis.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo; ; ; ; ORCiD logo; ; ORCiD logo
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1503539
Report Number(s):
PNNL-SA-135227
Journal ID: ISSN 2058-5276
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 3; Journal Issue: 7; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
marine algae, phosphate, proteomics, ocean warming

Citation Formats

Guo, Jian, Wilken, Susanne, Jimenez, Valeria, Choi, Chang Jae, Ansong, Charles, Dannebaum, Richard, Sudek, Lisa, Milner, David S., Bachy, Charles, Reistetter, Emily Nahas, Elrod, Virginia A., Klimov, Denis, Purvine, Samuel O., Wei, Chia-Lin, Kunde-Ramamoorthy, Govindarajan, Richards, Thomas A., Goodenough, Ursula, Smith, Richard D., Callister, Stephen J., and Worden, Alexandra Z. Specialized proteomic responses and an ancient photoprotection mechanism sustain marine green algal growth during phosphate limitation. United States: N. p., 2018. Web. doi:10.1038/s41564-018-0178-7.
Guo, Jian, Wilken, Susanne, Jimenez, Valeria, Choi, Chang Jae, Ansong, Charles, Dannebaum, Richard, Sudek, Lisa, Milner, David S., Bachy, Charles, Reistetter, Emily Nahas, Elrod, Virginia A., Klimov, Denis, Purvine, Samuel O., Wei, Chia-Lin, Kunde-Ramamoorthy, Govindarajan, Richards, Thomas A., Goodenough, Ursula, Smith, Richard D., Callister, Stephen J., & Worden, Alexandra Z. Specialized proteomic responses and an ancient photoprotection mechanism sustain marine green algal growth during phosphate limitation. United States. doi:10.1038/s41564-018-0178-7.
Guo, Jian, Wilken, Susanne, Jimenez, Valeria, Choi, Chang Jae, Ansong, Charles, Dannebaum, Richard, Sudek, Lisa, Milner, David S., Bachy, Charles, Reistetter, Emily Nahas, Elrod, Virginia A., Klimov, Denis, Purvine, Samuel O., Wei, Chia-Lin, Kunde-Ramamoorthy, Govindarajan, Richards, Thomas A., Goodenough, Ursula, Smith, Richard D., Callister, Stephen J., and Worden, Alexandra Z. Mon . "Specialized proteomic responses and an ancient photoprotection mechanism sustain marine green algal growth during phosphate limitation". United States. doi:10.1038/s41564-018-0178-7.
@article{osti_1503539,
title = {Specialized proteomic responses and an ancient photoprotection mechanism sustain marine green algal growth during phosphate limitation},
author = {Guo, Jian and Wilken, Susanne and Jimenez, Valeria and Choi, Chang Jae and Ansong, Charles and Dannebaum, Richard and Sudek, Lisa and Milner, David S. and Bachy, Charles and Reistetter, Emily Nahas and Elrod, Virginia A. and Klimov, Denis and Purvine, Samuel O. and Wei, Chia-Lin and Kunde-Ramamoorthy, Govindarajan and Richards, Thomas A. and Goodenough, Ursula and Smith, Richard D. and Callister, Stephen J. and Worden, Alexandra Z.},
abstractNote = {Marine algae perform approximately half of global carbon fixation, but their growth is often limited by availability of phosphate or other nutrients1,2. As oceans warm, the area of phosphate-limited surface waters is predicted to increase, resulting in ocean desertification3,4. Understanding the responses of key eukaryotic phytoplankton to nutrient limitation is therefore critical5,6. We used advanced photo-bioreactors to investigate how the widespread green alga Micromonas commoda grows under transitions from replete nutrients to chronic phosphate limitation and subsequent relief, analyzing photosystem changes and broad cellular responses using proteomics, transcriptomics and biophysical measurements. We find that physiological and protein expression responses previously attributed to stress are critical to supporting stable exponential growth when phosphate is limiting. Unexpectedly, the abundance of most proteins involved in light-harvesting does not change, but an ancient light-harvesting related protein, LHCSR, is induced and dissipates damaging excess absorbed light as heat during P-limitation. Concurrently, a suite of uncharacterized proteins with narrow phylogenetic distributions increase multifold. Notably, of the proteins that exhibit significant changes, 70% are not differentially expressed at the mRNA transcript level, highlighting the importance of post-transcriptional processes in microbial eukaryotes. Nevertheless, transcript-protein pairs with concordant changes were identified that will enable more robust interpretation of eukaryotic phytoplankton responses in the field from metatranscriptomic studies. Our results show P-limited Micromonas responds quickly to a fresh pulse of phosphate by rapidly increasing replication and that the protein network associated with this ability is composed of both conserved and phylogenetically recent proteome systems that promote dynamic phosphate homeostasis. That an ancient mechanism for mitigating light-stress is central to sustaining growth throughout extended periods of phosphate limitation highlights possible interactive effects, arising from multiple stressors under ocean change, which could reduce the efficacy of algal strategies for optimizing marine photosynthesis.},
doi = {10.1038/s41564-018-0178-7},
journal = {Nature Microbiology},
issn = {2058-5276},
number = 7,
volume = 3,
place = {United States},
year = {2018},
month = {6}
}

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