Whole cell affinity for 4‐amino‐5‐hydroxymethyl‐2‐methylpyrimidine (HMP) in the marine bacterium Candidatus Pelagibacter st. HTCC7211 explains marine dissolved HMP concentrations

• Published in: Environmental microbiology reports Vol. 16; no. 5; pp. e70023 - n/a
• Main Authors: Brennan, Elizabeth, Noell, Stephen, Davis, Edward W., Giovannoni, Stephen J., Suffridge, Christopher P.
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01.10.2024
• Subjects: Affinity; Alphaproteobacteria - genetics; Alphaproteobacteria - metabolism; aquatic bacteria; Aquatic Organisms - genetics; Aquatic Organisms - metabolism; Auxotrophy; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; biochemical pathways; Biological Transport; Biosynthesis; Candidatus Pelagibacter; Carbon; Carbon cycle; carbon metabolism; Carbon sources; Cell culture; Enzymes; Genes; genome; Growth factors; Kinases; Kinetics; Marine microorganisms; Metabolism; Microorganisms; moieties; Plankton; Precursors; Prokaryotes; Pyrimidines - metabolism; Seawater; Seawater - chemistry; Seawater - microbiology; Sodium; solutes; symporters; thiamin; Thiamine; Thiamine - metabolism; Tritium; Vitamin B; Vitamin B1
• ISSN: 1758-2229; 1758-2229
• DOI: 10.1111/1758-2229.70023

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. Most marine bacterioplankton have an obligate requirement for Vitamin B1's precursor moiety, HMP, and marine dissolved HMP concentrations are remarkably low (approximately 0.1–50 pM). We hypothesized that HMP uptake systems in marine microbes maintain these low ambient HMP concentrations. Our results suggest that HMP uptake by SAR11 bacteria in cell culture (strain HTCC7211) is subject to complex regulation and could explain natural HMP levels in seawater.