Whole cell affinity for 4-amino-5-hydroxymethyl-2-methylpyrimidine (HMP) in the marine bacterium Candidatus Pelagibacter st. HTCC7211 explains marine dissolved HMP concentrations.
Journal
Environmental microbiology reports
ISSN: 1758-2229
Titre abrégé: Environ Microbiol Rep
Pays: United States
ID NLM: 101499207
Informations de publication
Date de publication:
Oct 2024
Oct 2024
Historique:
received:
03
07
2024
accepted:
19
09
2024
medline:
5
10
2024
pubmed:
5
10
2024
entrez:
5
10
2024
Statut:
ppublish
Résumé
Vitamin B1 is a universally required coenzyme in carbon metabolism. However, most marine microorganisms lack the complete biosynthetic pathway for this compound and must acquire thiamin, or precursor molecules, from the dissolved pool. The most common version of Vitamin B1 auxotrophy is for thiamin's pyrimidine precursor moiety, 4-amino-5-hydroxymethyl-2-methylpyrimidine (HMP). Frequent HMP auxotrophy in plankton and vanishingly low dissolved concentrations (approximately 0.1-50 pM) suggest that high-affinity HMP uptake systems are responsible for maintaining low ambient HMP concentrations. We used tritium-labelled HMP to investigate HMP uptake mechanisms and kinetics in cell cultures of Candidatus Pelagibacter st. HTCC7211, a representative of the globally distributed and highly abundant SAR11 clade. A single protein, the sodium solute symporter ThiV, which is conserved across SAR11 genomes, is the likely candidate for HMP transport. Experimental evidence indicated transport specificity for HMP and mechanistically complex, high-affinity HMP uptake kinetics. Km values ranged from 9.5 pM to 1.2 nM and were dramatically lower when cells were supplied with a carbon source. These results suggest that HMP uptake in HTCC7211 is subject to complex regulation and point to a strategy for high-affinity uptake of this essential growth factor that can explain natural HMP levels in seawater.
Identifiants
pubmed: 39367564
doi: 10.1111/1758-2229.70023
doi:
Substances chimiques
Pyrimidines
0
Bacterial Proteins
0
Thiamine
X66NSO3N35
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e70023Subventions
Organisme : National Science Foundation
ID : DEB-1639033
Organisme : Simons Foundation International
ID : BIOS-SCOPE
Informations de copyright
© 2024 The Author(s). Environmental Microbiology Reports published by John Wiley & Sons Ltd.
Références
Atilho, R.M., Arachchilage, G.M., Greenlee, E.B., Knecht, K.M. & Breaker, R.R. (2019) A bacterial riboswitch class for the thiamin precursor HMP‐PP employs a terminator‐embedded aptamer. eLife, 8, e45210.
Beaudoin, G.A.W., Johnson, T.S. & Hanson, A.D. (2018) The PLUTO plastidial nucleobase transporter also transports the thiamin precursor hydroxymethylpyrimidine. Bioscience Reports, 38, 1–8.
Begley, T.P., Downs, D.M., Ealick, S.E., McLafferty, F.W., Van Loon, A.P., Taylor, S. et al. (1999) Thiamin biosynthesis in prokaryotes. Archives of Microbiology, 171, 293–300.
Bittner, M.J., Bannon, C.C., Rowland, E., Sundh, J., Bertrand, E.M., Andersson, A.F. et al. (2024) New chemical and microbial perspectives on vitamin B1 and vitamer dynamics of a coastal system. ISME Communications, 4(1), ycad016. Available from: https://doi.org/10.1093/ismeco/ycad016
Bradbeer, C. (1971) Transport of vitamin B12 in Ochromonas malhamensis. Archives of Biochemistry and Biophysics, 144, 184–192.
Bradbeer, C. & Woodrow, M.L. (1976) Transport of vitamin B12 in Escherichia coli: energy dependence. Journal of Bacteriology, 128, 99–104.
Bruns, S., Wienhausen, G., Scholz‐Böttcher, B., Heyen, S. & Wilkes, H. (2023) Method development and quantification of all B vitamins and selected biosynthetic precursors in winter and spring samples from the North Sea and de novo synthesized by Vibrio campbellii. Marine Chemistry, 256.
Bruns, S., Wienhausen, G., Scholz‐Bottcher, B. & Wilkes, H. (2022) Simultaneous quantification of all B vitamins and selected biosynthetic precursors in seawater and bacteria by means of different mass spectrometric approaches. Analytical and Bioanalytical Chemistry, 414, 7839–7854.
Carini, P., Campbell, E.O., Morré, J., Sañudo‐Wilhelmy, S.A., Thrash, J.C., Bennett, S.E. et al. (2014) Discovery of a SAR11 growth requirement for thiamin's pyrimidine precursor and its distribution in the Sargasso Sea. The ISME Journal, 8, 1727–1738.
Carini, P., Steindler, L., Beszteri, S. & Giovannoni, S.J. (2013) Nutrient requirements for growth of the extreme oligotroph ‘Candidatus Pelagibacter ubique'HTCC1062 on a defined medium. The ISME Journal, 7, 592–602.
Carlucci, A.F. & Bowes, P.M. (1970) Production of vitamin B‐12 thiamine and biotin by phytoplankton. Journal of Phycology, 6, 351–357.
Chatterjee, A., Hazra, A.B., Abdelwahed, S., Hilmey, D.G. & Begley, T.P. (2010) A “radical dance” in thiamin biosynthesis: mechanistic analysis of the bacterial hydroxymethylpyrimidine phosphate synthase. Angewandte Chemie International Edition, 49, 8653–8656.
Clifton, B.E., Alcolombri, U., Jackson, C.J. & Laurino, P. (2023) Ultrahigh‐affinity transport proteins from ubiquitous marine bacteria reveal mechanisms and global patterns of nutrient uptake. bioRxiv.
Cooper, L.E., O'Leary, S.N.E. & Begley, T.P. (2014) Biosynthesis of a thiamin antivitamin in clostridium botulinum. Biochemistry, 53, 2215–2217.
Dong, R., Peng, Z., Zhang, Y. & Yang, J. (2018) mTM‐align: an algorithm for fast and accurate multiple protein structure alignment. Bioinformatics, 34, 1719–1725.
Donovan, P.D., Holland, L.M., Lombardi, L., Coughlan, A.Y., Higgins, D.G., Wolfe, K.H. et al. (2018) TPP riboswitch‐dependent regulation of an ancient thiamin transporter in Candida. PLoS Genetics, 14, e1007429.
Garavito, M.F., Narváez‐Ortiz, H.Y. & Zimmermann, B.H. (2015) Pyrimidine metabolism: dynamic and versatile pathways in pathogens and cellular development. Journal of Genetics and Genomics, 42, 195–205.
Giovannoni, S.J. (2017) SAR11 bacteria: the most abundant plankton in the oceans. Annual Review of Marine Science, 9, 231–255.
Giovannoni, S.J., Bibbs, L., Cho, J.‐C., Stapels, M.D., Desiderio, R., Vergin, K.L. et al. (2005) Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature, 438, 82–85.
Giovannoni, S.J., Tripp, H.J., Givan, S., Podar, M., Vergin, K.L., Baptista, D. et al. (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science, 309, 1242–1245.
Greco, W.R. & Hakala, M.T. (1979) Evaluation of methods for estimating the dissociation constant of tight binding enzyme inhibitors. The Journal of Biological Chemistry, 254, 12104–12109.
Grote, J., Thrash, J.C., Huggett, M.J., Landry, Z.C., Carini, P., Giovannoni, S.J. et al. (2012) Streamlining and core genome conservation among highly divergent members of the SAR11 clade. MBio, 3, 00252‐212.
Gutowska, M.A., Shome, B., Sudek, S., McRose, D.L., Hamilton, M., Giovannoni, S.J. et al. (2017) Globally important haptophyte algae use exogenous pyrimidine compounds more efficiently than thiamin. MBio, 8, e01459‐01417.
Haughton, B.G. & King, H. (1958) Toxopyrimidine phosphate as an inhibitor of bacterial enzyme systems that require pyridoxal phosphate. Biochemical Journal, 70, 660–665.
Henriquez, T., Wirtz, L., Su, D. & Jung, H. (2021) Prokaryotic solute/sodium symporters: versatile functions and mechanisms of a transporter family. International Journal of Molecular Sciences, 22, 1–21.
Hernandez‐Plaza, A., Szklarczyk, D., Botas, J., Cantalapiedra, C.P., Giner‐Lamia, J., Mende, D.R. et al. (2023) eggNOG 6.0: enabling comparative genomics across 12 535 organisms. Nucleic Acids Research, 51, D389–D394.
Hunter, S. & Provasoli, L. (1964) Nutrition of algae. Annual Review of Plant Physiology, 15, 37–56.
Jurgenson, C.T., Begley, T.P. & Ealick, S.E. (2009) The structural and biochemical foundations of thiamin biosynthesis. Annual Review of Biochemistry, 78, 569–603.
Kraft, C.E. & Angert, E.R. (2017) Competition for vitamin B1 (thiamin) structures numerous ecological interactions. The Quarterly Review of Biology, 92, 151–168.
L'Annunziata, M.F., Tarancón, A., Bagán, H. & García, J.F. (2020) Chapter 6‐liquid scintillation analysis: principles and practice*. In: L'Annunziata, M.F. (Ed.) Handbook of radioactivity analysis, Fourth edition. Academic Press, pp. 575–801.
Llavero‐Pasquina, M., Geisler, K., Holzer, A., Mehrshahi, P., Mendoza‐Ochoa, G.I., Newsad, S.A. et al. (2022) Thiamine metabolism genes in diatoms are not regulated by thiamine despite the presence of predicted riboswitches. The New Phytologist, 235, 1853–1867.
McRose, D., Guo, J., Monier, A., Sudek, S., Wilken, S., Yan, S. et al. (2014) Alternatives to vitamin B1 uptake revealed with discovery of riboswitches in multiple marine eukaryotic lineages. The ISME Journal, 8, 2517–2529.
Meyer, M.M., Ames, T.D., Smith, D.P., Weinberg, Z., Schwalbach, M.S., Giovannoni, S.J. et al. (2009) Identification of candidate structured RNAs in the marine organism ‘Candidatus Pelagibacter ubique’. BMC Genomics, 10, 268.
Monteverde, D.R., Gómez‐Consarnau, L., Suffridge, C. & Sañudo‐Wilhelmy, S.A. (2017) Life's utilization of B vitamins on early earth. Geobiology, 15, 3–18.
Morris, R.M., Rappé, M.S., Connon, S.A., Vergin, K.L., Siebold, W.A., Carlson, C.A. et al. (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature, 420, 806–810.
Noell, S.E., Barrell, G.E., Suffridge, C., Morré, J., Gable, K.P., Graff, J.R. et al. (2021) SAR11 cells rely on enzyme multifunctionality to metabolize a range of polyamine compounds. M bio, 12, e01091‐01021.
Noell, S.E. & Giovannoni, S.J. (2019) SAR11 bacteria have a high affinity and multifunctional glycine betaine transporter. Environmental Microbiology, 21, 2559–2575.
Noell, S.E., Hellweger, F.L., Temperton, B. & Giovannoni, S.J. (2023) A reduction of transcriptional regulation in aquatic oligotrophic microorganisms enhances fitness in nutrient‐poor environments. Microbiology and Molecular Biology Reviews, 87, 1–27.
Paerl, R.W., Bertrand, E.M., Allen, A.E., Palenik, B. & Azam, F. (2015) Vitamin B1 ecophysiology of marine picoeukaryotic algae: strain‐specific differences and a new role for bacteria in vitamin cycling. Limnology and Oceanography, 60, 215–228.
Paerl, R.W., Bertrand, E.M., Rowland, E., Schatt, P., Mehiri, M., Niehaus, T.D. et al. (2018) Carboxythiazole is a key microbial nutrient currency and critical component of thiamin biosynthesis. Scientific Reports, 8, 5940.
Paerl, R.W., Sundh, J., Tan, D., Svenningsen, S.L., Hylander, S., Pinhassi, J. et al. (2018) Prevalent reliance of bacterioplankton on exogenous vitamin B1 and precursor availability. PNAS Nexus, 115(44), E10447–E10456.
Provasoli, L. & Carlucci, A.F. (1974) Vitamins and growth regulators.
Rapala‐Kozik, M. (2011) Vitamin B1 (thiamine): a cofactor for enzymes involved in the main metabolic pathways and an environmental stress protectant. In: Advances in botanical research. New York: Academic Press, pp. 37–91.
Reddick, J.J., Saha, S., Lee, J.‐M., Melnick, J.S., Perkins, J. & Begley, T.P. (2001) The mechanism of action of bacimethrin, a naturally occurring thiamin antimetabolite. Bioorganic & Medicinal Chemistry Letters, 11, 2245–2248.
Robbins James, C. & Oxender Dale, L. (1973) Transport Systems for Alanine, serine, and glycine in Escherichia coli K‐12. Journal of Bacteriology, 116, 12–18.
Rogers, E.F. (1970) [44] Thiamine antagonists. In: Methods in enzymology, Vol. 18, Part A. Academic Press, pp. 245–258. Available from: https://doi.org/10.1016/0076-6879(71)18312-7
Russell, J.B. (1990) Low‐affinity, high‐capacity system of glucose transport in the ruminal bacterium Streptococcus bovis: evidence for a mechanism of facilitated diffusion. Applied and Environmental Microbiology, 56, 3304–3307.
Sañudo‐Wilhelmy, S.A., Gómez‐Consarnau, L., Suffridge, C. & Webb, E.A. (2014) The role of B vitamins in marine biogeochemistry. Annual Review of Marine Science, 6, 339–367.
Sarhan, F., Houde, M. & Cheneval, J. (1980) The role of vitamin B12 binding in the uptake of the vitamin by euglena Gracilis: B12 UPTAKE BY euglena. The Journal of Protozoology, 27, 235–238.
Steindler, L., Schwalbach, M.S., Smith, D.P., Chan, F. & Giovannoni, S.J. (2011) Energy starved Candidatus Pelagibacter ubique substitutes light‐mediated ATP production for endogenous carbon respiration. PLoS One, 6, e19725.
Subki, A., Ho, C.L., Ismail, N.F.N., Zainal Abidin, A.A. & Balia Yusof, Z.N. (2020) Identification and characterisation of thiamine pyrophosphate (TPP) riboswitch in Elaeis guineensis. PLoS One, 15, e0235431.
Suffridge, C., Cutter, L. & Sanudo‐Wilhelmy, S. (2017) A new analytical method for direct measurement of particulate and dissolved B‐vitamins and their congeners in seawater. Frontiers in Marine Science, 4, 1–11.
Suffridge, C.P., Bolaños, L.M., Bergauer, K., Worden, A.Z., Morré, J., Behrenfeld, M.J. et al. (2020) Exploring vitamin B1 cycling and its connections to the microbial Community in the North Atlantic Ocean. Frontiers in Marine Science, 7, 1–16.
Suffridge, C.P., Gómez‐Consarnau, L., Monteverde, D.R., Cutter, L., Arístegui, J., Alvarez‐Salgado, X.A. et al. (2018) B vitamins and their congeners as potential drivers of microbial community composition in an oligotrophic marine ecosystem. Journal of Geophysical Research: Biogeosciences, 123(9), 2890–2907.
Tobüren‐Bots, I. & Hagedorn, H. (1977) Untersuchungen über das Transportsystem für Thiamin bei Bacillus cereus. Archives of Microbiology, 113, 23–31.
Tripp, H.J. (2008) Counting marine microbes with Guava Easy‐Cyte 96 well plate reading flow cytometer, Counting marine microbes with Guava Easy‐Cyte 96 well plate reading flow cytometer.
UniProt, C. (2023) UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Research, 51, D523–D531.
Wahlgren, W.Y., Dunevall, E., North, R.A., Paz, A., Scalise, M., Bisignano, P. et al. (2018) Substrate‐bound outward‐open structure of a Na(+)‐coupled sialic acid symporter reveals a new Na(+) site. Nature Communications, 9, 1753.
Watanabe, F., Tamura, Y., Stupperich, E. & Nakano, Y. (1993) Uptake of cobalamin by euglena Mitochondria1. Journal of Biochemistry, 114, 793–799.
Wei, T., Zhao, C., Quareshy, M., Wu, N., Huang, S., Zhao, Y. et al. (2021) A glycolipid glycosyltransferase with broad substrate specificity from the marine bacterium "Candidatus Pelagibacter sp." strain HTCC7211. Applied and Environmental Microbiology, 87, e0032621.
White, A.E., Giovannoni, S.J., Zhao, Y., Vergin, K. & Carlson, C.A. (2019) Elemental content and stoichiometry of SAR11 chemoheterotrophic marine bacteria. Limnology and Oceanography Letters., 4, 44–51.
Wienhausen, G., Dlugosch, L., Jarling, R., Wilkes, H., Giebel, H.A. & Simon, M. (2022) Availability of vitamin B12 and its lower ligand intermediate alpha‐ribazole impact prokaryotic and protist communities in oceanic systems. The ISME Journal, 16, 2002–2014.
Winkler, W., Nahvi, A. & Breaker, R.R. (2002) Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature, 419, 952–956.
Yamada, K. & Kawasaki, T. (1980) Properties of the thiamine transport system in Escherichia coli. Journal of Bacteriology, 141, 254–261.
Zilles, J.L., Croal, L.R. & Downs, D.M. (2000) Action of the thiamine antagonist bacimethrin on thiamine biosynthesis. Journal of Bacteriology, 182, 5606–5610.