In vivo transformations of positively charged nanoparticles alter the formation and function of RuBisCO photosynthetic protein corona

Abstract

The impact of nanomaterial transformations on photosynthetic proteins remains largely unknown. We report positively charged iron oxide (Fe₃O₄) nanoparticles experience transformations in Arabidopsis thaliana plants in vivo that alter the formation and function of RuBisCO protein corona, a key carbon fixation enzyme. In vitro, negatively charged Fe₃O₄ nanoparticles impact the RuBisCO function but not their positively charged counterparts. Computational and in vitro proteomic analyses revealed that positively charged Fe₃O₄ nanoparticles preferentially bind to a RuBisCO small subunit that lacks active carboxylation sites. However, both positively and negatively charged nanoparticles decrease RuBisCO carboxylation activity after experiencing transformations in vivo by 3.0 and 1.7 times relative to the controls, respectively. The pH- and lipid-coating-dependent transformations that occur during nanoparticle transport across plant membranes enhance RuBisCO binding to positively charged nanoparticles affecting its distribution in chloroplasts. Elucidating the rules of how nanoparticle properties and transformations affect photosynthetic coronas is crucial for sustainable nano-enabled agriculture.