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ISME J. 2014 Dec;8(12):2517-29. doi: 10.1038/ismej.2014.146. Epub 2014 Aug 29.

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

Author information

1
Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA.
2
School of Environmental Sciences, University of East Anglia, Norwich, UK.
3
1] Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada [2] Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, Toronto, Ontario, Canada.
4
Department of Chemistry, Texas A&M University, College Station, TX, USA.
5
1] Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, Toronto, Ontario, Canada [2] Biology Department, University of New Brunswick, Fredericton, New Brunswick, Canada.
6
1] Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA [2] Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, Toronto, Ontario, Canada.

Abstract

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.

PMID:
25171333
PMCID:
PMC4260697
DOI:
10.1038/ismej.2014.146
[Indexed for MEDLINE]
Free PMC Article

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