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Title: Evidence-based green algal genomics reveals marine diversity and ancestral characteristics of land plants

Abstract

Prasinophytes are widespread marine green algae that are related to plants. Abundance of the genus Micromonas has reportedly increased in the Arctic due to climate-induced changes. Thus, studies of these organisms are important for marine ecology and understanding Virdiplantae evolution and diversification. We generated evidence-based Micromonas gene models using proteomics and RNA-Seq to improve prasinophyte genomic resources. First, sequences of four chromosomes in the 22 Mb Micromonas pusilla (CCMP1545) genome were finished. Comparison with the finished 21 Mb Micromonas commoda (RCC299) shows they share ≤ 8,142 of ~10,000 protein-encoding genes, depending on the analysis method. Unlike RCC299 and other sequenced eukaryotes, CCMP1545 has two abundant repetitive intron types and a high percent (26%) GC splice donors. Micromonas has more genus-specific protein families (19%) than other genome sequenced prasinophytes (11%). Comparative analyses using predicted proteomes from other prasinophytes reveal proteins likely related to scale formation and ancestral photosynthesis. Our studies also indicate that peptidoglycan (PG) biosynthesis enzymes have been lost in multiple independent events in select prasinophytes and most plants. However, CCMP1545, polar Micromonas CCMP2099 and prasinophytes from other claasses retain the entire PG pathway, like moss and glaucophyte algae. Multiple vascular plants that share a unique bi-domain protein also havemore » the pathway, except the Penicillin-Binding-Protein. Alongside Micromonas experiments using antibiotics that halt bacterial PG biosynthesis, the findings highlight unrecognized phylogenetic complexity in the PG-pathway retention and implicate a role in chloroplast structure of division in several extant Vridiplantae lineages. Extensive differences in gene loss and architecture between related prasinophytes underscore their extensive divergence. PG biosynthesis genes from the cyanobacterial endosymbiont that became the plastid, have been selectively retained in some plants and algae, implying a biological function. As a result, our studies provide robust genomic resources for emerging model algae, advancing knowledge of marine phytoplankton and plant evolution.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [1];  [4];  [1];  [5];  [6];  [6];  [6];  [2];  [2];  [6];  [3];  [7]
  1. Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Hudson Alpha, Huntsville, AL (United States)
  4. Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States); California Inst. of Technology (CalTech), Pasadena, CA (United States)
  5. Univ. of California, La Jolla, San Diego, CA (United States)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  7. Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States); Canadian Institute for Advanced Research, Toronto (Canada)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1337274
Report Number(s):
PNNL-SA-114561
Journal ID: ISSN 1471-2164; 48135; KP1601030
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 17; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Environmental Molecular Sciences Laboratory; GreenCut; Archaeplastida evolution; Viridiplantae; Introner Elements; RNA sequencing; Proteomics; Evidence-based gene models; Peptidoglycan; PPASP

Citation Formats

van Baren, Marijke J., Bachy, Charles, Reistetter, Emily Nahas, Purvine, Samuel O., Grimwood, Jane, Sudek, Sebastian, Yu, Hang, Poirier, Camille, Deerinck, Thomas J., Kuo, Alan, Grigoriev, Igor V., Wong, Chee -Hong, Smith, Richard D., Callister, Stephen J., Wei, Chia -Lin, Schmutz, Jeremy, and Worden, Alexandra Z. Evidence-based green algal genomics reveals marine diversity and ancestral characteristics of land plants. United States: N. p., 2016. Web. doi:10.1186/s12864-016-2585-6.
van Baren, Marijke J., Bachy, Charles, Reistetter, Emily Nahas, Purvine, Samuel O., Grimwood, Jane, Sudek, Sebastian, Yu, Hang, Poirier, Camille, Deerinck, Thomas J., Kuo, Alan, Grigoriev, Igor V., Wong, Chee -Hong, Smith, Richard D., Callister, Stephen J., Wei, Chia -Lin, Schmutz, Jeremy, & Worden, Alexandra Z. Evidence-based green algal genomics reveals marine diversity and ancestral characteristics of land plants. United States. doi:10.1186/s12864-016-2585-6.
van Baren, Marijke J., Bachy, Charles, Reistetter, Emily Nahas, Purvine, Samuel O., Grimwood, Jane, Sudek, Sebastian, Yu, Hang, Poirier, Camille, Deerinck, Thomas J., Kuo, Alan, Grigoriev, Igor V., Wong, Chee -Hong, Smith, Richard D., Callister, Stephen J., Wei, Chia -Lin, Schmutz, Jeremy, and Worden, Alexandra Z. Thu . "Evidence-based green algal genomics reveals marine diversity and ancestral characteristics of land plants". United States. doi:10.1186/s12864-016-2585-6. https://www.osti.gov/servlets/purl/1337274.
@article{osti_1337274,
title = {Evidence-based green algal genomics reveals marine diversity and ancestral characteristics of land plants},
author = {van Baren, Marijke J. and Bachy, Charles and Reistetter, Emily Nahas and Purvine, Samuel O. and Grimwood, Jane and Sudek, Sebastian and Yu, Hang and Poirier, Camille and Deerinck, Thomas J. and Kuo, Alan and Grigoriev, Igor V. and Wong, Chee -Hong and Smith, Richard D. and Callister, Stephen J. and Wei, Chia -Lin and Schmutz, Jeremy and Worden, Alexandra Z.},
abstractNote = {Prasinophytes are widespread marine green algae that are related to plants. Abundance of the genus Micromonas has reportedly increased in the Arctic due to climate-induced changes. Thus, studies of these organisms are important for marine ecology and understanding Virdiplantae evolution and diversification. We generated evidence-based Micromonas gene models using proteomics and RNA-Seq to improve prasinophyte genomic resources. First, sequences of four chromosomes in the 22 Mb Micromonas pusilla (CCMP1545) genome were finished. Comparison with the finished 21 Mb Micromonas commoda (RCC299) shows they share ≤ 8,142 of ~10,000 protein-encoding genes, depending on the analysis method. Unlike RCC299 and other sequenced eukaryotes, CCMP1545 has two abundant repetitive intron types and a high percent (26%) GC splice donors. Micromonas has more genus-specific protein families (19%) than other genome sequenced prasinophytes (11%). Comparative analyses using predicted proteomes from other prasinophytes reveal proteins likely related to scale formation and ancestral photosynthesis. Our studies also indicate that peptidoglycan (PG) biosynthesis enzymes have been lost in multiple independent events in select prasinophytes and most plants. However, CCMP1545, polar Micromonas CCMP2099 and prasinophytes from other claasses retain the entire PG pathway, like moss and glaucophyte algae. Multiple vascular plants that share a unique bi-domain protein also have the pathway, except the Penicillin-Binding-Protein. Alongside Micromonas experiments using antibiotics that halt bacterial PG biosynthesis, the findings highlight unrecognized phylogenetic complexity in the PG-pathway retention and implicate a role in chloroplast structure of division in several extant Vridiplantae lineages. Extensive differences in gene loss and architecture between related prasinophytes underscore their extensive divergence. PG biosynthesis genes from the cyanobacterial endosymbiont that became the plastid, have been selectively retained in some plants and algae, implying a biological function. As a result, our studies provide robust genomic resources for emerging model algae, advancing knowledge of marine phytoplankton and plant evolution.},
doi = {10.1186/s12864-016-2585-6},
journal = {BMC Genomics},
number = 1,
volume = 17,
place = {United States},
year = {Thu Mar 31 00:00:00 EDT 2016},
month = {Thu Mar 31 00:00:00 EDT 2016}
}

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