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Title: Alternatives to vitamin B 1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages

Abstract

Here, vitamin B 1 (thiamine pyrophosphate, TPP) is essential to all life but scarce in ocean surface waters. In many bacteria and a few eukaryotic groups thiamine biosynthesis genes are controlled by metabolite-sensing mRNA-based gene regulators known as riboswitches. Using available genome sequences and transcriptomes generated from ecologically important marine phytoplankton, we identified 31 new eukaryotic riboswitches. These were found in alveolate, cryptophyte, haptophyte and rhizarian phytoplankton as well as taxa from two lineages previously known to have riboswitches (green algae and stramenopiles). The predicted secondary structures bear hallmarks of TPP-sensing riboswitches. Surprisingly, most of the identified riboswitches are affiliated with genes of unknown function, rather than characterized thiamine biosynthesis genes. Using qPCR and growth experiments involving two prasinophyte algae, we show that expression of these genes increases significantly under vitamin B 1-deplete conditions relative to controls. Pathway analyses show that several algae harboring the uncharacterized genes lack one or more enzymes in the known TPP biosynthesis pathway. We demonstrate that one such alga, the major primary producer Emiliania huxleyi, grows on 4-amino-5-hydroxymethyl-2-methylpyrimidine (a thiamine precursor moiety) alone, although long thought dependent on exogenous sources of thiamine. Thus, overall, we have identified riboswitches in major eukaryotic lineages not known tomore » undergo this form of gene regulation. In these phytoplankton groups, riboswitches are often affiliated with widespread thiamine-responsive genes with as yet uncertain roles in TPP pathways. Further, taxa with ‘incomplete’ TPP biosynthesis pathways do not necessarily require exogenous vitamin B 1, making vitamin control of phytoplankton blooms more complex than the current paradigm suggests.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [2];  [3];  [4];  [5];  [6]
  1. Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States)
  2. University of East Anglia, Norwich (United Kingdom)
  3. Dalhousie Univ., Halifas, NS (Canada); Canadian Institute for Advanced Research, Toronto, ON (Canada)
  4. Texas A & M Univ., College Station, TX (United States)
  5. Canadian Institute for Advanced Research, Toronto, ON (Canada); Univ. of New Brunswick, Fredericton, NB (Canada)
  6. Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States); Canadian Institute for Advanced Research, Toronto, ON (Canada)
Publication Date:
Research Org.:
Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1455183
Grant/Contract Number:  
SC0004765
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 8; Journal Issue: 12; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

McRose, Darcy, Guo, Jian, Monier, Adam, Sudek, Sebastian, Wilken, Susanne, Yan, Shuangchun, Mock, Thomas, Archibald, John M., Begley, Tadhg P., Reyes-Prieto, Adrian, and Worden, Alexandra Z. Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages. United States: N. p., 2014. Web. doi:10.1038/ismej.2014.146.
McRose, Darcy, Guo, Jian, Monier, Adam, Sudek, Sebastian, Wilken, Susanne, Yan, Shuangchun, Mock, Thomas, Archibald, John M., Begley, Tadhg P., Reyes-Prieto, Adrian, & Worden, Alexandra Z. Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages. United States. doi:10.1038/ismej.2014.146.
McRose, Darcy, Guo, Jian, Monier, Adam, Sudek, Sebastian, Wilken, Susanne, Yan, Shuangchun, Mock, Thomas, Archibald, John M., Begley, Tadhg P., Reyes-Prieto, Adrian, and Worden, Alexandra Z. Fri . "Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages". United States. doi:10.1038/ismej.2014.146. https://www.osti.gov/servlets/purl/1455183.
@article{osti_1455183,
title = {Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages},
author = {McRose, Darcy and Guo, Jian and Monier, Adam and Sudek, Sebastian and Wilken, Susanne and Yan, Shuangchun and Mock, Thomas and Archibald, John M. and Begley, Tadhg P. and Reyes-Prieto, Adrian and Worden, Alexandra Z.},
abstractNote = {Here, vitamin B1 (thiamine pyrophosphate, TPP) is essential to all life but scarce in ocean surface waters. In many bacteria and a few eukaryotic groups thiamine biosynthesis genes are controlled by metabolite-sensing mRNA-based gene regulators known as riboswitches. Using available genome sequences and transcriptomes generated from ecologically important marine phytoplankton, we identified 31 new eukaryotic riboswitches. These were found in alveolate, cryptophyte, haptophyte and rhizarian phytoplankton as well as taxa from two lineages previously known to have riboswitches (green algae and stramenopiles). The predicted secondary structures bear hallmarks of TPP-sensing riboswitches. Surprisingly, most of the identified riboswitches are affiliated with genes of unknown function, rather than characterized thiamine biosynthesis genes. Using qPCR and growth experiments involving two prasinophyte algae, we show that expression of these genes increases significantly under vitamin B1-deplete conditions relative to controls. Pathway analyses show that several algae harboring the uncharacterized genes lack one or more enzymes in the known TPP biosynthesis pathway. We demonstrate that one such alga, the major primary producer Emiliania huxleyi, grows on 4-amino-5-hydroxymethyl-2-methylpyrimidine (a thiamine precursor moiety) alone, although long thought dependent on exogenous sources of thiamine. Thus, overall, we have identified riboswitches in major eukaryotic lineages not known to undergo this form of gene regulation. In these phytoplankton groups, riboswitches are often affiliated with widespread thiamine-responsive genes with as yet uncertain roles in TPP pathways. Further, taxa with ‘incomplete’ TPP biosynthesis pathways do not necessarily require exogenous vitamin B1, making vitamin control of phytoplankton blooms more complex than the current paradigm suggests.},
doi = {10.1038/ismej.2014.146},
journal = {The ISME Journal},
issn = {1751-7362},
number = 12,
volume = 8,
place = {United States},
year = {2014},
month = {8}
}

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Works referenced in this record:

MrBayes 3: Bayesian phylogenetic inference under mixed models
journal, August 2003