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

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

Journal Article · Fri Aug 29 04:00:00 UTC 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)

Cite

Export

Save

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

References (68)

Molecular Phylogeny and Classification of the Mamiellophyceae class. nov. (Chlorophyta) based on Sequence Comparisons of the Nuclear- and Plastid-encoded rRNA Operons Marin, Birger; Melkonian, Michael Protist, Vol. 161, Issue 2 https://doi.org/10.1016/j.protis.2009.10.002	journal	April 2010
Requirement for Thiamine Among Some Marine and Supra-Littoral Protista Droop, M. R. Journal of the Marine Biological Association of the United Kingdom, Vol. 37, Issue 2 https://doi.org/10.1017/s0025315400023729	journal	June 1958
Simplified Statistics for Small Numbers of Observations Dean, R. B.; Dixon, W. J. Analytical Chemistry, Vol. 23, Issue 4 https://doi.org/10.1021/ac60052a025	journal	April 1951
Mechanistic Studies on Thiamin Phosphate Synthase: Evidence for a Dissociative Mechanism ^† Reddick, Jason J.; Nicewonger, Robb; Begley, Tadhg P. Biochemistry, Vol. 40, Issue 34 https://doi.org/10.1021/bi010267q	journal	August 2001
Biochemical Characterization of ThiT from Lactococcus lactis : A Thiamin Transporter with Picomolar Substrate Binding Affinity Erkens, Guus B.; Slotboom, Dirk Jan Biochemistry, Vol. 49, Issue 14 https://doi.org/10.1021/bi100154r	journal	April 2010
Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids Treusch, Alexander H.; Demir-Hilton, Elif; Vergin, Kevin L. The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.117	journal	September 2011
Discovery of a SAR11 growth requirement for thiamin’s pyrimidine precursor and its distribution in the Sargasso Sea Carini, Paul; Campbell, Emily O.; Morré, Jeff The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.61	journal	April 2014
Pan genome of the phytoplankton Emiliania underpins its global distribution Read, Betsy A.; Kegel, Jessica; Klute, Mary J. Nature, Vol. 499, Issue 7457 https://doi.org/10.1038/nature12221	journal	June 2013
The control mechanism of thiamine biosynthesis a model for the study of control of converging pathways Newell, Pc; Tucker, Rg Biochemical Journal, Vol. 100, Issue 2 https://doi.org/10.1042/bj1000517	journal	August 1966
Most harmful algal bloom species are vitamin B1 and B12 auxotrophs Tang, Y. Z.; Koch, F.; Gobler, C. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 48 https://doi.org/10.1073/pnas.1009566107	journal	November 2010
Vitamins in the sea Giovannoni, S. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 35 https://doi.org/10.1073/pnas.1211722109	journal	August 2012
thiBPQ Encodes an ABC Transporter Required for Transport of Thiamine and Thiamine Pyrophosphate in Salmonella typhimurium Webb, Eric; Claas, Kathy; Downs, Diana Journal of Biological Chemistry, Vol. 273, Issue 15 https://doi.org/10.1074/jbc.273.15.8946	journal	April 1998
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models Stamatakis, Alexandros Bioinformatics, Vol. 22, Issue 21 https://doi.org/10.1093/bioinformatics/btl446	journal	August 2006
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
The Pfam protein families database Finn, Robert D.; Mistry, Jaina; Tate, John Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp985	journal	November 2009
Eukaryotic TPP riboswitch regulation of alternative splicing involving long-distance base pairing Li, Sanshu; Breaker, Ronald R. Nucleic Acids Research, Vol. 41, Issue 5 https://doi.org/10.1093/nar/gkt057	journal	February 2013
Broadly Sampled Multigene Analyses Yield a Well-Resolved Eukaryotic Tree of Life Parfrey, Laura Wegener; Grant, Jessica; Tekle, Yonas I. Systematic Biology, Vol. 59, Issue 5 https://doi.org/10.1093/sysbio/syq037	journal	July 2010
The endosymbiotic origin, diversification and fate of plastids Keeling, Patrick J. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1541 https://doi.org/10.1098/rstb.2009.0103	journal	March 2010
Riboswitch Control of Gene Expression in Plants by Splicing and Alternative 3′ End Processing of mRNAs Wachter, Andreas; Tunc-Ozdemir, Meral; Grove, Beth C. The Plant Cell, Vol. 19, Issue 11 https://doi.org/10.1105/tpc.107.053645	journal	November 2007
Repression of Essential Chloroplast Genes Reveals New Signaling Pathways and Regulatory Feedback Loops in Chlamydomonas Ramundo, Silvia; Rahire, Michèle; Schaad, Olivier The Plant Cell, Vol. 25, Issue 1 https://doi.org/10.1105/tpc.112.103051	journal	January 2013
Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas Worden, A. Z.; Lee, J. -H.; Mock, T. Science, Vol. 324, Issue 5924 https://doi.org/10.1126/science.1167222	journal	April 2009
Algae Need Their Vitamins Croft, Martin T.; Warren, Martin J.; Smith, Alison G. Eukaryotic Cell, Vol. 5, Issue 8 https://doi.org/10.1128/ec.00097-06	journal	August 2006
The Structural and Biochemical Foundations of Thiamin Biosynthesis Jurgenson, Christopher T.; Begley, Tadhg P.; Ealick, Steven E. Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.78.072407.102340	journal	June 2009
Regulation of Bacterial gene Expression by Riboswitches Winkler, Wade C.; Breaker, Ronald R. Annual Review of Microbiology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.micro.59.030804.121336	journal	October 2005
Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified Keane, Thomas M.; Creevey, Christopher J.; Pentony, Melissa M. BMC Evolutionary Biology, Vol. 6, Issue 1 https://doi.org/10.1186/1471-2148-6-29	journal	March 2006
Identification of candidate structured RNAs in the marine organism 'Candidatus Pelagibacter ubique' Meyer, Michelle M.; Ames, Tyler D.; Smith, Daniel P. BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-268	journal	January 2009
Influence of vitamin B auxotrophy on nitrogen metabolism in eukaryotic phytoplankton Bertrand, Erin M.; Allen, Andrew E. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00375	journal	January 2012
Principles governing amino acid composition of integral membrane proteins: application to topology prediction 1 1Edited by J. Thornton Tusnády, Gábor E.; Simon, István Journal of Molecular Biology, Vol. 283, Issue 2 https://doi.org/10.1006/jmbi.1998.2107	journal	October 1998
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Recent progress in understanding thiamin biosynthesis and its genetic regulation in Saccharomyces cerevisiae Nosaka, Kazuto Applied Microbiology and Biotechnology, Vol. 72, Issue 1 https://doi.org/10.1007/s00253-006-0464-9	journal	July 2006
Prospects for Riboswitch Discovery and Analysis Breaker, Ronald R. Molecular Cell, Vol. 43, Issue 6 https://doi.org/10.1016/j.molcel.2011.08.024	journal	September 2011
Molecular Phylogeny and Classification of the Mamiellophyceae class. nov. (Chlorophyta) based on Sequence Comparisons of the Nuclear- and Plastid-encoded rRNA Operons Marin, Birger; Melkonian, Michael Protist, Vol. 161, Issue 2 https://doi.org/10.1016/j.protis.2009.10.002	journal	April 2010
Switching the light on plant riboswitches Bocobza, Samuel E.; Aharoni, Asaph Trends in Plant Science, Vol. 13, Issue 10 https://doi.org/10.1016/j.tplants.2008.07.004	journal	October 2008
Requirement for Thiamine Among Some Marine and Supra-Littoral Protista Droop, M. R. Journal of the Marine Biological Association of the United Kingdom, Vol. 37, Issue 2 https://doi.org/10.1017/S0025315400023729	journal	June 1958
Simplified Statistics for Small Numbers of Observations Dean, R. B.; Dixon, W. J. Analytical Chemistry, Vol. 23, Issue 4 https://doi.org/10.1021/ac60052a025	journal	April 1951
Mechanistic Studies on Thiamin Phosphate Synthase: Evidence for a Dissociative Mechanism ^† Reddick, Jason J.; Nicewonger, Robb; Begley, Tadhg P. Biochemistry, Vol. 40, Issue 34 https://doi.org/10.1021/bi010267q	journal	August 2001
Biochemical Characterization of ThiT from Lactococcus lactis : A Thiamin Transporter with Picomolar Substrate Binding Affinity Erkens, Guus B.; Slotboom, Dirk Jan Biochemistry, Vol. 49, Issue 14 https://doi.org/10.1021/bi100154r	journal	April 2010
Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids Treusch, Alexander H.; Demir-Hilton, Elif; Vergin, Kevin L. The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.117	journal	September 2011
Discovery of a SAR11 growth requirement for thiamin’s pyrimidine precursor and its distribution in the Sargasso Sea Carini, Paul; Campbell, Emily O.; Morré, Jeff The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.61	journal	April 2014
Control of alternative RNA splicing and gene expression by eukaryotic riboswitches Cheah, Ming T.; Wachter, Andreas; Sudarsan, Narasimhan Nature, Vol. 447, Issue 7143 https://doi.org/10.1038/nature05769	journal	April 2007
Pan genome of the phytoplankton Emiliania underpins its global distribution Read, Betsy A.; Kegel, Jessica; Klute, Mary J. Nature, Vol. 499, Issue 7457 https://doi.org/10.1038/nature12221	journal	June 2013
The control mechanism of thiamine biosynthesis a model for the study of control of converging pathways Newell, Pc; Tucker, Rg Biochemical Journal, Vol. 100, Issue 2 https://doi.org/10.1042/bj1000517	journal	August 1966
Thiamine biosynthesis in algae is regulated by riboswitches Croft, M. T.; Moulin, M.; Webb, M. E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 52 https://doi.org/10.1073/pnas.0705786105	journal	December 2007
Most harmful algal bloom species are vitamin B1 and B12 auxotrophs Tang, Y. Z.; Koch, F.; Gobler, C. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 48 https://doi.org/10.1073/pnas.1009566107	journal	November 2010
Multiple B-vitamin depletion in large areas of the coastal ocean Sanudo-Wilhelmy, S. A.; Cutter, L. S.; Durazo, R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 35 https://doi.org/10.1073/pnas.1208755109	journal	July 2012
thiBPQ Encodes an ABC Transporter Required for Transport of Thiamine and Thiamine Pyrophosphate in Salmonella typhimurium Webb, Eric; Claas, Kathy; Downs, Diana Journal of Biological Chemistry, Vol. 273, Issue 15 https://doi.org/10.1074/jbc.273.15.8946	journal	April 1998
Comparative Genomics of Thiamin Biosynthesis in Procaryotes: NEW GENES AND REGULATORY MECHANISMS Rodionov, Dmitry A.; Vitreschak, Alexey G.; Mironov, Andrey A. Journal of Biological Chemistry, Vol. 277, Issue 50 https://doi.org/10.1074/jbc.M208965200	journal	October 2002
MrBayes 3: Bayesian phylogenetic inference under mixed models Ronquist, Fredrik; Huelsenbeck, John P. Bioinformatics, Vol. 19, Issue 12, p. 1572-1574 https://doi.org/10.1093/bioinformatics/btg180	journal	August 2003
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models Stamatakis, Alexandros Bioinformatics, Vol. 22, Issue 21 https://doi.org/10.1093/bioinformatics/btl446	journal	August 2006
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
The Pfam protein families database Finn, Robert D.; Mistry, Jaina; Tate, John Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp985	journal	November 2009
Eukaryotic TPP riboswitch regulation of alternative splicing involving long-distance base pairing Li, Sanshu; Breaker, Ronald R. Nucleic Acids Research, Vol. 41, Issue 5 https://doi.org/10.1093/nar/gkt057	journal	February 2013
Broadly Sampled Multigene Analyses Yield a Well-Resolved Eukaryotic Tree of Life Parfrey, Laura Wegener; Grant, Jessica; Tekle, Yonas I. Systematic Biology, Vol. 59, Issue 5 https://doi.org/10.1093/sysbio/syq037	journal	July 2010
The endosymbiotic origin, diversification and fate of plastids Keeling, Patrick J. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1541 https://doi.org/10.1098/rstb.2009.0103	journal	March 2010
Riboswitch Control of Gene Expression in Plants by Splicing and Alternative 3′ End Processing of mRNAs Wachter, Andreas; Tunc-Ozdemir, Meral; Grove, Beth C. The Plant Cell, Vol. 19, Issue 11 https://doi.org/10.1105/tpc.107.053645	journal	November 2007
Repression of Essential Chloroplast Genes Reveals New Signaling Pathways and Regulatory Feedback Loops in Chlamydomonas Ramundo, Silvia; Rahire, Michèle; Schaad, Olivier The Plant Cell, Vol. 25, Issue 1 https://doi.org/10.1105/tpc.112.103051	journal	January 2013
INFLUENCE OF TEMPERATURE AND SOLAR RADIATION ON PERSISTENCE OF VITAMIN B ₁₂ , THIAMINE, AND BIOTIN IN SEAWATER Carlucci, A. F.; Silbernagel, S. B.; McNally, P. M. Journal of Phycology, Vol. 5, Issue 4 https://doi.org/10.1111/j.1529-8817.1969.tb02618.x	journal	December 1969
Green Evolution and Dynamic Adaptations Revealed by Genomes of the Marine Picoeukaryotes Micromonas Worden, A. Z.; Lee, J. -H.; Mock, T. Science, Vol. 324, Issue 5924 https://doi.org/10.1126/science.1167222	journal	April 2009
Algae Need Their Vitamins Croft, Martin T.; Warren, Martin J.; Smith, Alison G. Eukaryotic Cell, Vol. 5, Issue 8 https://doi.org/10.1128/EC.00097-06	journal	August 2006
The Structural and Biochemical Foundations of Thiamin Biosynthesis Jurgenson, Christopher T.; Begley, Tadhg P.; Ealick, Steven E. Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.78.072407.102340	journal	June 2009
Regulation of Bacterial gene Expression by Riboswitches Winkler, Wade C.; Breaker, Ronald R. Annual Review of Microbiology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.micro.59.030804.121336	journal	October 2005
Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified Keane, Thomas M.; Creevey, Christopher J.; Pentony, Melissa M. BMC Evolutionary Biology, Vol. 6, Issue 1 https://doi.org/10.1186/1471-2148-6-29	journal	March 2006
Identification of candidate structured RNAs in the marine organism 'Candidatus Pelagibacter ubique' Meyer, Michelle M.; Ames, Tyler D.; Smith, Daniel P. BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-268	journal	January 2009
The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing Keeling, Patrick J.; Burki, Fabien; Wilcox, Heather M. PLoS Biology, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pbio.1001889	journal	June 2014
Influence of vitamin B auxotrophy on nitrogen metabolism in eukaryotic phytoplankton Bertrand, Erin M.; Allen, Andrew E. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00375	journal	January 2012
Riboswitch-mediated control of gene expression in eukaryotes Wachter, Andreas RNA Biology, Vol. 7, Issue 1 https://doi.org/10.4161/rna.7.1.10489	journal	January 2010
The use of DAPI for identifying and counting aquatic microflora1 Porter, Karen G.; Feig, Yvette S. Limnology and Oceanography, Vol. 25, Issue 5 https://doi.org/10.4319/lo.1980.25.5.0943	journal	September 1980
Assessing the dynamics and ecology of marine picophytoplankton: The importance of the eukaryotic component Worden, Alexandra Z.; Nolan, Jessica K.; Palenik, B. Limnology and Oceanography, Vol. 49, Issue 1 https://doi.org/10.4319/lo.2004.49.1.0168	journal	January 2004

Cited By (27)

Use of plankton-derived vitamin B1 precursors, especially thiazole-related precursor, by key marine picoeukaryotic phytoplankton Paerl, Ryan W.; Bouget, Francois-Yves; Lozano, Jean-Claude The ISME Journal, Vol. 11, Issue 3 https://doi.org/10.1038/ismej.2016.145	journal	December 2016
Phylogenomic and comparative analysis of the distribution and regulatory patterns of TPP riboswitches in fungi Mukherjee, Sumit; Retwitzer, Matan Drory; Barash, Danny Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-23900-7	journal	April 2018
Intron Invasions Trace Algal Speciation and Reveal Nearly Identical Arctic and Antarctic Micromonas Populations Simmons, Melinda P.; Bachy, Charles; Sudek, Sebastian Molecular Biology and Evolution, Vol. 32, Issue 9 https://doi.org/10.1093/molbev/msv122	journal	May 2015
Globally Important Haptophyte Algae Use Exogenous Pyrimidine Compounds More Efficiently than Thiamin Gutowska, Magdalena A.; Shome, Brateen; Sudek, Sebastian mBio, Vol. 8, Issue 5 https://doi.org/10.1128/mbio.01459-17	journal	November 2017
Evidence-based green algal genomics reveals marine diversity and ancestral characteristics of land plants van Baren, Marijke J.; Bachy, Charles; Reistetter, Emily Nahas BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2585-6	journal	March 2016
A promising approach to enhance microalgae productivity by exogenous supply of vitamins Tandon, Puja; Jin, Qiang; Huang, Limin Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0834-2	journal	November 2017
Evidence for Strain-Specific Exometabolomic Responses of the Coccolithophore Emiliania huxleyi to Grazing by the Dinoflagellate Oxyrrhis marina Poulson-Ellestad, Kelsey L.; Harvey, Elizabeth L.; Johnson, Matthew D. Frontiers in Marine Science, Vol. 3 https://doi.org/10.3389/fmars.2016.00001	journal	January 2016
Vitamin B1 in marine sediments: pore water concentration gradient drives benthic flux with potential biological implications Monteverde, Danielle R.; GÃ³mez-Consarnau, Laura; Cutter, Lynda Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00434	journal	May 2015
B Vitamins and Their Congeners as Potential Drivers of Microbial Community Composition in an Oligotrophic Marine Ecosystem Suffridge, C. P.; Gómez-Consarnau, L.; Monteverde, D. R. Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 9 https://doi.org/10.1029/2018jg004554	journal	September 2018
Cross-exchange of B-vitamins underpins a mutualistic interaction between Ostreococcus tauri and Dinoroseobacter shibae Cooper, Matthew B.; Kazamia, Elena; Helliwell, Katherine E. The ISME Journal, Vol. 13, Issue 2 https://doi.org/10.1038/s41396-018-0274-y	journal	September 2018
Phylogenomic and comparative analysis of the distribution and regulatory patterns of TPP riboswitches in fungi Mukherjee, Sumit; Retwitzer, Matan Drory; Barash, Danny Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-23900-7	journal	April 2018
How haptophytes microalgae mitigate vitamin B12 limitation Nef, Charlotte; Jung, Sébastien; Mairet, Francis Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-44797-w	journal	June 2019
Modeling vitamin B1 transfer to consumers in the aquatic food web Ejsmond, M. J.; Blackburn, N.; Fridolfsson, E. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-46422-2	journal	July 2019
Mosaic Patterns of B-vitamin Synthesis and Utilization in a Natural Marine Microbial Community Gómez-Consarnau, Laura; Sachdeva, Rohan; Gifford, Scott M. Environmental Microbiology https://doi.org/10.1101/280438	journal	January 2018
Mosaic patterns of B-vitamin synthesis and utilization in a natural marine microbial community: B-vitamin mosaics Gómez-Consarnau, Laura; Sachdeva, Rohan; Gifford, Scott M. Environmental Microbiology, Vol. 20, Issue 8 https://doi.org/10.1111/1462-2920.14133	journal	May 2018
Transcriptomic and proteomic responses of the oceanic diatom Pseudo-nitzschia granii to iron limitation Cohen, Natalie R.; Gong, Weida; Moran, Dawn M. Environmental Microbiology, Vol. 20, Issue 8 https://doi.org/10.1111/1462-2920.14386	journal	August 2018
Metabolic relationships of uncultured bacteria associated with the microalgae Gambierdiscus Rambo, Ian M.; Dombrowski, Nina; Constant, Lauren Environmental Microbiology, Vol. 22, Issue 5 https://doi.org/10.1111/1462-2920.14878	journal	December 2019
How mutualisms arise in phytoplankton communities: building eco-evolutionary principles for aquatic microbes Kazamia, Elena; Helliwell, Katherine Emma; Purton, Saul Ecology Letters, Vol. 19, Issue 7 https://doi.org/10.1111/ele.12615	journal	June 2016
Metabolic Model of the Phytophthora infestans -Tomato Interaction Reveals Metabolic Switches during Host Colonization Rodenburg, Sander Y. A.; Seidl, Michael F.; Judelson, Howard S. mBio, Vol. 10, Issue 4 https://doi.org/10.1128/mbio.00454-19	journal	July 2019
Evidence-based green algal genomics reveals marine diversity and ancestral characteristics of land plants van Baren, Marijke J.; Bachy, Charles; Reistetter, Emily Nahas BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2585-6	journal	March 2016
A promising approach to enhance microalgae productivity by exogenous supply of vitamins Tandon, Puja; Jin, Qiang; Huang, Limin Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0834-2	journal	November 2017
TPP riboswitch-dependent regulation of an ancient thiamin transporter in Candida Donovan, Paul D.; Holland, Linda M.; Lombardi, Lisa PLOS Genetics, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pgen.1007429	journal	May 2018
Deficiency syndromes in top predators associated with large-scale changes in the Baltic Sea ecosystem Majaneva, Sanna; Fridolfsson, Emil; Casini, Michele PLOS ONE, Vol. 15, Issue 1 https://doi.org/10.1371/journal.pone.0227714	journal	January 2020
Cross-exchange of B-vitamins underpins a mutualistic interaction between Ostreococcus tauri and Dinoroseobacter shibae. Cooper, Matthew B.; Kazamia, Elena; Helliwell, Katherine E. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.28008	text	January 2019
Essential Biomolecules in Food Webs Ruess, Liliane; Müller-Navarra, Dörthe C. Frontiers in Ecology and Evolution, Vol. 7 https://doi.org/10.3389/fevo.2019.00269	journal	July 2019
The Exometabolome of Two Model Strains of the Roseobacter Group: A Marketplace of Microbial Metabolites Wienhausen, Gerrit; Noriega-Ortega, Beatriz E.; Niggemann, Jutta Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01985	journal	October 2017
Metabolism of Dietary and Microbial Vitamin B Family in the Regulation of Host Immunity Yoshii, Ken; Hosomi, Koji; Sawane, Kento Frontiers in Nutrition, Vol. 6 https://doi.org/10.3389/fnut.2019.00048	journal	April 2019

Similar Records

ERAD Components in Organisms with Complex Red Plastids Suggest Recruitment of a Preexisting Protein Transport Pathway for the Periplastid Membrane

Journal Article · Mon Nov 15 04:00:00 UTC 2010 · Genome Biology and Evolution · OSTI ID:1625325

Felsner, Gregor; Sommer, Maik S.; Gruenheit, Nicole; +5 more

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton

Journal Article · Wed Jul 28 04:00:00 UTC 2010 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1051835

Cuvelier, Marie L.; Allen, Andrew E.; Monier, Adam; +19 more

Structural Basis for Gene Regulation by a Thiamine Pyrophosphate-Sensing Riboswitch

Journal Article · Sun Jan 01 04:00:00 UTC 2006 · Nature · OSTI ID:914289

Serganov, A; Polonskaia, A; Phan, A; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

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

Citation Formats

References (68)

Cited By (27)

Similar Records

Related Subjects

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