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

Abstract

Background: Prasinophytes are widespread marine green algae that are related to plants. Cellular abundance of the prasinophyte Micromonas has reportedly increased in the Arctic due to climate-induced changes. Thus, studies of these unicellular eukaryotes are important for marine ecology and for understanding Viridiplantae evolution and diversification. Results: 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 genome of Micromonas commoda (RCC299; named herein) shows they share ≤8,141 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 plants. However, CCMP1545, polar Micromonas CCMP2099 and prasinophytes from other classes retain the entire PG pathway, like moss and glaucophyte algae. Surprisingly,more » multiple vascular plants also have the PG pathway, except the Penicillin-Binding Protein, and share a unique bi-domain protein potentially associated with the pathway. Alongside Micromonas experiments using antibiotics that halt bacterial PG biosynthesis, the findings highlight unrecognized phylogenetic complexity in PG-pathway retention and implicate a role in chloroplast structure or division in several extant Viridiplantae lineages. Conclusions: Extensive differences in gene loss and architecture between related prasinophytes underscore their divergence. PG biosynthesis genes from the cyanobacterial endosymbiont that became the plastid, have been selectively retained in multiple plants and algae, implying a biological function. Our studies provide robust genomic resources for emerging model algae, advancing knowledge of marine phytoplankton and plant evolution« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1618541
Alternate Identifier(s):
OSTI ID: 1337274; OSTI ID: 1615262
Report Number(s):
PNNL-SA-114561
Journal ID: ISSN 1471-2164; 267; PII: 2585
Grant/Contract Number:  
SC0004765; AC05-76RL01830; AC02-05CH11231
Resource Type:
Journal Article: Published Article
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Name: BMC Genomics Journal Volume: 17 Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United Kingdom
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 Kingdom: 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 Kingdom. 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 Kingdom. doi:10.1186/s12864-016-2585-6.
@article{osti_1618541,
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 = {Background: Prasinophytes are widespread marine green algae that are related to plants. Cellular abundance of the prasinophyte Micromonas has reportedly increased in the Arctic due to climate-induced changes. Thus, studies of these unicellular eukaryotes are important for marine ecology and for understanding Viridiplantae evolution and diversification. Results: 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 genome of Micromonas commoda (RCC299; named herein) shows they share ≤8,141 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 plants. However, CCMP1545, polar Micromonas CCMP2099 and prasinophytes from other classes retain the entire PG pathway, like moss and glaucophyte algae. Surprisingly, multiple vascular plants also have the PG pathway, except the Penicillin-Binding Protein, and share a unique bi-domain protein potentially associated with the pathway. Alongside Micromonas experiments using antibiotics that halt bacterial PG biosynthesis, the findings highlight unrecognized phylogenetic complexity in PG-pathway retention and implicate a role in chloroplast structure or division in several extant Viridiplantae lineages. Conclusions: Extensive differences in gene loss and architecture between related prasinophytes underscore their divergence. PG biosynthesis genes from the cyanobacterial endosymbiont that became the plastid, have been selectively retained in multiple plants and algae, implying a biological function. 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},
issn = {1471-2164},
number = 1,
volume = 17,
place = {United Kingdom},
year = {2016},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1186/s12864-016-2585-6

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Cited by: 11 works
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