Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages

McRose, Darcy, Guo, Jian, Monier, Adam, Sudek, Sebastian, Wilken, Susanne, Yan, Shuangchun, Mock, Thomas ORCID:, Archibald, John M., Begley, Tadhg P., Reyes-Prieto, Adrian and Worden, Alexandra Z. (2014) Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages. ISME Journal, 8 (12). pp. 2517-2529. ISSN 1751-7362

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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 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 B 1, making vitamin control of phytoplankton blooms more complex than the current paradigm suggests.

Item Type: Article
Additional Information: Funding Information: Financial support was from the Packard Foundation, a GBMF Investigator Award, NSF IOS0843119 and DOE DE-SC0004765 to AZW. AM is now at University of Exeter, Exeter, UK. DM is now at Princeton University, Princeton, NJ, USA.
Uncontrolled Keywords: microbiology,ecology, evolution, behavior and systematics,sdg 14 - life below water ,/dk/atira/pure/subjectarea/asjc/2400/2404
Faculty \ School: Faculty of Science > School of Environmental Sciences
UEA Research Groups: Faculty of Science > Research Groups > Centre for Ocean and Atmospheric Sciences
Faculty of Science > Research Groups > Environmental Biology
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Depositing User: LivePure Connector
Date Deposited: 08 Mar 2024 12:33
Last Modified: 12 Mar 2024 10:30
DOI: 10.1038/ismej.2014.146

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