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Title: Effect of Aggregation and Molecular Size on the Ice Nucleation Efficiency of Proteins

Journal Article · · Environmental Science and Technology

Aerosol acts as ice-nucleating particles (INPs) by catalyzing the formation of ice crystals in clouds at temperatures above the homogeneous nucleation threshold (-38 °C). In this study, we show that the immersion mode ice nucleation efficiency of the environmentally relevant protein, ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), occurs at temperatures between -6.8 and -31.6 °C. Further, we suggest that this range is controlled by the RuBisCO concentration and protein aggregation. The warmest median nucleation temperature (-7.9 ± 0.8 °C) was associated with the highest concentration of RuBisCO (2 × 10–1 mg mL–1) and large aggregates with a hydrodynamic diameter of ~103 nm. We investigated four additional chemically and structurally diverse proteins, plus the tripeptide glutathione, and found that each of them was a less effective INP than RuBisCO. Ice nucleation efficiency of the proteins was independent of the size (molecular weight) for the five proteins investigated in this study. In contrast to previous work, increasing the concentration and degree of aggregation did not universally increase ice nucleation efficiency. RuBisCO was the exception to this generalization, although the underlying molecular mechanism determining why aggregated RuBisCO is such an effective INP remains elusive.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE; National Science Foundation (NSF)
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
2324015
Journal Information:
Environmental Science and Technology, Journal Name: Environmental Science and Technology Journal Issue: 10 Vol. 58; ISSN 0013-936X
Publisher:
American Chemical Society (ACS)Copyright Statement
Country of Publication:
United States
Language:
English

References (85)

Quantitative Evaluation of Experimental Results an the Heterogeneous Freezing Nucleation of Supercooled Liquids journal April 1971
Ice-nucleating proteins are activated by low temperatures to control the structure of interfacial water journal February 2021
Prediction of Amyloid Fibril-forming Proteins journal December 2000
Toward Understanding Bacterial Ice Nucleation journal January 2022
Ice-nucleating bacteria control the order and dynamics of interfacial water journal April 2016
Self-Assembly of Amyloid Fibrils That Display Active Enzymes journal June 2014
Ice nucleation catalyzed by the photosynthesis enzyme RuBisCO and other abundant biomolecules journal February 2023
The ice-nucleating activity of Arctic sea surface microlayer samples and marine algal cultures journal January 2020
How Size and Aggregation of Ice-Binding Proteins Control Their Ice Nucleation Efficiency journal April 2019
Distinct stress conditions result in aggregation of proteins with similar properties journal April 2016
Lignin's ability to nucleate ice via immersion freezing and its stability towards physicochemical treatments and atmospheric processing journal January 2020
What Governs Protein Content of Pollen: Pollinator Preferences, Pollen–Pistil Interactions, or Phylogeny? journal November 2000
Fragmentation of monoclonal antibodies journal May 2011
Large Structures at High Resolution: The 1.6 Å Crystal Structure of Spinach Ribulose-1,5- Bisphosphate Carboxylase/Oxygenase Complexed with 2-Carboxyarabinitol Bisphosphate journal May 1996
Structure and Protein-Protein Interactions of Ice Nucleation Proteins Drive Their Activity journal June 2022
The effect of (NH4)2SO4 on the freezing properties of non-mineral dust ice-nucleating substances of atmospheric relevance journal October 2021
Immersion freezing of birch pollen washing water journal January 2013
Contrasting Behavior of Antifreeze Proteins: Ice Growth Inhibitors and Ice Nucleation Promoters journal February 2019
Ice nucleation active bacteria in precipitation are genetically diverse and nucleate ice by employing different mechanisms journal July 2017
Ice nucleation by viruses and their potential for cloud glaciation journal July 2021
On the pH Dependence of Protein Stability journal May 1993
Ice Nucleation Induced by Pseudomonas syringae journal September 1974
Ocean Aerobiology journal October 2021
The protofilament structure of insulin amyloid fibrils journal July 2002
Evaluating the potential for Haloarchaea to serve as ice nucleating particles journal June 2021
Bovine and human insulin adsorption at lipid monolayers: a comparison journal July 2015
Ice Nucleation Activity in Fusarium acuminatum and Fusarium avenaceum journal September 1992
The crystal structure of bovine bile salt activated lipase: insights into the bile salt activation mechanism journal September 1997
DLS and zeta potential – What they are and what they are not? journal August 2016
Size-resolved characterization of the polysaccharidic and proteinaceous components of sea spray aerosol journal April 2017
Contribution of soil algae to the global carbon cycle journal February 2022
Overview of Ice Nucleating Particles journal January 2017
Efficiency of immersion mode ice nucleation on surrogates of mineral dust journal January 2007
The importance of feldspar for ice nucleation by mineral dust in mixed-phase clouds journal June 2013
Rubisco forms a lattice inside alpha-carboxysomes journal August 2022
The use of dynamic light scattering and Brownian microscopy to characterize protein aggregation journal May 2011
Protein aggregation—Pathways and influencing factors journal May 2010
Isolation of subpollen particles (SPPs) of birch: SPPs are potential carriers of ice nucleating macromolecules journal October 2021
Marine microgels as a source of cloud condensation nuclei in the high Arctic journal August 2011
A marine biogenic source of atmospheric ice-nucleating particles journal September 2015
Suspendable macromolecules are responsible for ice nucleation activity of birch and conifer pollen journal January 2012
Ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RuBisCO): A long‐lived protein in the deep ocean journal May 2012
Predicting global atmospheric ice nuclei distributions and their impacts on climate journal June 2010
Size of bacterial ice-nucleation sites measured in situ by radiation inactivation analysis journal March 1988
Heterogeneous freezing of ice on atmospheric aerosols containing ash, soot, and soil journal January 2009
Microphysics of Clouds and Precipitation journal January 1998
Transfer of labile organic matter and microbes from the ocean surface to the marine aerosol: an experimental approach journal September 2017
The Protein Data Bank journal January 2000
Ice Nucleation by Marine Aerosols Over the North Atlantic Ocean in Late Spring journal February 2020
The adsorption of fungal ice-nucleating proteins on mineral dusts: a terrestrial reservoir of atmospheric ice-nucleating particles journal January 2016
Glutathione: Overview of its protective roles, measurement, and biosynthesis journal February 2009
A comprehensive characterization of ice nucleation by three different types of cellulose particles immersed in water journal January 2019
Dynamic light scattering: a practical guide and applications in biomedical sciences journal October 2016
Towards accurate structural characterization of metal centres in protein crystals: the structures of Ni and Cu T 6 bovine insulin derivatives journal December 2013
The global mass and average rate of rubisco journal February 2019
Intercomparing different devices for the investigation of ice nucleating particles using Snomax ® as test substance journal January 2015
Ice nucleation from aqueous NaCl droplets with and without marine diatoms journal January 2011
Live oak pollen as a source of atmospheric particles journal December 2022
Mixed-Phase Clouds: Progress and Challenges journal January 2017
Sources of organic ice nucleating particles in soils journal January 2016
Protein aggregates nucleate ice: the example of apoferritin journal March 2020
Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships journal June 2007
Ice nucleation activity in the widespread soil fungus Mortierella alpina journal January 2015
Addressing the ice nucleating abilities of marine aerosol: A combination of deposition mode laboratory and field measurements journal May 2016
Pollen Emissions of Subpollen Particles and Ice Nucleating Particles journal April 2023
Ice-Nucleating and Antifreeze Proteins Recognize Ice through a Diversity of Anchored Clathrate and Ice-like Motifs journal March 2018
Impacts of Lipase Enzyme on the Surface Properties of Marine Aerosols journal June 2018
Stimulation of ice nucleation by marine diatoms journal December 2010
The K+-Dependent and -Independent Pyruvate Kinases Acquire the Active Conformation by Different Mechanisms
  • Ramírez-Silva, Leticia; Hernández-Alcántara, Gloria; Guerrero-Mendiola, Carlos
  • International Journal of Molecular Sciences, Vol. 23, Issue 3 https://doi.org/10.3390/ijms23031347
journal January 2022
Ice Nucleation Activity and Aeolian Dispersal Success in Airborne and Aquatic Microalgae journal November 2018
Investigating the Heterogeneous Ice Nucleation of Sea Spray Aerosols Using Prochlorococcus as a Model Source of Marine Organic Matter journal December 2018
Technical Note: A proposal for ice nucleation terminology journal January 2015
Oxidative Processing Lowers the Ice Nucleation Activity of Birch and Alder Pollen journal February 2018
Ice nucleation by cellulose and its potential contribution to ice formation in clouds journal March 2015
Ice nucleation by particles immersed in supercooled cloud droplets journal January 2012
Characterization of airborne ice-nucleation-active bacteria and bacterial fragments journal May 2015
Kinetic and X-ray structural studies of three mutant E. coli alkaline phosphatases: insights into the catalytic mechanism without the nucleophile ser102 1 1Edited by D. C. Rees journal April 1998
Novel dimeric β-helical model of an ice nucleation protein with bridged active sites journal January 2011
Influence of Biogenic Organics on the Chemical Composition of Arctic Aerosols journal October 2019
Structure of Rubisco fromArabidopsis thalianain complex with 2-carboxyarabinitol-1,5-bisphosphate journal January 2018
BINARY: an optical freezing array for assessing temperature and time dependence of heterogeneous ice nucleation journal January 2015
Analytical Challenges Assessing Protein Aggregation and Fragmentation Under Physiologic Conditions journal September 2021
Ice nucleation by water-soluble macromolecules journal January 2015
The Earth’s Energy Budget, Climate Feedbacks and Climate Sensitivity book July 2023
Kinetics of the thermal inactivation and aggregate formation of rabbit muscle pyruvate kinase in the presence of trehalose journal October 2009