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; Archibald, John M.; Begley, Tadhg P.; Reyes-Prieto, Adrian; Worden, Alexandra Z.

doi:10.1038/ismej.2014.146

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

Journal Article · Fri Aug 29 00:00:00 EDT 2014 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2014.146· OSTI ID:1455183

McRose, Darcy ^[1]; Guo, Jian ^[2]; Monier, Adam ^[2]; Sudek, Sebastian ^[2]; Wilken, Susanne ^[2]; Yan, Shuangchun ^[2]; Mock, Thomas ^[3]; Archibald, John M. ^[4]; Begley, Tadhg P. ^[5]; Reyes-Prieto, Adrian ^[6]; Worden, Alexandra Z. ^[7]

Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States); Monterey Bay Aquarium Research Institute, Moss Landing, California (United States)
Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States)
University of East Anglia, Norwich (United Kingdom)
Dalhousie Univ., Halifas, NS (Canada); Canadian Institute for Advanced Research, Toronto, ON (Canada)
Texas A & M Univ., College Station, TX (United States)
Canadian Institute for Advanced Research, Toronto, ON (Canada); Univ. of New Brunswick, Fredericton, NB (Canada)
Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States); Canadian Institute for Advanced Research, Toronto, ON (Canada)

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.

View Accepted Manuscript (DOE)

Research Organization:: Monterey Bay Aquarium Research Institute, Moss Landing, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0004765

OSTI ID:: 1455183

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 12 Vol. 8; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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