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Title: Identifying Aspects of the Post-Transcriptional Program Governing the Proteome of the Green Alga Micromonas pusilla

Abstract

Micromonas is a unicellular green alga that belongs to the prasinophytes, a sister lineage to land plants. This picoeukaryotic (<2 μm diameter) alga is widespread in the marine environment but still not understood at the cellular level. Here, we examine the mRNA and protein level changes that take place over the course of the day-night cycle using mid-exponential nutrient replete cultures of Micromonas pusilla CCMP1545 grown and analyzed in biological triplicate. During the experiment, samples were collected at key transition points during the diel for evaluation using high-throughput LC-MS proteomics. We also sequenced matched mRNA samples from the same time points, using pair-ended directional Illumina RNA-Seq to investigate the dynamics and relationship between the mRNA and protein expression programs of M. pusilla. Similar to a prior study of the marine cyanobacterium Prochlorococcus, we found significant divergence in the mRNA and proteomics expression dynamics in response to the light:dark cycle. Additionally, expressional responses of genes and the proteins they encoded could also be variable within the same metabolic pathway, such as the oxygenic photosynthesis pathway. A regression framework was used to predict protein levels using both mRNA expression and gene-specific sequence-based features. Several features in the genome sequence were found tomore » influence protein abundance including the codon usage and the length of the 3’ UTR. Collectively, our studies provide insights into the regulation of the proteome over a diel as relationships between the transcriptional and translational programs in the widespread marine green alga Micromonas.« less

Authors:
 [1];  [2];  [2];  [3];  [3];  [2];  [4];  [4];  [3];  [3];  [1];  [5];  [6]
  1. Univ. of California, Santa Cruz, CA (United States)
  2. Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States); Univ. of California, Santa Cruz, CA (United States); Canadian Inst. for Advanced Research, Toronto (Canada)
  6. Queen's Univ., Belfast, Northern Ireland (United Kingdom)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1342328
Report Number(s):
PNNL-SA-115265
Journal ID: ISSN 1932-6203; 47672; KP1601030
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 11; Journal Issue: 7; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Environmental Molecular Sciences Laboratory; protein expression; messenger RNA; transcription factors; protein abundance; proteomic databases; proteomes; algae; photosynthesis

Citation Formats

Waltman, Peter H., Guo, Jian, Reistetter, Emily Nahas, Purvine, Samuel, Ansong, Charles K., van Baren, Marijke J., Wong, Chee-Hong, Wei, Chia-Lin, Smith, Richard D., Callister, Stephen J., Stuart, Joshua M., Worden, Alexandra Z., and Mills, Ken. Identifying Aspects of the Post-Transcriptional Program Governing the Proteome of the Green Alga Micromonas pusilla. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0155839.
Waltman, Peter H., Guo, Jian, Reistetter, Emily Nahas, Purvine, Samuel, Ansong, Charles K., van Baren, Marijke J., Wong, Chee-Hong, Wei, Chia-Lin, Smith, Richard D., Callister, Stephen J., Stuart, Joshua M., Worden, Alexandra Z., & Mills, Ken. Identifying Aspects of the Post-Transcriptional Program Governing the Proteome of the Green Alga Micromonas pusilla. United States. https://doi.org/10.1371/journal.pone.0155839
Waltman, Peter H., Guo, Jian, Reistetter, Emily Nahas, Purvine, Samuel, Ansong, Charles K., van Baren, Marijke J., Wong, Chee-Hong, Wei, Chia-Lin, Smith, Richard D., Callister, Stephen J., Stuart, Joshua M., Worden, Alexandra Z., and Mills, Ken. 2016. "Identifying Aspects of the Post-Transcriptional Program Governing the Proteome of the Green Alga Micromonas pusilla". United States. https://doi.org/10.1371/journal.pone.0155839. https://www.osti.gov/servlets/purl/1342328.
@article{osti_1342328,
title = {Identifying Aspects of the Post-Transcriptional Program Governing the Proteome of the Green Alga Micromonas pusilla},
author = {Waltman, Peter H. and Guo, Jian and Reistetter, Emily Nahas and Purvine, Samuel and Ansong, Charles K. and van Baren, Marijke J. and Wong, Chee-Hong and Wei, Chia-Lin and Smith, Richard D. and Callister, Stephen J. and Stuart, Joshua M. and Worden, Alexandra Z. and Mills, Ken},
abstractNote = {Micromonas is a unicellular green alga that belongs to the prasinophytes, a sister lineage to land plants. This picoeukaryotic (<2 μm diameter) alga is widespread in the marine environment but still not understood at the cellular level. Here, we examine the mRNA and protein level changes that take place over the course of the day-night cycle using mid-exponential nutrient replete cultures of Micromonas pusilla CCMP1545 grown and analyzed in biological triplicate. During the experiment, samples were collected at key transition points during the diel for evaluation using high-throughput LC-MS proteomics. We also sequenced matched mRNA samples from the same time points, using pair-ended directional Illumina RNA-Seq to investigate the dynamics and relationship between the mRNA and protein expression programs of M. pusilla. Similar to a prior study of the marine cyanobacterium Prochlorococcus, we found significant divergence in the mRNA and proteomics expression dynamics in response to the light:dark cycle. Additionally, expressional responses of genes and the proteins they encoded could also be variable within the same metabolic pathway, such as the oxygenic photosynthesis pathway. A regression framework was used to predict protein levels using both mRNA expression and gene-specific sequence-based features. Several features in the genome sequence were found to influence protein abundance including the codon usage and the length of the 3’ UTR. Collectively, our studies provide insights into the regulation of the proteome over a diel as relationships between the transcriptional and translational programs in the widespread marine green alga Micromonas.},
doi = {10.1371/journal.pone.0155839},
url = {https://www.osti.gov/biblio/1342328}, journal = {PLoS ONE},
issn = {1932-6203},
number = 7,
volume = 11,
place = {United States},
year = {Tue Jul 19 00:00:00 EDT 2016},
month = {Tue Jul 19 00:00:00 EDT 2016}
}

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Cited by: 7 works
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Works referenced in this record:

PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees
journal, November 2012


A dynamic model of proteome changes reveals new roles for transcript alteration in yeast
journal, January 2011


Photosynthetic Genes of Petunia (Mitchell) Are Differentially Expressed during the Diurnal Cycle
journal, March 1989


DAnTE: a statistical tool for quantitative analysis of -omics data
journal, May 2008


Marine algae and land plants share conserved phytochrome signaling systems
journal, September 2014


Global quantification of mammalian gene expression control
journal, May 2011


InterProScan: protein domains identifier
journal, July 2005


The nucleolar RNA methyltransferase Misu (NSun2) is required for mitotic spindle stability
journal, July 2009


Correlation between stability of a protein and its dipeptide composition: a novel approach for predicting in vivo stability of a protein from its primary sequence
journal, January 1990


Decon2LS: An open-source software package for automated processing and visualization of high resolution mass spectrometry data
journal, January 2009


A multi-omic analysis of human naïve CD4+ T cells
journal, November 2015


TopHat: discovering splice junctions with RNA-Seq
journal, March 2009


Proteome-Wide Analysis and Diel Proteomic Profiling of the Cyanobacterium Arthrospira platensis PCC 8005
journal, June 2014


Stochastic gradient boosting
journal, February 2002


InterProScan - an integration platform for the signature-recognition methods in InterPro
journal, September 2001


Pathway Tools version 13.0: integrated software for pathway/genome informatics and systems biology
journal, December 2009


Correlation of mRNA and protein in complex biological samples
journal, October 2009


Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae
journal, March 2003


Transcriptome and Proteome Dynamics of a Light-Dark Synchronized Bacterial Cell Cycle
journal, August 2012


Cell cycle regulated expression of nucleolar antigen P120 in normal and transformed human fibroblasts
journal, January 1993


Green algae and the origin of land plants
journal, October 2004


Glycerolipids in photosynthesis: Composition, synthesis and trafficking
journal, April 2014


The anatomy of microbial cell state transitions in response to oxygen
journal, September 2007


Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
journal, September 2005


Gene Ontology: tool for the unification of biology
journal, May 2000


Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012


KEGG for integration and interpretation of large-scale molecular data sets
journal, November 2011


Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags
journal, August 2002


Analysis of Biostimulated Microbial Communities from Two Field Experiments Reveals Temporal and Spatial Differences in Proteome Profiles
journal, December 2010


An introduction to multivariate adaptive regression splines
journal, September 1995


Large-scale gene function analysis with the PANTHER classification system
journal, July 2013


A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
journal, January 2003


The use of DAPI for identifying and counting aquatic microflora1
journal, September 1980


Purification and Characterization of Class-I and Class-II Fructose-1,6-bisphosphate Aldolases from the Cyanobacterium Synechocystis sp. PCC 6803
journal, March 2003


Integrative analysis of RNA, translation, and protein levels reveals distinct regulatory variation across humans
journal, August 2015


Dynamic proteomic profiling of a unicellular cyanobacterium Cyanothece ATCC51142 across light-dark diurnal cycles
journal, January 2011


Structure and Function of Sphingosine-1-Phosphate Lyase, a Key Enzyme of Sphingolipid Metabolism
journal, August 2010


System wide analyses have underestimated protein abundances and the importance of transcription in mammals
journal, January 2014


Open-source machine learning: R meets Weka
journal, May 2008


Characterizing Microbial Community and Geochemical Dynamics at Hydrothermal Vents Using Osmotically Driven Continuous Fluid Samplers
journal, April 2013


Posttranscriptional Expression Regulation: What Determines Translation Rates?
journal, January 2007


AU-rich elements and associated factors: are there unifying principles?
journal, December 2005


Circadian Rhythms Confer a Higher Level of Fitness to Arabidopsis Plants
journal, May 2002


Mapping the dynamic organization of the nuclear pore complex inside single living cells
journal, October 2004


The ENZYME database in 2000
journal, January 2000


The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications
journal, January 1987


Correlation between Protein and mRNA Abundance in Yeast
journal, March 1999


Sequence signatures and mRNA concentration can explain two‐thirds of protein abundance variation in a human cell line
journal, January 2010


The nuclear pore complex protein ALADIN is anchored via NDC1 but not via POM121 and GP210 in the nuclear envelope
journal, December 2009


Post-Transcriptional Regulation of Iron Homeostasis in Saccharomyces cerevisiae
journal, July 2013


Crystal Structure of Diaminopimelate Epimerase from Arabidopsis thaliana, an Amino Acid Racemase Critical for l-Lysine Biosynthesis
journal, January 2009


Smallest Algae Thrive As the Arctic Ocean Freshens
journal, October 2009


Comparative proteomic and transcriptomic profiling of the fission yeast Schizosaccharomyces pombe
journal, January 2007


Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans
journal, April 2009


Protein Expression Regulation under Oxidative Stress
journal, September 2011


Galaxy: A platform for interactive large-scale genome analysis
journal, September 2005


Boosting Algorithms: Regularization, Prediction and Model Fitting
journal, November 2007


Plant Circadian Rhythms
journal, April 2006


Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence
journal, July 2000


Role of HuD and other RNA-binding proteins in neural development and plasticity
journal, March 2002


Regularization Paths for Generalized Linear Models via Coordinate Descent
journal, January 2010


Spectral Probabilities and Generating Functions of Tandem Mass Spectra: A Strike against Decoy Databases
journal, August 2008


Plant sphingolipids: decoding the enigma of the Sphinx: Tansley review
journal, December 2009


Delayed Correlation of mRNA and Protein Expression in Rapamycin-treated Cells and a Role for Ggc1 in Cellular Sensitivity to Rapamycin
journal, November 2009


AREsite: a database for the comprehensive investigation of AU-rich elements
journal, November 2010


VIPER: an advanced software package to support high-throughput LC-MS peptide identification
journal, June 2007


PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes
journal, June 2003


Insights into the regulation of protein abundance from proteomic and transcriptomic analyses
journal, March 2012


Change in flagellar beat frequency of Chlamydomonas in response to light
journal, January 1982


Cell cycle regulated expression of nucleolar antigen P120 in normal and transformed human fibroblasts
journal, January 1993


Role of HuD and other RNA-binding proteins in neural development and plasticity
journal, March 2002


Augmenting Product Defect Surveillance Through Web Crawling and Machine Learning in Singapore
journal, June 2021


Glycerolipids in photosynthesis: Composition, synthesis and trafficking
journal, April 2014


The nuclear pore complex protein ALADIN is anchored via NDC1 but not via POM121 and GP210 in the nuclear envelope
journal, December 2009


Correlation of mRNA and protein in complex biological samples
journal, October 2009


Crystal Structure of Diaminopimelate Epimerase from Arabidopsis thaliana, an Amino Acid Racemase Critical for l-Lysine Biosynthesis
journal, January 2009


Structure and Function of Sphingosine-1-Phosphate Lyase, a Key Enzyme of Sphingolipid Metabolism
journal, August 2010


AU-rich elements: characterization and importance in mRNA degradation
journal, November 1995


The WD repeat: a common architecture for diverse functions
journal, May 1999


Analysis of Biostimulated Microbial Communities from Two Field Experiments Reveals Temporal and Spatial Differences in Proteome Profiles
journal, December 2010


Characterizing Microbial Community and Geochemical Dynamics at Hydrothermal Vents Using Osmotically Driven Continuous Fluid Samplers
journal, April 2013


Spectral Probabilities and Generating Functions of Tandem Mass Spectra: A Strike against Decoy Databases
journal, August 2008


A dynamic model of proteome changes reveals new roles for transcript alteration in yeast
journal, January 2011


Comparative proteomic and transcriptomic profiling of the fission yeast Schizosaccharomyces pombe
journal, January 2007


Large-scale gene function analysis with the PANTHER classification system
journal, July 2013


Insights into the regulation of protein abundance from proteomic and transcriptomic analyses
journal, March 2012


Transcriptomic mapping uncovers Purkinje neuron plasticity driving learning
journal, May 2022


Mir34a constrains pancreatic carcinogenesis
journal, June 2020


Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae
journal, March 2003


Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans
journal, April 2009


New technology may reveal mechanisms of radiation resistance in Deinococcus radiodurans
journal, August 2002


Pathway Tools version 13.0: integrated software for pathway/genome informatics and systems biology
journal, December 2009


InterProScan - an integration platform for the signature-recognition methods in InterPro
journal, September 2001


The Pathway Tools software
journal, July 2002


VIPER: an advanced software package to support high-throughput LC-MS peptide identification
journal, June 2007


DAnTE: a statistical tool for quantitative analysis of -omics data
journal, May 2008


TopHat: discovering splice junctions with RNA-Seq
journal, March 2009


The ENZYME database in 2000
journal, January 2000


AU-rich elements and associated factors: are there unifying principles?
journal, December 2005


AREsite: a database for the comprehensive investigation of AU-rich elements
journal, November 2010


KEGG for integration and interpretation of large-scale molecular data sets
journal, November 2011


Purification and Characterization of Class-I and Class-II Fructose-1,6-bisphosphate Aldolases from the Cyanobacterium Synechocystis sp. PCC 6803
journal, March 2003


Correlation between stability of a protein and its dipeptide composition: a novel approach for predicting in vivo stability of a protein from its primary sequence
journal, January 1990


Galaxy: A platform for interactive large-scale genome analysis
journal, September 2005


The anatomy of microbial cell state transitions in response to oxygen
journal, September 2007


Circadian Rhythms Confer a Higher Level of Fitness to Arabidopsis Plants
journal, May 2002


Photosynthetic Genes of Petunia (Mitchell) Are Differentially Expressed during the Diurnal Cycle
journal, March 1989


Plant Circadian Rhythms
journal, April 2006


Plant sphingolipids: decoding the enigma of the Sphinx: Tansley review
journal, December 2009


Smallest Algae Thrive As the Arctic Ocean Freshens
journal, October 2009


Translational efficiency is regulated by the length of the 3' untranslated region.
journal, January 1996


An introduction to multivariate adaptive regression splines
journal, September 1995


Decon2LS: An open-source software package for automated processing and visualization of high resolution mass spectrometry data
journal, January 2009


Dynamic proteomic profiling of a unicellular cyanobacterium Cyanothece ATCC51142 across light-dark diurnal cycles
journal, January 2011


A multi-omic analysis of human naïve CD4+ T cells
journal, November 2015


Boosting Algorithms: Regularization, Prediction and Model Fitting
journal, November 2007


Posttranscriptional Expression Regulation: What Determines Translation Rates?
journal, January 2007


Transcriptome and Proteome Dynamics of a Light-Dark Synchronized Bacterial Cell Cycle
journal, August 2012


Proteome-Wide Analysis and Diel Proteomic Profiling of the Cyanobacterium Arthrospira platensis PCC 8005
journal, June 2014


Post-Transcriptional Regulation of Iron Homeostasis in Saccharomyces cerevisiae
journal, July 2013


Green algae and the origin of land plants
journal, October 2004


Works referencing / citing this record:

Spatial Variability of Picoeukaryotic Communities in the Mariana Trench
journal, October 2018


Spatial Variability of Picoeukaryotic Communities in the Mariana Trench
journal, October 2018


Responses of the picoprasinophyte Micromonas commoda to light and ultraviolet stress
journal, March 2017