Phosphates form spectroscopically dark state assemblies in common aqueous solutions

Joshua S. Straub, Mesopotamia S. Nowotarski, Jiaqi Lu, Tanvi Sheth, Sally Jiao, Matthew P.A. Fisher, M. Scott Shell, Matthew E. Helgeson, Alexej Jerschow, Songi Han

Research output: Contribution to journalArticlepeer-review

Abstract

Phosphates and polyphosphates play ubiquitous roles in biology as integral structural components of cell membranes and bone, or as vehicles of energy storage via adenosine triphosphate and phosphocreatine. The solution phase space of phosphate species appears more complex than previously known. We present nuclear magnetic resonance (NMR) and cryogenic transmission electron microscopy (cryo-TEM) experiments that suggest phosphate species including orthophosphates, pyrophosphates, and adenosine phosphates associate into dynamic assemblies in dilute solutions that are spectroscopically "dark." Cryo-TEM provides visual evidence of the formation of spherical assemblies tens of nanometers in size, while NMR indicates that a majority population of phosphates remain as unassociated ions in exchange with spectroscopically invisible assemblies. The formation of these assemblies is reversibly and entropically driven by the partial dehydration of phosphate groups, as verified by diffusion-ordered spectroscopy (DOSY), indicating a thermodynamic state of assembly held together by multivalent interactions between the phosphates. Molecular dynamics simulations further corroborate that orthophosphates readily cluster in aqueous solutions. This study presents the surprising discovery that phosphate-containing molecules, ubiquitously present in the biological milieu, can readily form dynamic assemblies under a wide range of commonly used solution conditions, highlighting a hitherto unreported property of phosphate's native state in biological solutions.

Original languageEnglish (US)
Article numbere2206765120
Pages (from-to)e2206765120
JournalProceedings of the National Academy of Sciences of the United States of America
Volume120
Issue number1
DOIs
StatePublished - Jan 3 2023

Keywords

  • assembly
  • dark state
  • dehydration
  • phosphate

ASJC Scopus subject areas

  • General

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